Discontinuity between human and nonhuman minds?

In a recent issue of Brain and Behavioral Science (BBS) Penn, Holyoak and Povinelli argue for a profound difference in kind, not degree, between human and animal minds. Their suggestions elicit mainly vigorous opposition as well as some support from an array of commentators. Several of the commentators point out evidence for flexible relational capabilities within a physical symbol system exhibited by dolphins and birds. As I read through the debate and its mind-numbing detail I give up on trying to convey a succinct summary, but here is their abstract. (You might compare this with the work of Hauser et al, that I mentioned in a previous post.):

Over the last quarter century, the dominant tendency in comparative cognitive psychology has been to emphasize the similarities between human and nonhuman minds and to downplay the differences as “one of degree and not of kind” (Darwin 1871). In the present target article, we argue that Darwin was mistaken: the profound biological continuity between human and nonhuman animals masks an equally profound discontinuity between human and nonhuman minds. To wit, there is a significant discontinuity in the degree to which human and nonhuman animals are able to approximate the higher-order, systematic, relational capabilities of a physical symbol system (PSS) (Newell 1980). We show that this symbolic-relational discontinuity pervades nearly every domain of cognition and runs much deeper than even the spectacular scaffolding provided by language or culture alone can explain. We propose a representational-level specification as to where human and nonhuman animals' abilities to approximate a PSS are similar and where they differ. We conclude by suggesting that recent symbolic-connectionist models of cognition shed new light on the mechanisms that underlie the gap between human and nonhuman minds.

Growing new brain cells enhanced by social contact

From the editor's choice section of the May 30 issue of Science, a suggestion that increased social input from a larger number of other animals enhances the survival of new brain cells in brain areas involved in communication:

Out With the Old, In With the New

Might this adage, which some pundits have claimed as the basis for the vernal electoral calamities that have befallen the Labour Party in the United Kingdom, apply equally forcefully to the turnover of neurons in the brain? Adar et al. have performed a painstaking histological and immunofluorescence accounting of the survival likelihoods of newly born neurons in the brain of the zebra finch, a songbird that serves as an animal model for studying innate and learned influences on vocal communication. They focused on the nidopallium caudale (NC) region because it participates in auditory processing and is activated by social stimuli (other songbirds in this notably social species). By varying the complexity of the social environment, they found that the youngest cells--which had recently migrated from the site of their birth and were still becoming integrated, quite literally, as they established syn-aptic connections with existing NC neurons--were more likely to have survived if the bird had been exposed to a large group of male and female birds; conversely, in birds housed with only one other individual, the survival of older (though still relatively young) cells was enhanced. One interpretation of these data is that an increase in demand--in the form of an upturn in auditory/social inputs needing to be processed--acts as a selective pressure favoring the survival of new recruits.

Do chimpanzees have a theory of mind? 30 years later

Call and Tomasello offer a review in the May issue of Trends in Neuroscience on the controversial question of how much our nearest relatives understand about the minds of others:

On the 30th anniversary of Premack and Woodruff's seminal paper asking whether chimpanzees have a theory of mind, we review recent evidence that suggests in many respects they do, whereas in other respects they might not. Specifically, there is solid evidence from several different experimental paradigms that chimpanzees understand the goals and intentions of others, as well as the perception and knowledge of others. Nevertheless, despite several seemingly valid attempts, there is currently no evidence that chimpanzees understand false beliefs. Our conclusion for the moment is, thus, that chimpanzees understand others in terms of a perception–goal psychology, as opposed to a full-fledged, human-like belief–desire psychology.

