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[MUSIC PLAYING] Stanford University Let’s get started Let’s see Once again, game plan for the coming week or so Next three lectures will be the TA overviews– introductions to nervous system, endocrinology Once again– what I emphasized the other day is– if you’re not sure if you’ve got enough background exposure to these topics for it to be worth coming, I would suggest you assume that you don’t Because it could do nothing more than help, even if you’ve had a lot of this before Following that, some more advanced topics in the subject, and then barreling on into the midterm OK Today we leap yet another discipline into yet another one, this one being concerned with basically the same exact issues that we’ve had before– nature, nurture, interaction, behavior And this one, as you will see, with a completely different approach than all the prior ones Now the other day, when going through what heritability means and doesn’t mean, one of the key points that came out at the end was that whole business of, the more different environments you study something in, the lower your heritability term is going to be So what’s one of the punch lines that comes out of that? If you want to understand the genetics of behavior, you’ve got to go look at the behavior in lots of different environments What today’s discipline is about is taking that one step broader If you want to understand anything about the biology of behavior, number one, you want to study it in lots of different environments Number two, you want to study it in as natural of environments as possible And number three, go in there assuming that you are going to have to translate a language The quote at the beginning there, something to the effect of ethology, the field we’ll be looking at today Ethology is the process of interviewing an animal, but in its own language So what we’ll see here is this is an expansion, in a certain way, on that notion that if you want to understand behavior, get your animal out of the laboratory Now to begin to sort of appreciate the context this has in history, we start off– God help us– with history of psychology at around 1900 or so When, universally agreed upon, the Grand Poobah of psychology was William James And all I know about William James is that he was highly philosophical, and I fall asleep every time I try to read the guy But he dominated the period in a way in which psychology was basically an introspective business that was sort of a branch of philosophy And coming out in the decades after that were the Young Turks of psychology, who despised this whole approach, because they wanted to make psychology a science– a quantitative science, an experimental science They wanted numbers Enough of this philosophy stuff And out of it came this very deep, deep reflexive distrust of any behavior you couldn’t see and you couldn’t measure And you didn’t want to know what was going on inside anybody’s personal life, inside their head, whether they were a fish or a human All you were interested in is what was going on in the outside world just before that behavior occurred and what behavior was it Simple organisms as input output black boxes Forget this philosophy stuff Give me something I can measure And this was this emerging discipline of behaviorism, which became the dominant school in American psychology by the middle of the last century We’ve already heard from one of the starting founding fathers of it, and that was John Watson That was the guy from the first lecture– give me a kid from any background, and I’ll turn him into a butcher, baker, candlestick maker sort of thing, and that everything could be controlled in environment And thus, you could shape behavior to any direction you want Behaviorism sort of hit its heyday, its absolute apogee, with its most famous practitioner, who was BF Skinner Skinner– who dominated, I think, most studies show Or that he was the best known, most cited psychologist throughout the middle part of the last century Incredibly influential, and American psychology at the time was all about behaviors What are the key features of it? First one was this hysterical, radical, extreme environmentalism The notion that we are all table rases, whatever that is That we are all blank slates and all that we come in with is this blank slate to be written on by environment

Don’t tell me about genes Don’t tell me about biology at all Don’t tell me about anything other than what’s going on in the environment, and how does that shape the behavior coming out the other end, and can I measure it? Extreme radical environmentalism in terms of gene environment There were no genes There were no interactions as far as they were concerned The next building principal was this notion of reinforcement theory Let me control when any given organism receives a positive reinforcement, a reward Let me control when it receives a negative reinforcement of punishment Give me the ability to control those in the environment, and I will produce any behavior you want in that organism Once again, whether it is a fish or a human and everything in between, this utter reliance on behavior is shaped by the rewards and punishments of environment Reinforcement theory The final piece of it was this notion of universality Which is, it works this way in everybody! It works this way in every single species out there And if you want to study lab rats, you’re going to learn the exact same thing as if you were studying giraffes But it’s a lot harder to study them in a lab You sure don’t need to study them out in their natural habitat, because it’s just understanding the reinforcements coming in, the behavior coming out the other end They’re all the same This period dominated by the behaviorists was, historically, a total drag Because these guys had just a stranglehold on the field And all of them, like, looked the same If you ever look in one of those time-life books on the history of the mind or whatever, there will be the inevitable picture of BF Skinner with some pigeon And Skinner was like your archetypal out-of-central-casting behaviors He had this inordinately shiny forehead and these big glasses And every picture of him, for some reason, photographers were always forced to kneel down and take a picture of him looming over with his pigeon And everything considered, this was an incredibly frightening looking man And he would then be free to go on with astonishing quotes like, dog, cat, rat, child, doesn’t matter It’s all the same This notion of universality of behaviorism And Skinner invented all sorts of Utopian societies– one, a book of his that was very influential, a novel called Walden Two You can build a perfect world out of reinforcement theory all with environmentalism And I could have built the exact same utopia studying this with grasshoppers as with humans– boy, cat, dog, rat, whatever They’re all the same So the building of American behaviorism– utter reliance on environmentalism, utter reliance on the notion that all of behavior could be explained– could be shaped by the rewards and punishments, the positive and negative reinforcements of environment And this works the same way in every single type of animal out there, so you might as well just study it in a rat, in a pigeon Those were the two backbones of behaviorist research Because they’re a lot more convenient And you can study it in the lab, because it’s the exact same thing It is purely a function of the environment you’re controlling And you understand that And as long as there is some behavior coming out the other end that you could measure and generate numbers, you are doing scientific psychology, and this is what the whole field was about Meanwhile, over in Europe, there was a totally different tradition emerging And what it has its greatest similarities to is– you know, you read any of these books on the history of evolution, and there’s always this phase of like all of these 19th century British naturalists, where like half of them were Parsons in some Anglican church or whatever They always had to be Parsons And they would always be out trumping around the woods of England with a butterfly net And these were the guys who would come back with a gazillion different types of butterflies This is when butterfly collecting became this obsession with like British, upper middle class and Parsons and stuff who would just go out in the country And what would you do? You would come back, and you would generate these whatevers of all the different types of butterflies and just wallow in the variability That was the main thing of it Look at all these different colors Look at all these different shapes of wings The interpretation at the time of course was, look at all this glorious variability of life and God’s work showing in it But the main thing emotionally that these guys were about was variety– the range of differences, the range of different ways that species could look like

And what this new field was emerging in Europe was ethology What ethology was about was the same exact emotional pulse as in those 19th century Parsons with the butterfly nets But what ethologists would do is go out and collect behaviors And they would come back, and they would just wallow and just be buoyant by all of the different types of behavioral variety And that’s the most important thing So we can see right off the bat, they are not going to be getting along very well with the behaviorists– with the rat equals boy equals hippo business there Because what these guys were all about was just the sheer variety of behavior and, implicit in that, how you have to study it in natural environments So there were three guys during this period, beginning work early in the 20th century, who were the official godfathers of the whole field of ethology One was Niko Tinbergen Next was Konrad Lorenz The next was Hugo Von Frisch And these were the big three They eventually got their Nobel prizes And Tinbergen was basically a saint, an incredibly sort of accomplished, interesting man who did all sorts of extraordinarily good things Konrad Lorenz, as we know, was Nazi scum And Hugo Von Frisch was just really, really, really old Somehow he was just really old from the very beginning And he was about 89 when he got his Nobel price These were the starting three that began the whole field So we’ve got our archetypal behaviorist villains there with their shiny foreheads leaning over the camera guy and waving pigeons at them And what are the ethologists about? All of them were guys with these knobby knees and very hairy legs, with big thick old hiking boots covered in mud and alpine whatevers And what they were doing was just tromping around in the outside world collecting behaviors, just looking at the sheer variety OK It’s obvious which team I’m rooting for here But even, you know, that they hung out with Konrad Lorenz OK The ethologists are much more nuanced– the much broader, much more multi-faceted, diverse view of life there The ethologists, completely unconnected with behaviorism in the United States Instead, we’re developing this whole field premised on all sorts of very different notions Behaviorists, this radical environmentalism What ethology was about, from day one, was gene environment interactions– behaviorist rules of positive negative reinforcement That explains the entire world As we’ll see, some of the most amazing things ethologists came up with were examples of animals acquiring new behaviors that broke every rule on earth of behaviorism about how learning occurs Finally, over there with the behaviorists, with their universality– cat equals hippo– and what the ethologists were about was, every species solves its environmental challenges, and its history of evolutionary challenges, in a unique way And out of that came Tinbergen’s famous quote Which is, again, ethology is the study of animal behavior, but where you’re interviewing the animal in its own language And the whole premise of ethology was, that’s preferable, and that’s not going to happen unless you’re out there in the nature in the animal’s real habitat And you better be real open minded as to what counts as communication, as what counts to be the animal’s language that you are talking to it with One example of this And this was somewhat of a different discipline, but in the 1960s, there was this very interesting sort of cottage industry of research that came out Which is, you take a normal lab rat And now what you do instead is put it in an enriched environment You put it in a big enclosure with lots of other rats and beeping toys and interesting smells and cell phones and all sorts of sounds of that sort And what they would show was landmark– take a rat and put it in an enriched environment and– in 1960s neurobiology, of a type we’ve heard about already– you get a thicker cortex People went wild over that in terms of enriching the environment This prompted a gazillion studies during the ’60s built around this very Great Society ’60s optimism about things The Head Start program emerged during that period out of a demonstration that all sorts of privations in various points of life, early in life, could be buffered, reversed, by the right sort