Here is one description of an experimen showing that Chimpanzees infer a human's intentions:

Buttelmann et al. [Dev. Sci. 10 (2007 pp. F31–F38]...tested six human-raised chimpanzees in the so-called rational-imitation paradigm. The chimpanzees were shown how to operate an apparatus to produce an interesting result (e.g. lights or sounds), and then they were given a turn. The most natural behavior for them in all cases was to operate it with their hands. But this obvious behavior was never demonstrated for them; they always saw a human manipulate the apparatus in a novel way with some other body part. The idea was that in some cases the physical constraints of the situation dictated that the human (referred to as ‘E’ in the figure) had to use that unusual body part; for example, he had to turn on a light with his head because his hands were occupied holding a blanket or he had to operate a light with his foot because his hands were occupied with a heavy bucket (see Figure I). When the chimpanzees saw this forced use of the unusual body part, they mostly discounted it and used their hands as they normally would (because the constraints were not present for them). However, when they saw the human use the unusual body part when there was no physical constraint dictating this, they quite often copied the unusual behavioral means themselves. If we interpret this experiment the way it is interpreted for human infants, the conclusion is that the chimpanzees understood not only what the experimenter was trying to do (his goal) but also why he was doing it in the way he was doing it – the rationality behind the choice of the plan of action toward the goal. According to Tomasello et al. [Behav. Brain Sci. 28 (2005), pp. 675–691], an understanding of the action plan chosen toward a goal constitutes an understanding of the intention.

Negligent mouse moms - a model for humans?

From the laboratory of my Univ. of Wisconsin Zoology colleague Steve Gammie, along with Anthony Auger in the Psychology Department, an interesting account of a mouse model for human maternal neglect: a strain of mice that exhibit unusually high rates of maternal neglect, with approximately one out of every five females failing to care for her offspring. By comparing the good mothers to their less attentive relatives, this group has found that negligent parenting seems to have both genetic and non-genetic influences, and may be linked to dysregulation of the brain signaling chemical dopamine. In more detail, they:

...examined brain activity in neglectful and nurturing mice. c-Fos expression was significantly elevated in neglectful relative to nurturing mothers in the CNS, particularly within dopamine associated areas, such as the zona incerta (ZI), ventral tegmental area (VTA), and nucleus accumbens. Phosphorylated tyrosine hydroxylase (a marker for dopamine production) was significantly elevated in ZI and higher in VTA (although not significantly) in neglectful mice. Tyrosine hydroxylase levels were unaltered, suggesting a dysregulation of dopamine activity rather than cell number. Phosphorylation of DARPP-32, a marker for dopamine D1-like receptor activation, was elevated within nucleus accumbens and caudate-putamen in neglectful versus nurturing dams.

Episodic-like memory in rats - not like humans

Until recent experiments showing that scrub jays remember where and when they cached or discovered foods of differing palatability, it had been thought that episodic memory - defined as ability to remember an event (what) as well as where and when it happened - was confined to humans. Memory for 'when' observed in scrub jays has been taken to suggest that animals can mentally travel in time or locate a past event within a temporal framework of hours and days. Roberts et al. point out that:

An alternative possibility is that, instead of remembering when an event happened within a framework of past time, animals are keeping track of how much time has elapsed since caching or encountering a particular food item at a particular place and are using elapsed time to indicate return to or avoidance of that location. The cues of when and how long ago are typically confounded in studies of episodic-like memory. Thus, animals might be remembering how long ago an event occurred by keeping track of elapsed time using accumulators, circadian timers, their own behavior, or the strength of a decaying memory trace. If this is the case, then episodic-like memory in animals may be quite different from human episodic memory in which people can reconstruct past experiences within an absolute temporal dimension.

Their experiments show that this is the case.

Three groups of Long-Evans hooded rats were tested for memory of previously encountered food. The different groups could use only the cues of when, how long ago, or when + how long ago. Only the cue of how long ago food was encountered was used successfully. These results suggest that episodic-like memory in rats is qualitatively different from human episodic memory.

Rodent trained to be Las Vegas croupier

Atshushi Iriki's group in Tokyo has trained degus (intelligent rodents native to the highlands of Chile) to provide the first example (published in PLOS ONE) of rodents wielding tools for a task. (see my 5/7/2007 post for an example with Ravens. Monkeys and Chimps also use tools - Hihara et al. have found extension of corticocortical afferents into the anterior bank of the intraparietal sulcus after tool-use training in adult monkeys.) It will be interesting to see whether tool-use training in degus also results in extended representations in parietotemporal areas and newly formed connections between brain areas, including the prefrontal cortex, similar to those observed in the macaque brain. Work of this sort begins to define brain structures used in the development of tool use.