of enriched environments Incredibly influential Billions of studies done And hidden away in the literature was one very interesting study Which is, when you took these enrichment sort of Poobahs there– and now, what they did in this one study was they studied wild rats And they brought in wild rats And what they saw was, even without the enrichment– you didn’t need to do a thing about enrichment You take the best environmental enrichment laboratory paradigm to get you the thickest cortex around, and it’s not going to be as thick as in a wild rat And these guys were not– these guys were not ethologists, but this is exactly the sort of thing that ethology is built around You were not going to be seeing normal behavior in a cage, looking at a rat in there That’s like studying dolphins swimming in a bath tub You are going to be missing everything under those And, whoa, there is stuff going on out there If a wild rat has a thicker cortex than we know how to come up with, we need to be studying animals in their natural setting OK So that was their basic sort of call to arms What ethologists worked out were a number a very clear experimental approaches built around a whole bunch of the W questions– who, and what, and where, and why, or whatever it is we did in fifth grade Here’s what they looked at They looked at, first, what was the behavior? What was the behaviors? We’ll see they had a certain jargony term for it– fixed action patterns And what we’ll see about it is this is a very specific realm of types of behavior that had a very interesting subtle relationship with things like instinct Next What in the outside world triggered that behavior to occur? And their jargon stuff, terminology– what was the environmental releasing stimulus that caused this fixed action pattern to come out? Next Dramatically different from where the behaviorists were– what’s going on in that organism’s head so that that releasing stimulus triggers the fixed action pattern to occur? What are the intervening mechanisms? What are the innate releasing mechanism, was the jargon they came up with Very jargony, middle European stuff But what’s going on in an animal’s head? What’s the behavior? What triggered it outside there? What’s the machinery that took that releasing stimulus in the environment and turned it into the behavior? And finally, a realm which connects them with evolution type people, what’s the value? What’s the adaptive value of that behavior? And what we’ll see is that question meant an utterly different world to ethologists than it did to evolution people OK So starting off, those fixed action patterns Fixed action patterns, when you first begin to learn how ethologists thought about it, you immediately sense they’re talking about instincts They’re talking about reflexes They were definitely not And terms like instinct had incredibly dirty connotations among psychologists and animal behaviorists around that time, just because, like an earlier period, animals, humans had instincts for maternal behavior, and instincts for inevitable aggression, and instincts for entrepreneurship, and instincts for– and it was a totally meaningless term, because it described anything that you wanted to say was something that’s supposed to happen and that I’m good at doing What you had instead, in their view, was something much more subtle A fixed action pattern is not maternalism A fixed action pattern is not entrepreneurship A fixed action pattern is a relatively tractable piece of behavior involving a bunch of interconnected muscles and producing this characteristic behavior which had a meaning to it OK Nice and abstract We will see example shortly But what they also had, that separated it from instincts by miles and miles, was animals didn’t have to learn how to do it It was hardwired, but animals had to learn how to do it better And that was an amazing insight in terms of gene environment interactions The word gene was not appearing in their thinking at the time But fixed action patterns In other words, experience could change the way you do the fixed action pattern Or, already harking back to the molecular lecture and that obsession with if/then clauses, what experience mostly would do is not so much change the nature of the fixed action pattern but change the context

Teaching you when to do it, when not to If/then clauses of, if this environmental event is happening, then bring out this cohesive set of behaviors that have at least some superficial resemblance to instinct but doesn’t hold up for long This was really important OK So what would be examples? What does this look like– a behavior where animals simply know how to do it without learning, without experience? And they can do it right from the start and nonetheless experience shapes that Obviously, first example was all of Charlotte’s babies knowing how to say salutations within a few seconds of being born there And no doubt they would soon learn who not to say that to Classic example And this was one that Lorenz studied for years and always wanted to have the pig killed because Nazi scum OK But anyway, I digress And other examples You take a squirrel You take a squirrel that’s been raised in a cage without ever seeing another squirrel– a squirrel that has subsisted on nothing but a liquid diet and that kind of thing And give it a nut, and it will know how to crack it It will know to carry out this fixed action pattern This is not an instinct for food acquisition This is something instinctual for how you hold this thing and where you chew on it or whatever it is that squirrels do It’s in there The squirrel doesn’t have to learn how to do it But what you see is, you take that squirrel without any prior experience with nut cracking, and you look at them over time, and they get better at it! They do it faster They get a larger percentage of whatever’s inside there They have a basic, hardwired fixed action pattern– a bunch of coordinated muscles doing a coherent set behavior, and it is shaped by experience In this case, they learn how to do it better Another example This is one where you have any of those intro psych books from anywhere in 1950s, ’60s or so, and there was this inevitable picture where you had– it was this room There was this surface, and it had a checkerboard linoleum on it And the surface came to around here, and then it dropped down about three feet and then continued the same on the bottom It was always the same checkerboard linoleum Linoleum which was like worth its weight in gold at the time Linoleum which was going to make life better for everyone So you had this checkered linoleum thing there And the critical thing was right around here When the wall dropped down, right here was a sheet of glass that continued out there In other words, the actual floor would continue here on the glass, while it was also dropping down to this And what was always in one of those pictures would be some adorable, cute baby animal sitting out there on the glass, totally freaking out Because it’s out there, and it’s looking way down there, and there’s stuff– a yawning chasm below of three feet– and you are eliciting what was called a visual cliff response Which is, get me out of here! I’m floating up in the air here You did not have to have animals who already had experience by trial and error learning that when you’re floating in the air, that tends not to last for long And you go to [INAUDIBLE] afterward There was no– it’s there in the first place You take a baby dog You take a baby human You take a baby blue whale, whatever And you push them out on the glass there, and they look down, and they totally freak out Unless they’re a baby sloth Oh! Isn’t that kind of interesting? Because if you’re a baby sloth who gets freaked out by yawning space underneath you, you are not going to be a very functioning sloth when you grow up there Oh, species specific fixed action patterns. , Where in this case, this visual cliff could evoke this whole fixed action pattern of panic responses, all of that So where does the learning come in? You push this poor animal out there enough times– the 40th time, the elephant’s out there, and it begins to learn I don’t know what’s up with this, because this gravity business is making sense otherwise But it seems to be OK when I’m out here You could habituate the visual cliff response But all sorts of animals– except for arboreal ones hanging up there– all sorts of species didn’t have to have prior experience with not liking to drop down open spaces It was there already They learn the context better Another example of this that the ethologists showed These were with captive primates You take a monkey who was raised in isolation,