In Most Species, Faithfulness Is a Fantasy

This post has the title of a great article by Natalie Angier in the NYTimes Science section. Elliot Spitzer was doing nothing that hasn't been done by males and females of thousands of other species - representatives of every taxonomic twig on the great tree of life.

Even the “oldest profession” that figured so prominently in Mr. Spitzer’s demise is old news. Nonhuman beings have been shown to pay for sex, too. Reporting in the journal Animal Behaviour, researchers from Adam Mickiewicz University and the University of South Bohemia described transactions among great grey shrikes, elegant raptorlike birds with silver capes, white bellies and black tails that, like 90 percent of bird species, form pair bonds to breed. A male shrike provisions his mate with so-called nuptial gifts: rodents, lizards, small birds or large insects that he impales on sticks. But when the male shrike hankers after extracurricular sex, he will offer a would-be mistress an even bigger kebab than the ones he gives to his wife — for the richer the offering, the researchers found, the greater the chance that the female will agree to a fly-by-night fling.

In another recent report from the lubricious annals of Animal Behaviour entitled “Payment for sex in a macaque mating market,” Michael D. Gumert of Hiram College described his two-year study of a group of longtailed macaques that live near the Rimba ecotourist lodge in the Tanjung Puting National Park of Indonesia. Dr. Gumert determined that male macaques pay for sex with that all-important, multipurpose primate currency, grooming. He saw that, whereas females groomed males and other females for social and political reasons — to affirm a friendship or make nice to a dominant — and mothers groomed their young to soothe and clean them, when an adult male spent time picking parasites from an adult female’s hide, he expected compensation in the form of copulation, or at the very least a close genital inspection. About 89 percent of the male-grooming-female episodes observed, Dr. Gumert said in an interview from Singapore, where he is on the faculty of Nanyang Technological University, “were directed toward sexually active females” with whom the males had a chance of mating.

A voice region in the monkey brain

Both human and monkey brains have visual regions that are activated most strongly by the faces of conspecifics. Our brains also have have a region that is specialized for processing human voices that is located anteriorly on the temporal lobe, on the upper bank of the superior-temporal sulcus. Logothetis and his colleagues have now found a corresponding region in monkey brains. Their abstract and a portion of one of the figures:

For vocal animals, recognizing species-specific vocalizations is important for survival and social interactions. In humans, a voice region has been identified that is sensitive to human voices and vocalizations. As this region also strongly responds to speech, it is unclear whether it is tightly associated with linguistic processing and is thus unique to humans. Using functional magnetic resonance imaging of macaque monkeys (Old World primates, Macaca mulatta) we discovered a high-level auditory region that prefers species-specific vocalizations over other vocalizations and sounds. This region not only showed sensitivity to the 'voice' of the species, but also to the vocal identify of conspecific individuals. The monkey voice region is located on the superior-temporal plane and belongs to an anterior auditory 'what' pathway. These results establish functional relationships with the human voice region and support the notion that, for different primate species, the anterior temporal regions of the brain are adapted for recognizing communication signals from conspecifics.

Figure - The color code from orange to red indicates voxels with a clear and significant preference for macaque vocalizations. The cyan-to-blue color code identifies voxels with no preference for MVocs. The slice orientation and position are shown in the lower inset

The social brains of Hyenas

There is a correlation between brain size, particularly the newer frontal lobes, and the size of the social group an animal lives in. This rule works for our primate lineage and, it turns out, also for hyenas: those with the simplest social systems have the tiniest frontal cortices. The spotted hyena, which lives in the most complex societies, has far and away the largest frontal cortex. The brown and striped hyenas, with intermediate social systems, have intermediate brains. It appears that primates are not unique in the complexity of their social lives. An article by Zimmer describes the work of Holekamp and colleagues, who have found an array of complex social behaviors in spotted hyenas that are as complex as those of baboons. The groups are comprised of 60 to 80 individuals who all know each other individually. There are alliances, rivalries, and social hierarchies headed by an alpha female. Cubs undergo an education period. Hyena clans patrol their territory borders together against neighboring clans, kills near these borders can provoke clan conflicts. These behaviors are accomplished by brains with frontal lobes that are as easily distinguished as those of social primates (see figure.)