who has never seen another monkey, and at some point in adolescence It’s a male monkey And you sit him down, and you show him a film And the film consists of the face of a huge, scary male monkey of the same species giving a threatening display, which is usually displaying the canines there And this is a monkey who has no prior experience with monkeys It has never seen a monkey before All of its interactions have been with Barney or whatever, knows nothing about any of this And you show it that, and it will freak out and give a fixed action pattern– a subordinate gesture crouching down and not making eye contact Whoa! Where’d that come from? No learning from trial and error It was simply there as a fixed action pattern– a whole bunch of things that the monkey does with its torso, its face, all of that Where does experience come in? The monkey needs to learn that you give a subordinating gesture like that to some big, scary animal, you don’t give it to infants It needs to learn the right social context So that’s where it comes in So you’ve got all these examples of behaviors that are hardwired, whatever that means And what you have, nonetheless, is shaping by experience And this is what the ethologists learned And what was clear after awhile was all sorts of animals already knew all about ethology They understood what a fixed action pattern was As follows Type of monkey in East Africa called vervet monkeys If you were a vervet monkey, there are three things on Earth that terrify you One is a leopard Another is a snake, and the third is an eagle Leopards come from below Snakes come from below Eagles come from above And what you have in vervet monkeys are fixed action patterns of alarm calls that they give when spotting one of the predators They have different alarm calls for each of the species And what has been shown is, you fly over the silhouette of a perfectly nice bird there that’s not going to try to carry it away, and you don’t elicit it It’s not just things going on up there It’s a fixed action pattern for scary, terrifying stuff up above verses scary, terrifying stuff below with four legs, versus scary, terrifying below with no legs at all And they all know how to do this without prior experience But what goes on is the same thing that makes it a fixed action pattern, which is it can be sculpted by experience What am I saying here? Which is, you are a young vervet monkey, and you’ve got these fixed action patterns That’s great! What you have to learn how to do, though, is not screw up and say, oh my god, there’s an eagle, when you actually should be saying, there’s a leopard Because if you say, there’s an eagle, everyone’s going to run down the tree And if you say, there’s a leopard, everybody’s going to run up the tree! And you get some kid who gets it backwards, and that’s going to have some bad consequences How do you know adult vervet monkeys have studied ethology and fixed action patterns? Because they don’t listen to the kid until some adult agrees with them, because they know this is some dumbass kid that doesn’t know the language yet very well and makes mistakes Under a certain age, adult vervets don’t respond to alarm calls other than with vigilance, trying to figure out what the kid’s talking about, until it is seconded by an adult So what about fixed action patterns in humans? Classic example– infant smiling, involving all sorts of muscles that who knows what’s involved in them? All sorts of muscles that produce this without prior experience How do you know? Fiberoptic mysteries show that fetuses smile at various points What else? You will see smiling in blind babies So there’s no visual information coming in What’s smiling? It’s a fixed action pattern Where’s the learning? Learning who to smile at Learning that mannequins aren’t going to smile back at you and things of that sort That’s it being shaped by experience More fixed action patterns Infants are not having to have trial and error experience with learning there’s this thing you do with your mouth right after you’re born that keeps you from being really, really hungry, and it’s called nursing Oh, can somebody demonstrate that for me? That’s a fixed action pattern What happens is, kids get more and more efficient at it– the number of calories they can consume per unit of time They get better at doing it More fixed action patterns in humans Every culture on earth, people raising their eyebrows and greeting to somebody Every culture on earth, people can

recognize what anger looks like, what fear looks like, what disgust, what contempt, all of those These are all fixed action patterns And where does the context come in? With all of them obviously learning when you interpret this as good news, bad news When you pretend you don’t see it, all of that Learning the social context So humans are absolutely full of fixed action patterns Next, the next sort of question that the ethologists would ask after getting to this point of, what’s the behavior– what does learning have to do with it? And now asking the question– the same one the evolutionary folks would ask– which is, well, what’s the benefit of it? What’s the adaptive value? And a totally different way of thinking about it than the evolution people The evolution folks going on with adaptive value, which is it allows you to pass on more copies of your genes And over the generations, the prevalence of that trait becomes more common What the ethologists did instead were experiments They simply went and experimented to see what this information– what these fixed action patterns– actually meant So Tinbergen was famous for one of those Which was there was like some gull something or other that he would study, and the outside of gull eggs were all speckled And there would be this very distinctive fixed action pattern shortly after the chicks pop out, which is mom would go around systematically turning over all the fragments of egg where the white of egg shell– where the white was facing up– and would turn it over so that the speckled part was facing up Whoa! That’s an interesting behavior Does that make that gull more attractive to males and thus pass on more copies of her genes? But, no, here’s what Tinbergen does He goes in with these gulls who just finished doing it and with her new pups, chicks– her new chicks just having hatched And she goes off to get them food or whatever And this total vicious, heartless Tinbergen sneaks in, and he turns the shells back over to white And what happens? All sorts of raptors flying around up there are better at spotting down there that there’s all these baby chicks, who are gone by the time mom comes back Tragically I know! And I’m complaining about Lorenz? [LAUGHTER] OK But that’s showing, oh, why do gull mothers, shortly after giving birth, go through this interesting collection of motoric movements which they don’t have to learn how to do, flipping these things over? Does this make their groups better to out-compete those with the next Ice Age comes? No It’s because you turn it over so that some predator up there in the sky can’t see the egg shells– the adaptive value Next Next example of this– and this is like one of the most famous, iconic sort of stories to come out of ethology– this was the work of Von Frisch showing bee dancing, bee communication And what bees are about is– they’re scary, and they go find out about food sources And they fly back to their colony And what they need to do is communicate to everybody else that they have found a food source And they have to communicate all sorts of types of information Which direction? How far? How much? Is it totally exciting, or is it, I just stumbled into a little bit? And what Von Frisch was able to work out was bees came back and did this fixed action pattern movement which has been seen in every bee species on Earth Which is, they do this figure eight, a waggle dance They’re shaking their rear back and forth And they’re moving over the floor of the hive, where everybody is watching and cheering them on, and going around and doing this figure eight And what is this about? What is this about? Von Frisch was able to dissect it, and with brilliant, experimental tricks showing the bee was giving three pieces of information The axis of the figure eight told the bees, with respect to sunlight, which direction to go to find the source The longer the bee danced, the further away the food source was And the more frantically it was wiggling its rear around, the more exciting of a food source it was This was information This was what’s the adaptive value So Von Frisch is sitting there saying, well, I think it might mean this, because I’m finding this interesting pattern I may speculate What do you do? You do an experiment instead Which is, now you take a beehive, and you put it on a bar stool thing And it’s sitting out there in the field, and you grab some bee And I don’t know how he did it, but he lived to a ripe old age But you grab a bee, and you give it some amazing food source out here, and you let it fly back to the hive

where it goes berserk with the waggle dance stuff, telling everybody there’s something amazing over there Meanwhile, Von Frisch, in his hiking boots, is slithering on his belly towards the beehive with the piano stool, and comes up underneath it, and rotates it– rotates it 180 degrees And what happens then? Everybody in the hive comes barreling out and goes in the wrong direction! Because they were given directions as to where to go with respect to the hive’s entrance That’s how you show it actually contained information And then he would have the food source closer or further, and show the length of the dancing and all sorts of other cruel things he would do to the hive to confuse them and wipe out the credibility of that one bee But this is how you get the information He would show this explicitly– oh, why do they do this fascinating fixed action pattern? Because they’re telling them something! And here’s how you prove it And you rotate it around So you can begin to see the ethologists were really good, clever experimentalists And they were just trying to do it in the animal’s own language This became really clear when you study their next category of questions– that business of, well, what is it that just happened in the outside world that triggered this fixed action pattern to occur? What was the sensory trigger? Their jargon– what was the releasing stimulus? And they had general strategies for doing this OK You were speculating that this site is the thing that triggers whatever this behavior in this animal How do you begin to test it? Let’s remove the– OK, enough with the abstract stuff Baby birds– baby gulls or something– peck at mom’s mouth, at her beak And that is meant to get mom to regurgitate some exciting food How do they know how to do this? What is it that gets them to do this behavior? On mom’s beak, there’s a little red circle And the early ethologists noting that, oh, that’s kind of interesting I wonder if they’re looking at the red circle there? I wonder if that’s the thing that’s causing them to start this behavior? What were the experimental techniques for saying, oh, is a red circle on mom’s beak a releasing stimulus for this fixed action pattern of pecking? Let’s do an experiment And the standard experimental models they would have would be to subtract out the thing that you think is the stimulus Take mom and white out her little red circle there and see if the kids no longer peck Replacement Which is, now you’ve done that to mom And you draw a little red circle back, and you see if they start pecking again Replacement substitution Now you take something completely different You put some neon triangle on mom’s beak, and you see if you will elicit the same– oh, what’s the specificity of it? Finally, the thing that they really specialized in– which is now you would do what they called super stimulation Which is, you wave a piece of paper in front of the chick there– that you’ve drawn a gigantic red circle on– and you see if it goes out of its mind and pecks at it like there’s no tomorrow Experimental approaches like this If you take away this thing, does the fixed action pattern no longer occur? If you put it back, does it work again? If you replace it with something else, if you exaggerate the traits, do you get even more of the behavior? These were the standard approaches for figuring this out And ethology types who were interested in this realm of releasing stimuli, the thing they have gotten incredible mileage out of recent years is making little robotic animals Because you could program to do certain behaviors, and you could see if you could elicit everybody else to respond to the behaviors And, of course, the first ones were all sorts of techie folks building robotic bees who could dance in certain dimensions And they would stick him in there and wind up the gear shaft thing And they would just dance away, and they could get the other bees to go flying off someplace– the bees not being very discriminating as to which dancers they pay attention to But the point there was, this was a substitution– a mechanical substitution for that releasing stimulus Or there’s some amazing paper a couple years ago, where somebody made a robotic cockroach and was able to trick all the other cockroaches into doing some sort of imprudent behavior And so you see this is high tech versions of this approach Oh, it might be this stimulus that’s– let’s replicate it Let’s make it even more exciting So using this approach, the ethologists would begin to figure out, what is it in the sensory world of this animal that caused that fixed action pattern to occur? And it was never more than in this domain that they were doing that whole sound byte about interviewing