Video game addiction, and taking play seriously.

Video games trigger reward and addiction centers of the brain, just like cocaine. Hoeft et. al. at Stanford have compared the activation of these centers in men's and women's brains as they played video games and found them to be more active in male than in female participants. Males showed greater activation and functional connectivity compared to females in the mesocorticolimbic system. The more the men won, the stronger their brain activity. Women's responses were less intense and didn't correlate with winning. This may have something to do with why men seem to become addicted to video games much more easily than women.

There is an interesting and more general article by Robin Henig on play in animals and humans in the New York Times Magazine. The general consensus is that play activity is very important in the development of social intelligence and the ability to respond to rapidly changing situations. It turns out that the rise and decay of play activity in animals corresponds closely to the development curve of the cerebellum, which is important in skilled movements. In one interesting study, experimenters:

...raised 12 female rats from the time they were weaned until puberty under one of two conditions. In the control group, each rat was caged with three other female juveniles. In the experimental group, each rat was caged with three female adults. Pellis knew from previous studies that the rats caged with adults would not play, since adult rats rarely play with juveniles, even their own offspring. They would get all the other normal social experiences the control rats had — grooming, nuzzling, touching, sniffing — but they would not get play... (in) the rats raised in a play-deprived environment, they found a more immature pattern of neuronal connections in the medial prefrontal cortex... less selective pruning of cells and a more tangled, immature medial prefrontal cortex in play-deprived rats might mean that the rat will be less able to make subtle adjustments to the social world.

There are numerous theories about the function of play. It doesn't seem unreasonable that that the fragmentary, disorderly, unpredictable, exaggerated, improvised, vertiginous, and nonsensical nature of play trains the brain allows for a wider behavioral repertory and perhaps more competence in responding to novel or unforeseen situations.

Killer Instincts.

Dan Jones writes a news feature in Nature on neuroscientific and evolutionary perspectives on homicide, mainly carried out by men. Here are some selected chunks:

Men are not just more likely to kill other people than women are, they are also more likely to do so in groups ...Humans are not the only primates to form coalitions that kill members of neighbouring communities. ...five long-term study sites dotted around Africa have seen murderous 'gang violence' in chimpanzees...Wilson and Muller have compared death rates from conflict between groups of chimps in the five long-term study sites with data for inter-group human conflicts in numerous subsistence-farmer and hunter–gatherer societies...Overall, humans and chimpanzees showed comparable levels of violent death from aggression between groups...however, chimps display within group aggression and killing behaviour 200 times more frequently that aboriginal human groups...this prosocial lack of violence looks like a fundamental aspect of human nature — the human ability to generate in-group amity often goes hand in hand with out-group enmity...Choi and Bowles have produced models in which altruism and war co-evolve, promoting conflict between groups and greater harmony within them.

A decline in inter-personal violence (as opposed to inter-group war) can be seen over the shorter timescale and narrower field of modern European history. Eisner has documented a trend of declining homicide rates estimated from historical records left by coroners, royal courts and other official sources spanning Europe from the twelfth century to the modern day. After rising from an average of 32 homicides per 100,000 people per year in the thirteenth and fourteenth centuries to 41 in the fifteenth, the murder rate has steadily dropped in every subsequent century, to 19, 11, 3.2, 2.6 and finally 1.4 in the twentieth century...a few centuries is too short a time for evolution to have shaped human nature much... A part of the answer that is consistent with an evolutionary approach is a long-term reduction in inequalities of life circumstances and prospects.

Human and Animal Math

Michael Beran writes a brief review of the evolutionary and developmental foundations of mathematics. Humans and other higher animals are born with a dedicated systems for numerical processing.