an animal in its own language Because what it’s all about is recognizing other species out there are functioning in sensory modalities we can’t even guess at What they began to see One example– the sorts of auditory stimuli that would trigger fixed action patterns One example– deer moose Big things What are they called? Elk! Elk! Is elk a female name for– bulls OK So you get Bullwinkles there And what he’s doing is he is trying to find a mate And how does he do it? What they do, when they use northern Minnesotan beasts, is they bellow They give these bellowing calls that are heard for miles and miles Male deer– I guess it’s deer OK They bellow It could be heard miles away And if you were the right kind of female, and you hear some guy bellowing in the next valley, do you know what you do? You ovulate Auditory induced ovulation And not only that, you begin to go try to find the guy And when you get there, you start this whole courting display thing, if he’s the right kind of guy and he expresses himself And what you have there is– what’s the releasing stimulus? An auditory one Even more bizarre– discovering that rats, rats are responsive to certain types of stimuli For example, you tickle them on their rib cage, and they giggle Yes! Your tax dollars going on that that could instead be spent on nuking something or other What you’ve got there is rats giggle They giggle in an ultrasonic range So you can’t hear it until you’ve got some rat giggle decoder thing And they giggle in response to logical things Like you tickle them, and they giggle And then they come back for more And you show all those patterns with it And if you get it at the right frequency only, and they do this giggling chirping thing, and you’re releasing that there, and other rats come over to check it out Because the sound– the auditory releasing stimulus, in this case of rat chirping giggling– induces this, whoa, let’s go see where the party is response in the other rats Another example of this– interesting thing that you see in various species, including humans– which is when females are ovulating, their voices go a little higher And studies showing that males subliminally can detect this More evidence of modality supplying information we would never even guess at OK Then you can show releasing stimuli in the visual domain And one example of this is that you have turkeys, and turkeys apparently do their sexual attraction stuff visually And this prompted one of the cruelest, most savage studies I’ve ever seen, which is trying to figure out what is it that makes female turkeys attractive to male turkeys And what they did was, they would show the male, and they studied his behavior for a long period And the scientists began to guess at what were the releasing stimuli, the visual information from the female, that would elicit this behavior? So they did the subtraction substitution technique They made themselves an artificial female turkey They took a big old ball of Styrofoam, and they stuck this fake turkey head on at one end And they stuck a bunch of feathery things at the other end and just stuck it out there in the field And, of course, the idiot male turkeys instantly are like all around the thing and courting it And all, oh So interesting visual stimuli What about it actually attracts the male? And here’s where the cruelty came in They would begin to mess with the artificial females And I once saw a film of this And like the empathy you feel for this poor turkey guy there Because they have a– and he comes in there, and they’ve got the Styrofoam female with this stuff there, and he’s courting it and having a great time And now they put him back there, and they do something or other there And he comes out, and the back feathers are kind of perpendicular to the head And that doesn’t– so you see he sort of stops there and kind of circles around for a bit But, being a male, he decides what the hell and starts courting the thing Then they put him back in the room there And now they let him out And the tail and the head are on the same side He stands there, looking a little more confused, before starting to court the thing Put him away, come back in, and the head is over there,

and the feathers are there, and the Styrofoam ball And you see he’s kind of like looking around and goes up to this and– well, that’s not going to work– and goes over to the next one And you’re seeing what the information– can you believe how cruel this was? You could begin to see this sort of information– what were the building blocks of that visual releasing stimulus– in order to find out about that Then there is, not surprisingly, a whole world of olfactory releasing stimuli And we won’t spend any time on that here, because all that stuff is going to come big time in the lectures on sexual behavior– pheromones, information that triggers behaviors, sexual behaviors in all sorts of species, including humans Olfactory information One example with humans, which was this very cool study that was published a couple of months ago What you need is sweat from terrified people So here’s what you do You throw somebody out of an airplane who’s never parachuted before And the whole thing is, I guess you can do your first jump in tandem with the instructor who’s attached to you and who knows what to do The instructor who’s doing all the physical work while you’re just there attached to them being scared out of your pants Then you get a control group– a control group who, instead, have generated stress sweat on an exercise bicycle Totally fine So quick, you get the guys lying down in the field They’re hyperventilating You run at them with cotton swabs, and push his armpits into it, and get some of his sweat, and seal it away And then you get the person on the bicycle, and you get some of their sweat And now you sit down people, and you let them smell the two sources Objectively, people cannot distinguish between them Put the person in a brain scanner, and give them the odors And if they’re smelling the sweat from the terrified person, their amygdala activates Not if you smell the sweat from the other individual And not only that, you now show them faces where the facial expression is ambiguous It’s been sort of merged halfway between a scared appearance and a happy one, between different facial expressions And you get somebody after they’ve smelled the scared sweat, and they interpret faces as more frightened Whoa! Smells? The smells of people’s armpits and whether they were terrified or not changes how your brain is working and changes how you judge pictures of facial expressions We’ve got stuff going on in all sorts of sensory domains that we can’t even begin to guess at Showing this even more, other species where you go into stuff we don’t even know about Electric fish You want to understand releasing stimuli for electric fish, you’ve got to understand electricity, and how they sing to each other in electric fish songs, and how they– where is that coming from? Oh, right, they’re singing to each other in electricity And, yes, you get territorial songs You get specific ones You get males who are courting the same female, trying to jam each other’s frequencies This actually is demonstrated quite readily You see relatedness of frequency patterns between siblings They’re going about this with electricity Whoa! What is happening in the outside world there that we haven’t a clue at interviewing an animal in its own language? Vibration All sorts of insects communicate with each other by vibrating Arachnids, there’s all sorts of things where they communicate– I don’t know what they want to talk about– but by vibrating a web They can produce distinctive patterns of it, which sends information And oh, OK, weirdo insects and spiders and stuff Really interesting work done in recent years, by somebody who used to be here on campus named Caitlin O’Connell-Rodwell, looking at elephants And it turns out elephants have all sorts of interesting pressure transducer receptor little corpuscle thingies in their feet Nobody else has stuff like that in their feet among mammals These are things that are supposed to be in other parts of the body You don’t see them at the bottom of your feet And what are these about? When an elephant walks, it’s causing tiny, tiny bits of vibration in the ground that could be picked up hundreds of yards away And what she has shown experimentally is elephants can communicate with each other with vibration through their feet And she has done some brilliant classical ethology studies of manipulating it and seeing if you could change the elephant They’re talking to each other with vibration All of this very, very different than we would guess Tactile stimulation

And out of this came one of the iconic experiments and one we will come back to lots in lecturers to come This one you’ve also seen every single intro textbook out there, which is the surrogate mother monkeys You got the monkey who’s raised in social isolation, and all he’s got are two surrogate moms to choose from And one has this chicken wire tube torso thing with this little unconvincing Styrofoam head put on top And the other one is wrapped in this nice, warm, terry cloth around its chicken wire torso, with a head on top What’s the difference? The first one, the chicken wire one, has a bottle of milk sticking out That one supplies milk, supplies calories This one supplies warmth And in the mid-1950s, you would ask somebody, well, why do babies like their mothers? Because their mothers positively reinforce them with milk, says BF Skinner, who clearly knows endlessly about that What is bonding between mother and child about? It’s about the mother meeting the caloric and temperature needs of a child By reinforcing the child with milk now and then, the child becomes attached And this is what dominated in the field OK Nice, abstract question Interesting realm where it had an implication– you take an infant, you take a very young child, and you put him in a pediatric ward for a couple of weeks because of some illness And what’s the philosophy at the time, derived from hard-nosed behaviorism? It would say, dog equals cat equals monkey It would say, one person with a bottle of milk equals another person equals another Parents, they don’t know the routines here They never wash their hands enough So what we’re going to do, what was standard practice in pediatric wards at the time, was parents were allowed to visit 30 minutes a week And otherwise, all of the care was provided by people working there And eventually, the best thing ever came along that would make any behaviorist delighted You could do things with infants, keeping them going, without even being touched by human beings Someone modified chicken egg incubators and invented human incubators And an entire just grotesque literature shows the more incubators a hospital had, the shorter the life expectancy was of infants who came in in their ward But that was the dominant notion at the time What do infants like about mom? She gets calories She gives them calories So OK So you’ve got the baby monkey there And she’s got two moms to choose from– the one that gives milk, and the one that has the terry cloth with the tactile stuff And which one is she going to cling to? It’s clear, if you had BF Skinner in there, he’d be up there nursing on the milk bottle within a couple of seconds But what does the baby do instead? Which one does it bond to? The warm, terrycloth mother Ah Love has so much more to do than just calories, and adequate clothing, and a vaccine every now and then This was a study by a man named Harry Harlow which transformed– began to get people to think utterly differently about the nature of bonding We will hear tons about that work down the line So tactile stuff Finally, what is the realm of the most brilliant combination of various releasing stimuli triggering fixed action patterns out the wazoo? What baby animals look like in every species out there short of crocodiles and snakes All the baby animals and all the different species have the little short muzzles, and the big round eyes, and the big shiny forehead, and the big ears sticking out there, and maybe a distinctive coloration that sets them off different from mom, from adults And every species, you take some incredibly cute baby monkey, and polar bears are going to say, oh, look how cute! And their eyes are going to dilate, their pupils, and you are going to elicit cute responses The term, this set of fixed action patterns that people and all sorts of species do in response to the releasing stimuli of a cute baby And, I kid you not, the early generations of Disney illustrators studied this They studied what it is that makes baby faces baby And an amazing paper, classic one by Stephen Jay Gould, talking about Mickey Mouse, the evolution of Mickey Mouse If you go back to when Mickey Mouse started off in, I don’t know, the 1920s or so, his name was Steamboat Willie And he was this rat He was this like skinny, angular, ectomorph rat thing with five fingers

And he was basically sort of this double entendre-ing sort of mildly sexual aggressive beast, who was always ripping people off And somehow he turned from that into our Mickey, who delights people And what Gould showed was– in this paper, he actually showed the evolution of Mickey Mouse’s muzzle as over the decades, showing how it was getting smaller, and the ratio of the forehead to this And somewhere along the way, Mickey lost one of his fingers And somewhere along the way, his voice got real prepubescent, which it wasn’t early on And suddenly, the oh so chased mysterious Minnie shows up, and all they ever do is sing and dance And this is an amazing paper on how the Disney artists eventually learned what is it about baby animals that makes everybody want to be around them So we see here the releasing stimuli Next thing, after the break, what’s going on in the head in between the releasing stimulus, and out comes the fixed action pattern OK So five minutes Two great questions The first one, going back to Niko Tinbergen’s attempts to get baby gulls eaten– that whole business about flipping the eggshells over Somebody asking, so why haven’t eggs and birds and stuff evolved so that the inside of the egg shell is speckled also? And the answer is, I haven’t a clue Does anybody know why? Is there some good reason why the inside of egg shells have to be white? Calcium or– well, there’s got to be some good reason But you go out and test that OK So that would have been an interesting study I have no idea why The other one, of the same sort of bent of the, how do they figure this out– how do they figure out that human males can detect, like the sound of women’s voices when they rise around the time of ovulation? What you do is you record voices, and then you manipulate the pitch that it’s at And this is a very subtle effect, but people listen to it And if they’re men and they listen to it, on the average, they will rate the voices that are a little bit higher as more appealing We will hear plenty about stuff like that down the line OK So what do we got so far? We have looked at interviewing an animal in its own language and asking what the behavior is about– the effect of experience on the behavior Looking at what’s going on in terms of adaptive value in a totally different way than the evolutionary folks would be looking at Looking at what– in the outside world, what releasing stimulus triggered the behavior Huge take home message there being animals, including us, are communicating information in sensory realms we could never even guess at– interviewing in its own language And also, along the way there, training ethologists to come up with really clever, cool, elegant experiments So the next step What’s going on here between when the releasing stimulus happens, and out pops the behavior from the other side? Old ethology jargon– what is the innate releasing mechanism? Which is like this really unfortunate phrase But what’s going on inside? And it was right around this point that all the classical ethologists would say, we don’t know! It’s obviously important, but we’re not able to understand it And that has changed now And what that field is called is neuroethology And that is the hottest part of the field in the last few decades, trying to understand what’s going on in the brain that turns certain releasing stimuli into behaviors out the other end And there have been some amazing successes in this realm in terms of working out the nuts and bolts of it One example, the one that’s probably the most studied, which is understanding the neurobiology of birdsong Bird song– how does a bird learn its species specific song? How does a bird learn one that winds up being distinctive for itself? What happens to birds that have to come up with a new song every year, because they’re seasonal breeders in a way where they’re migrating around? How do they learn that? What sort of sensory stimulation do they need from around them? If you raise a bird in complete isolation, does it come up with a song which is exactly what its species does? No, but it’s kind of close to it It needs experience to shape it What’s going on in bird species like [INAUDIBLE] birds that imitate the sounds of other birds? And people have been dissecting this down to the individual neurons for years, understanding what’s going on in between Another domain that seems far more inexplicable for why people would want to spend decades on it is– for people who took Bio core, I always go over this one– a reflex

A reflex you find in female hamsters Which is you get a female hamster, and you put pressure, tactile pressure, on her rear end And what she will do is arch her back at that point and produce what is called a lordosis reflex So what’s that about? It’s obviously a fixed action pattern Let’s ask an adaptive question What’s the advantage of having a lordosis reflex? What it does is, by arching up that way, it exposes the female’s genitals, making it easier for a male to mount her Well, when is that useful for the female? If she’s ovulating You only get this reflex when estrogen levels are elevated And adaptive value of that built around the fact that most things that are pressing on the rear end of female hamsters are not grad students trying to get their degree eventually [INAUDIBLE] ethologically relevant context, that’s part of the mating courtship display stuff And there is a guy I know who is the king– the king of pressing on the rear end of female hamsters People will not be able to talk about the behavior for centuries to come without his name being sung about there And he and his lab have gotten it down to individual neurons in the whole reflex pathway, and which neurons are affected by estrogen, and how exactly it works– neuroethology Another realm of it, of neuroethology, is one done with humans these days– taking advantage of brain scanning techniques, and seeing what sort of subliminal sensory information you give someone, and what parts of the brain change their levels of activity And the scared sweat versus the neutral sweat study is a perfect example of that, and we will hear plenty of those in the lectures to come As neuroethology really took off, an additional elaboration happened, which is people began to try doing neuroethology out in the field with animals in their real habitat Because all the ones I just described were the laboratory animals trying to do it out in the field, and there’s been a number of approaches One is, people– a guy named John Wingfield used to be at the University of Washington John Wingfield studies birds And I have no idea if he ever actually wanted to study birds or if he was fated to do this from the start But what he does is, he studies the physiology and the behavior of bird species that migrate from Baja up to the Arctic each year and back again Bird species where what happens with their migratory behavior, if there’s an extra freeze that’s unexpected, if spring comes earlier, what are the– and he traps these birds He nets them, and he’s got like electrodes in their heads, and lets them go to fly off to Alaska, recording from there And this is neuroethology stuff– figuring out the circuitry going on precisely with that, with birds in their natural setting Another example, which is some of the work I’ve done over the years, which is studying baboons out in their natural habitat and trying to do ethology, neuroethology stuff, out there What, for example, does your personality– if you were a baboon– have to do with the brain chemistry of anxiety in you? You remember the stuff by now, benzodiazepines and the benzodiazepine receptors Are there personality related differences in the brain chemistry of benzodiazepines in baboons out there And you can squeeze out a surprising amount of information All of this is part of the transition back when of saying, well, something has to be going on in between there You’re a behaviorist, and you say, who cares? You’re an ethologist, and you would say, wouldn’t it be great that someday we’re going to be able to study it? And what the neuroethologist actually can do is study it and begin to work out circuitry maps and all of that, what’s going on inside Interviewing the brain of an animal in its own language Because– as you will see in some of the anatomy, neuroanatomy lectures to come– you’re not going to make any sense about which parts of the brain are big, and send projections to which other parts, until you know something about the behavior of that species and what sort of sensory systems it pays attention to OK So these are sort of the big pieces of the ethological approach What’s the behavior? What triggered it? What are the intervening neuro endo steps in there? What’s the adaptive value? What was also the final piece of the ethological approach was, what does learning have to do with all of this? We already know that learning is relevant in terms of those fixed action patterns But exploring learning in all sorts of additional ways And the ethological contribution to that field is basically twofold The first would be boring, classical, sort of behaviorist type learning paradigms that behaviorists had explained centuries before