The fruits of promiscuity...more dancing and food

From the research highlights section of the Jan. 24 issue of Nature, summarizing work by Matilla et al:

A honeybee colony led by a promiscuous queen does better than one led by a faithful queen: the colony forages more, stores more food and grows faster. Heather Mattila and her colleagues at Cornell University in Ithaca, New York, think this happens because genetically diverse colonies dance more....Honeybees 'waggle dance' to tell each other where to fly to find food. Mattila's team compared colonies in which the queen always bred with the same male to colonies ruled by a queen that had been inseminated by 15 drones. On average, worker bees from the latter category performed 36% more dances daily, kept waggling for 62% longer and communicated about food discoveries farther from the nest than did workers from single-father colonies.

Songbirds also have mirror neurons.

Mirror neurons in humans and other primates fire both when a given action is either performed or observed (see the 'mirror neuron' category in the left column of this blog.) Now Prather et al. have found similar neurons in the swamp sparrow, which like humans depends on auditory experience to learn its vocal repertoire. These forebrain neurons are specialized for auditory-vocal monitoring and have virtually the same response to a given note sequence, whether performed or heard. They also innervate striatal structures important for song learning, raising the possibility that singing-related activity in these cells is compared to auditory feedback to guide vocal learning. Here is a graphic from a New and Views article on this work by Tchernichovski1 & Wallman in the same issue of Nature.

(click to enlarge) Figure legend: The neurons identified by Prather and colleagues could be involved in three sensorimotor processes. a, The delayed corollary discharge of song patterns can be simultaneously compared with auditory feedback of the bird's own song, allowing tuning. b, The auditory responses (in the mirroring neurons) to songs of a neighbour might be compared with the memory of the corollary discharge produced during singing. This might allow the bird to identify an imitation by that neighbour. c, Corollary discharges while singing might be compared with a memory of the mirroring neurons' response to the parent's song. The error may then feed back to the song generator and guide vocal learning during song development, in addition to guidance from auditory input during singing (lowest arrow).

Face perception after no experience of faces

This work really nails down the fact that face processing is a special perceptual process and is organized as such at birth, as contrasted with having its origin in a more general-purpose perceptual system that becomes specialized after frequent visual experiences. Sugita has studied face perception in monkeys reared with no exposure to faces. Here is his abstract, and one figure from the paper:

Infant monkeys were reared with no exposure to any faces for 6–24 months. Before being allowed to see a face, the monkeys showed a preference for human and monkey faces in photographs, and they discriminated human faces as well as monkey faces. After the deprivation period, the monkeys were exposed first to either human or monkey faces for a month. Soon after, the monkeys selectively discriminated the exposed species of face and showed a marked difficulty in regaining the ability to discriminate the other nonexposed species of face. These results indicate the existence of an experience-independent ability for face processing as well as an apparent sensitive period during which a broad but flexible face prototype develops into a concrete one for efficient processing of familiar faces.

Figure: An infant monkey and her living circumstance. An infant monkey and a caregiver with (A) and without (B) a facemask. Both photos were taken after the face-deprivation period. (C) Toys placed in the monkey's home cage. (D) Decorations provided around the home cage.

Drunken flies get hypersexual - and gay

Sound familiar? Reminds me of similar behaviors after University of Wisconsin football games, when drunken guys who could not find an appropriate female object would go ahead with what was available - other guys. This news item by Heidi Ledford in Nature describes experiments by Lee et al. that:

...tested the effects of chronic alcohol exposure on sexual behaviour in the fruitfly Drosophila melanogaster. The researchers noted that male flies repeatedly exposed to ethanol vapour became less discriminate in their mate selection. The buzzed flies often courted fellow males, pursuing them around the cage while serenading with a traditional fruitfly courtship song played on vibrating wings.


[Figure: Love Chain, male fruit flies chase each other in a circle] Eventually, the lusty flies devolve into a courting frenzy. “You get a chain of males chasing each other,” says Heberlein, who was not associated with the study but has observed similar behaviour in her own unpublished work. In contrast, alcohol had little effect on mating in female fruitflies, which normally do not court their mates.