What was interesting, showing it in domains of animal behavior, where everybody else would have said, they have to learn how to do that? That’s not an instinct? Showing realms of traditional learning that were very unexpected The second piece was showing types of learning that break every rule about how learning works if you’re a behaviorist OK So what would be a standard example of normal learning? You get reinforced, you’re more likely to do something You get punished, you’re less likely The whole song and dance there Where does just plain old normal learning– learning from trial and error– come in in places that one would not expect? If you are a female monkey, it is not instinctual for you to know what you’re doing with your first baby Maternal competence is not a strong instinct It does not produce a bunch of fixed action patterns in, for example, female rhesus monkeys They have to learn how to do it They have to learn how to hold on to the kid when they’re jumping up in a tree They have to learn which end you try to stick on to the nipple You have to learn all sorts of stuff like that Weird All of my kids starved to death, but then today I tried switching this one around this way Isn’t that cool? Anybody know Niko Tinbergen’s email address? What you wind up seeing there is they have to learn how to do it So what sort of evidence would you see? For example, you have mothers having a higher likelihood of their kids surviving as you go from their first offspring to later ones OK But maybe you can come up with all sorts of other things going on there What else do researchers find? If you have a big sister, and you are a female rhesus monkey– or a female baboon, it’s been shown as well If you have a big sister who has a baby, when you have your first baby, your child is more likely to survive How come? Because you watched her You watched your big sister doing it Or if your mother had another sister, another daughter, and you got to– no, another child of either sex– and you got to watch, what was even more clear in the literature was the more experience you had actually holding on to your niece or nephew there, the more– as termed in the field now– the more [INAUDIBLE] behavior that you had, the more likely your first child was to survive Because you were learning how to be a competent mother as a primate, as a monkey It’s not, oh, instinctual They just know how to do it It’s all hardwired somehow This is a realm where you have to learn Another domain where this happens, and another one where what you would immediately say is, wait, they didn’t do this just by reflex or instinctually? Meerkats– meerkats who eat all sorts of unlikely things And one of the things they eat are scorpions And mom meerkats have to teach the kids how to hunt and eat scorpions without getting yourself in trouble there What is shown– like teaching techniques, they would be teaching three blocks away in the Ed school, in terms of progressively making the task harder in small increments What happens? The meerkat mom goes and kills a scorpion And for the first couple of days, the baby learns how to eat a scorpion that’s already dead Then, once the kid has that under control, the mom goes and captures a scorpion Which remains alive, but mom is able to bite off the stinger, and now leaves the kid with this live scorpion that it can learn how to hunt, and learn how to kill, and get food And only when they’re doing that, then mom captures a live scorpion with the stinger still on and plops it down for the kid This is exactly what they teach you to do if you’re being a good teacher Which is a nice, small, incremental steps You don’t want to do the same thing for too long The kid gets bored You don’t want to have too big of steps They get learned helpless And you just– they’re teaching their kids how to hunt, because the kids don’t know how to do it Perfectly clear example of classical learning, but in a domain where nobody thought it would be going on Another example of it– and this is one where the behavior itself was so unlikely that nobody would ever have been saying, oh, animals just know instinctually how to do this, because nobody believed this behavior could occur– which is animals making tools This has been shown in a number of species, including, for example, cetaceans Where it’s been best studied is in apes Other ape species Actually, we make tools, too So all of the ape species And Jane Goodall, pioneer of chimp research, was the first one to discover this– chimps being able to strip the little bark and stuff off of a long twig

and insert it into a termite mound and pull it up with all the termites that grabbed onto the stick when it was down there And now being able to eat the termites And chimps, various types of populations of chimps, they use tools to hammer, to break open nuts They know how to use a hammer and anvil They get a flat rock, and they do this with this All sorts of tool making and tool using As we will hear, there is at least one population of chimps that has been studied where males will actually fashion large pieces of wood– Where they will work to modify it, to use it as a weapon They can build tools that are weapons So what’s going on with that? And all sorts of studies showing, for example, the more experience you have sitting and watching somebody else make these things, the faster you’re going to master it But you actually want hands on practice The more the individual, the other chimp, gives you the building blocks of it to start doing the piece and all of that, and you begin to master it learning by experience One thing that is very amusing is that it has been shown that chimps, the daughters learn much, much faster than the sons Because the sons don’t pay attention to mom when she’s sitting there and trying to get them with their hands to do this The daughters are much more attentive What you also see is, the larger the social group, the earlier in life the kids learn the tool use And this is brilliant ape behavior, brilliant ape learning Monkeys don’t do this I have seen baboons– films of them, actually I have seen baboons on films where they are watching these chimps doing the thing with the stick there, and going down, and out come the termites And do it again and again And finally, the chimp is just gorged with all the termites and staggers off for a nap And the baboon comes over and will pick up the stick and shake it at the termite mound or push it against the side of it Monkeys can’t do this Apes can, but they don’t do it instinctually They gotta learn how to do this So another domain of learning– learning purely of the, we know how this works, we just didn’t think it would be going on in this realm But then, what ethology has been most amazing at is showing types of learning that are simply unexpected, that break all the classic rules of reinforcement theory One example One example of it is what is now called one trial learning Which is another term that I think I used the other day, the one that’s sort of more– sort of a classic that everybody learned back when, that animals will imprint on something after one round of exposure to it And the classic example would be Konrad Lorenz and his famous little duckies That when birds come out, there is a short period after which where they imprint on any big thing moving around, on a fairly safe assumption that, in most cases, that big thing is going to be mom That’s how they bond to mom There is a short window, what is now known as a critical period, where the bonding goes on during that time And whatever big thing is moving around– and eventually, people were doing classic ethology studies with subtraction and substitution of stimuli and running around with like a stuffed Big Bird And they imprint on that, and all sorts of large mobile objects– basically anything that moves And that’s where you would get all the little duckies, goose stepping behind Konrad Lorenz when they had imprinted on him And this is not by trial and error Oh, I initially got bonded to this thing with sharp teeth and claws And that was kind of a bummer That involved all sorts of blood loss So I’ve learned, don’t bond to that sort of thing Well, then I tried bonding to, are you my mother bulldozers? And then I tried bonding to this And, oh, eventually you figure out your mother is the one you should be hanging out No This is not a domain where you can learn by trial and error And what is seen instead is this phenomenon of one trial learning The first thing baby birds are exposed to in many species, the first big thing moving around, statistically likely to be mom, that’s who you get attached to And lots of interesting neuroethology has gone on over the years trying to figure out what are the mechanisms of imprinting One of the things that come out is it’s nowhere near as dramatic of critical periods– if you don’t figure out who mom is in the next 7 and 1/2 minutes, you are up the creek You will never– it’s more a sort of relative term But nonetheless, that’s not how learning works You’re supposed to learn from trial and error that snakes, and leopards, and all of those guys are not good mothering models

But it happens Another realm Something that came to be known as prepared learning Which is, there’s all sorts of ways in which some piece of information can be learned Or there’s all sorts of sensory associations you could make with something, but you are prepared to make certain of those associations more easily than others What do I mean by this? A classic example of it is what’s called the sauce Bearnaise syndrome And sauce Bearnaise is some fancy French food that seems very unappealing And I don’t know what it’s made of But this was first described by a guy, University of Pennsylvania, Martin Seligman, one of the most sort of major figures in psychology in the last decades or so We will hear plenty about him to come And this was, one evening he went out for dinner, where he had sauce Bearnaise And then he went to a concert of some opera or something, and then he went home And for some reason or other, he got himself a terrible stomach ache Terrible stomach ache It was a total drag All night long, he had it He didn’t throw up It wasn’t that bad But he had a terrible stomach ache, recovered from it Weeks, months later, he goes out for dinner And he goes off to this French restaurant, and has sauce Bearnaise, and is about to take the first spoonful, or forkful, or handful, or whatever And he realizes this smells totally repulsive to him He could not eat the sauce Bearnaise He has never been able to since then, because he’s associating it with the stomach pains afterward Remember, he didn’t throw up He wasn’t burping up sauce Bearnaise vapors or anything So it’s not like, oh, the taste was just like the acidic stuff that came roaring up the other direction, just associating with the stomach pain OK That’s sensible I mean, that’s not great, but you can kind of see how that happens But you think about it, and that’s breaking all sorts of classical rules of behaviorism and classical learning Which is, if you were going to make an association– you can have a choice between an association of a with b or a with c– you’re going to make the association more readily with whichever one comes closer in time to a So what came closer in time for him? The opera He finished dinner, and then he went to the opera and spent hours listening to Wagner or something, and he didn’t attribute his stomach ache to that The next time he went to an opera, he was perfect He was just fine with that He had prepared learning For pain coming from your gut, you are far more likely to associate with food than with music Prepared learning in us for pain in our GI tract with gustatory stimuli More examples are prepared learning So now you take these, and you’re trying to teach them where there’s a food source Experimental stuff And you give them some like mark or sign or whatever to tell them, here it is, and remember this for the next time Do they make an association between the food source and whatever marker you put up? And what they show in the studies is, they can modify the marker They either modify the shape of it– here’s a little triangle, square, or whatever– the color of it, or they can modify the smell The smell that they– some smell source that they– And what they show is, bees have prepared learning They learn the smell associations much, much faster than the shape or the color associations They can learn of the other ones, but bees have prepared learning for making associations by olfactory cues more readily than making them by color or shape More examples One of the great urban legends is that humans are innately scared of spiders and snakes Humans are not, because there’s all sorts of cultures where people love spiders and where, in fact, they love spiders Because they love to chase after them, and pull their legs out, and then cook them up and eat them, and people are not scared in front of spiders and getting the willies from them It is not innate But humans show prepared learning for being scared of spiders and snakes Which is, you can show in humans and in monkeys, as well, the conditioning that’s needed to associate, for example, a picture of a spider with the autonomic response to a mild shock, versus a picture of Disneyland and Mickey and associate it That it takes less of an association for we primates to associate something like a spider or a snake picture with something unpleasant than all sorts of other animate stimuli More examples of how this works You give people– or, as it turns out,

you give monkeys– a task You flash up a complex picture, and you take it away for a few seconds or whatever And then you flash it up again, and one thing has changed in the picture It’s a street scene, wherever it is And you need to pick out which it is And with the monkey studies, you need to indicate sort of where it was to get the reward Are you able to pick up the subtle thing that changed? Humans and monkeys are better picking up for animate objects that change, are better at spotting if there are things like snakes, than if they are animals that we don’t associate like that We are better, in this very rapid exposure, almost subliminal stimuli, we have prepared learning for that Do the exact sort of thing with humans, where what changes from one flash to the other is either an animate object or an inanimate object Humans have prepared learning to pick up stimuli of animate objects much, much more readily A shorter exposure time, more of a subliminal cue, all of that So prepared learning is being all of these examples where, by any logic, universal rules You learn to associate this with this, as BF Skinner, or just as easily with this, or just as easily with this And dog, and cat, and they’re interchangeable, and sensory stimuli But no, all sorts of species come already wired up to learn certain associations more readily than others So completely violating behaviorism OK Final domain where ethologists think about interesting stuff is one of those ones that used to be just the backwaters, or one of those were people would say, there’s no way this could ever be studied And people finally got some headway in figuring how to look at this stuff, which is finally all sorts of interesting things– not just studying the ethology releasing stimuli, neurobiology adaptive advantage of behaviors, but understanding what the internal cognitive and emotional life is of an animal And you can see, it’s right at this point that old classical behaviorists would just have to leave the room they were so repulsed by this Because this was just like William James navel contemplation What do you mean what’s going on inside the head of the animal? You measure what it’s doing It produces a behavior, and that’s how you study it And what instead has come out is another new branch of ethology known as cognitive ethology What’s going on there? One of these sort of landmark ones of it– of sort of a piece of it– came from a guy named Donald Griffin, who passed away a few years ago He was in his 90s He was one of the towering figures of animal behavior, whatever, over the centuries What Donald Griffin discovered was echolocation– that bats echolocate Classic, classic ethologist flavored thing of, whoa! How about we interview the bat in sound frequencies that we humans don’t consider to be sensory stimuli? And opening up this whole new world He was central, played a key role in World War II in the development of sonar, working off of some of the same principles But he’s the person who discovered echolocation Just to make all of you who are seniors feel really upset, this was his senior honors thesis at Harvard And, oh! Discovered echolocation So he passed And he spent his entire career on this and doing amazingly elegant stuff And people came to kiss his feet He was such an amazing experimentalist And when he was about 70 years old, clearly what occurred to him was, I don’t really care what anybody else thinks at this point I’ve got something that I want to bring up, which is the possibility that animals actually have awareness And he published a book called On the Question of Animal Awareness And it’s clear he published it then because he had tenure And he already had tenure in his nursing home, and he wasn’t going to get booted out by everyone saying, oh my god, did you see what happened to Donald Griffin? He used to be a real scientist What happened to the guy? Here he is, sitting around speculating on, do animals have internal lives of awareness? And what he did was outline how what a research program to get at that would be like And people have been studying it ever since and showing that animals have strategic awareness They are doing all sorts of subtle really Really interesting field So starting it off with that Closely related to that was the issue of whether animals have self-awareness And we know that dogs don’t, because they will bark at themselves in the mirror for the rest of time But do animals have self-awareness? This was something pioneered by a guy named Gordon Gallup And like one of those brilliant, elegant studies Here’s what he did

He would take a chimp, a captive chimp, and he would give it a mild anesthetic, so the chip would be a little bit drowsy for a minute or two And while it was down, he would quickly run in with a magic marker and put a little circle like on the forehead of the chimp Chimp comes to, goes back to its business, where there is now a mirror in the room And at some point, the chimp comes up to it, because they’ll wander around and encounter this And here’s the critical question right now Can the chimp figure out that’s not another chimp, that’s me? And what the evidence was that he produced to suggest this was precisely the case was showing the chimps were now far more likely than at the chance level– you see how it’s being set up, this is a well-designed experiment– far more likely to look in the mirror and scratch here to see what is this thing? Where did this thing come from? And that has been viewed as the gold standard for self-awareness Do you look at that and respond as if you were knowing that that is you rather than, that’s some other animal? And self-awareness by this test has been shown in all sorts of species Elephants by this rule have self-awareness I don’t know who puts the magic marker thing up on their forehead But when you do that, they will bring the trunk up and investigate it But interestingly, marmoset monkeys– those delightful, pair bonding for life South American monkeys– marmoset monkeys don’t have self-awareness And that’s kind of puzzling, because all sorts of other primates that in the rough way are as neurobiologically complex had it And they don’t And, OK, so Marmoset monkeys don’t But then an ethologist, a guy named Marc Hauser at Harvard, thought in the monkey’s own language And knowing marmosets– he was a marmoset researcher– in order to spot this on your forehead, if you were a monkey, you have to be looking in the mirror something very close to looking in your reflection’s eyes And marmosets don’t do that as part of their social system They never noticed there was this up there, because they never look up at that part of their reflection So what he would do is, he would now do the same paradigm and put the little dot here And marmosets, off they are a minute later trying to figure out what this thing was about Interviewing the animal in its own language What else? Another domain of this So awareness, self awareness Another thing now shown in other species called theory of mind One that psychologists, developmental psychologists love Theory of mind At what point when you were growing up do you suddenly realize, number one, there are other individuals? There are boundaries to individuals You are not one sort of ego boundaryless sort of continuation of mom There’s other individuals who could have different information about the world than you do And that usually comes around age 4 or 5 or so My children got theory of mind when they were 3 and 1/2 And we can document that if need be, but it comes out somewhere around then And what you see– it’s a classic test that it’s done You tell the child a story, OK, here’s the– some of you will know this The Mary Ann, the Barbie Ann? The Sally Anne OK The Sally Anne test of theory of mind So you tell this kid this story about, here’s this kid who has their doll named Sally Anne Sally? OK, Sally OK So they have this doll named Sally Anne And you tell them– they’re totally attached to Sally Anne They go to sleep with it, and always on the bed, and all of that And the kid goes off every day to preschool or whatever And this is the day that mom looks at Sally Anne there and says, oh no, Sally Anne is all soiled, and it’s time to throw Sally Anne in the washing machine So in goes Sally Anne And Sally Anne is then on the dryer, eventually sitting on top of the dryer, when child comes back from school And now you say to the kid you’re testing, oh, where’s that child going to go and look for Sally Anne? If you have theory of mind, you will know the kid doesn’t know that Sally Anne wound up in the washing machine, because she was off at preschool And you would then say, oh, still in the bedroom On the other hand, if you don’t have theory of mind, it’s inconceivable to you that the child in the story wouldn’t know, because you know And they must know the same thing, because we all know the same thing And you would say, the child will go look on the washing machine That’s how you begin to see the evidence of beginning to understand that another individual has different information than you have And people were soon showing this with chimps Here would be one example That’s not a smile

That’s a banana So you would have one chimp here and one chimp here And here’s how you would do this paradigm, which is this would be a high ranking chimp This would be a low ranking one Put him in there, and they’re watching And an experimenter comes along and puts down a really cool piece of food and in a way that the chimps can’t necessarily see But the main thing here is that there are these dividers in between In one case the divider, near the dominant individual, is glass They can see through it In the other case, it’s opaque They can’t see through it So now, you release the chimps to go for the food And what happens is the low ranking guy– if and only if this was glass here– doesn’t bother trying to get the banana Because he knows the other guy saw the banana Put up an opaque one, and now he will go for it Design is all wrong here There’s no divider here So release this guy And if this was opaque, he will now go for it, because he knows the other guy doesn’t know there’s a banana there He knows that the other guy has different information than he does Parts of the controls you would expect to see now have this with the glass here, where the dominant individual sees somebody bring in the banana, shows it to them, put it down behind the opaque screen And take out this dominant guy, and put in a different dominant guy, let them loose, and he will go for the banana Because he knows, oh, it’s not simply the rule that dominant guys who scare me know there’s a banana there They know, he’s the one who saw there’s the banana This guy doesn’t know there’s a banana there Theory of mind Or now do it with a lower ranking individual, and it doesn’t matter to you whether or not they could look through the glass or not You’re going to go for the banana, because you’re going to get it regardless The first bits of evidence of theory of mind that a chimp understands that other chimps have different information than them What the studies since then have shown is that chimps do not know how to do theory of mind in a cooperative setting They can only do it for competition They can only do it when they are highly motivated in that way But still, this is an ape This is really quite impressive Birds can do theory of mind Apparently, the smartest birds in the entire universe are corvids, which are ravens and crows who are wildly smart And all sorts of interesting ethology studies that have been done on them, including doing theory of mind You show, with these guys, you give them nuts or whatever it is, seeds or whatever, which they will hide in places And if there is another one around looking at them, they won’t hide it Or they’ll put it there They’ll dig it down into the sawdust there or whatever And when the other guy isn’t looking, they’ll quick get it and move it to someplace else Because they will know, when it’s over here, that this guy doesn’t have the information They can do theory of mind when stashing food More things that animals can do that fall within the realm of this cognitive ethology stuff, which is animals can distinguish between intentional and unintentional behaviors How has this been done in studies? One example, you take a chimp, a captive chimp And it has some totally great food item sitting out there that it’s about to get access to And along comes some lummox of a human walking through And in one case, the human leans down and takes the plate of food and flings it someplace else And in the other circumstance, the human comes along and accidentally trips over the plate, flinging it someplace else When the human leans down and flung it away, the chimp will bang on the walls a lot longer than when the person accidentally tripped over it Chimps can distinguish between intentional and unintentional gestures like that And dogs know the difference Dogs absolutely know the difference between somebody who has kicked them and somebody who has tripped over them All sorts of stuff like that, as well What else? Evidence of animals being able to plan for the future And one great example of this has been with those corvid birds And here you have a design where every day, there’s two compartments that the bird can go into And on one day, you put food here And the next day there, and the next day there You alternate back and forth The key thing is, any time you put food in here, you put a huge amount in here

And at the end of the day, you clear it out Whereas when you’re putting in food here, you’re putting in only a tiny amount So on alternating days, they get a lot here The next day, a little bit A lot here, a little And what you show, what you see after not that long of a time, is these guys, on the day that there’s food here, will take some of it and stash it there for the next day Ravens and crows will do this This is planning for the future They have flexible, cognitive strategies Here’s what’s been shown in bees OK So you do your basic Hugo Von Frisch deal Which is you show a bee some interesting food source They go back to the hive, and they dance and tell everybody about it But this time, what you do is you give the bee completely ridiculous, implausible information You take the bee out to the middle of the lake in your rowboat, and you give him the food there, the nectar And they go flying back to the hive, and they dance like mad, and everything we know about ethology predicts what the bees are supposed to do at this point But the bees don’t do that Because, in effect, they’re sitting there saying, yeah, right In the middle of the lake? You know what you’re telling us? You’re telling us there’s food over in the middle of the lake there That doesn’t make any sense We’re not going to listen to you They don’t respond if a bee, thanks to an experimental manipulation, is telling about a food source in a place that cannot possibly be Flexible cognitive strategies Finally, some evidence in various species, but predominately studied in chimps, of numerosity Numerosity, as in having a sense of numbers having meaning in and of themselves This is totally cool, this experiment OK What you do is you teach a chimp a series of three objects And you show him the first three, and they need to recognize that, if I’ve seen this one before, I press a lever, I get a food reward You train them at the same time to recognize three other pictures– another trio, another trio, another trio So the chimp has now learned a dozen different trios of pictures and knows how to do that If I have seen this trio before, hit the lever, and I get a food reward Now what you do is you make a mistake What you do is you take– here, instead of HIJ, you take out the J, and you substitute it with A In this case, what you do is you take out the I, and you substitute it with B. What’s the difference? In this first case, what you’re doing is you’re removing the third object in the sequence and replacing it with something from the first object in a different sequence In this case, you’re replacing a second object in the sequence with another second object in the sequence And when you do this quickly, tasks quickly, chimps make more mistakes with this than with this What’s going on in their heads? They’re saying, oh yeah, this one looks right No, wait, that one’s not right It’s a different number two than the one for this trio When it matches the number in the sequence, they make more mistakes, because they have partially filed it away Not only have I seen this picture before– not only have I seen this picture before as part of this trio, but when I see it as the trio, it’s the third one that I see It’s the first one they have had some sort of numerosity information coming in there Another study showing this, and this one with chimps And in this one, what you do is a strategy you’ve heard already, which is you record the vocalizations of chimps And what you do is you record the sounds of big male chimps giving threatening bellows So now, you hide the speaker in some bush there, and you’ve got your chimps nearby And you play the sound of some big male bellowing, and it’s a chimp they’ve never heard before Chimps recognize individual voices, no big surprise And what happens is all the males run over to the bush to investigate Now make it a little scarier Play the sound of two strange male chimps bellowing, giving their territorial calls And do you run over or not? You have a whole bunch of males run over Now make it even scarier Three voices of them And what you see is, by the time it gets up to there, if there are more voices of novel males that they’re hearing, than the number of males in their group, they get out of there And what you’ll see is, they’re playing the voice there They begin, and they add in another one sequentially And say this will come up to four voices, and they’ll show the three chimps are like coming up there ready to investigate And three voices, and uh-oh, we’re out numbered Numbered We’re out numbered And they slither back and go the other way at that point

They have a sense of the number four is bigger than the number three Finally, evidence of transitive thinking Not just in nonhuman primates, but as shown here by Russ Fernals in the bio department in fish I’m watching a defeat b Then b defeats me I go and give a subordinate gesture to a And this has now been shown And a similar theme again, it’s only done in the context of competition, highly motivated circumstances OK So what do we got now? We’ve got a completely different way of thinking about behavior and emphasizing here natural setting– experimentation rather than coming up with those just so stories The notions of all sorts of species, including us, functioning in sensory domains that are unheard of And finally, all sorts of types of learning that are ways in which organisms are not supposed to learn that all of us do For more, please visit us at standford.edu

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