The findings suggest that the flies do not fundamentally change their sexual orientation, but rather get over-sexed. “Multiple alcohol exposures makes them essentially hypersexual,” says Heberlein. The mind-dulling effects of alcohol might also make it more of a challenge for male fruitflies to distinguish the gender of other flies in the crowd.

Because of the genetic tools available, fruitflies might be a good model system for probing the idea, suggested for humans, that the neurotransmitter dopamine is a link between sex and alcohol.

Love hangover - the sex peptide

A male, after copulation, has a particular interest in seeing that the female involved ceases further sexual activity that might dilute his genetic contribution. It turns out that male fruitflies don't have to stand by and guard their transferred genetic material — a sex peptide in their semen will do the job. This peptide leads to increased egg-laying by the mated female and behavioural changes that reduce the likelihood of her re-mating. Yapici et al. have now identified the receptor protein for this peptide. It functions in a subset of neurons implicated in other sex-related behaviors. The receptor is highly conserved across insect species, raising the possibility that it could be targeted to disrupt reproduction in insect pests or host-seeking behaviour in disease vectors. (There appears to be no evidence for such a mechanism in primates and humans!).

More on laughing rats...and human chanting?

This is a sequel to my March 20 and June 18, 2007, posts on laughing rats. Rats use ultrasonic communication, with 50-kHz vocalizations indicating an animal's positive subjective state. Wöhr and Schwarting now show that show that 50-kHz signals (either natural 50-kHz calls, which had been previously recorded from other rats, or artificial sine wave stimuli, which were identical to these calls with respect to peak frequency, call length and temporal appearance) can induce approach behaviors. The effect is more pronounced in juvenile rats. It is commonly assumed that humans have lost this mechanism, but I wonder if the powerful bonding emotions induced in groups of humans doing very low frequency vocal chants, which surely have harmonics in the 50-mHz range, might be a evolutionary derivative of this early mammalian behavior . Here are several Tibetan master chants offered by the free sound project. Do they chill you out?

Why can't we perform perfectly?

Some fascinating experiments by Tumer and Brainar on songbirds inform me on why I am not able to perform a completely learned and exhaustively practiced piano piece the same way each time I bang it out.... from the Nature Editor's review of their article:

Why is it that even the best-trained athletes and musicians cannot perform perfectly? One thought is that residual variability in performance is 'noise' that reflects fundamental limits on our ability to control our movements. Experiments using the exceptionally well-rehearsed songs of adult songbirds as a model point to an alternative explanation. Computerized monitoring of the apparently stereotyped songs of adult Bengalese finches revealed minuscule variations in performance. When the birds were given corrections each time the song varied beyond a certain limit, they rapidly learned to adapt their vocalizations. The implication is that once learned, songs can be maintained despite subtle changes to the vocal system due to factors such as ageing. So behavioural 'noise', rather than simply being a nuisance, may reflect experimentation by the nervous system to refine performance.

The abstract from Rumer and Brainar:

Significant trial-by-trial variation persists even in the most practiced skills. One prevalent view is that such variation is simply 'noise' that the nervous system is unable to control or that remains below threshold for behavioural relevance. An alternative hypothesis is that such variation enables trial-and-error learning, in which the motor system generates variation and differentially retains behaviours that give rise to better outcomes. Here we test the latter possibility for adult bengalese finch song. Adult birdsong is a complex, learned motor skill that is produced in a highly stereotyped fashion from one rendition to the next. Nevertheless, there is subtle trial-by-trial variation even in stable, 'crystallized' adult song. We used a computerized system to monitor small natural variations in the pitch of targeted song elements and deliver real-time auditory disruption to a subset of those variations. Birds rapidly shifted the pitch of their vocalizations in an adaptive fashion to avoid disruption. These vocal changes were precisely restricted to the targeted features of song. Hence, birds were able to learn effectively by associating small variations in their vocal behaviour with differential outcomes. Such a process could help to maintain stable, learned song despite changes to the vocal control system arising from ageing or injury. More generally, our results suggest that residual variability in well learned skills is not entirely noise but rather reflects meaningful motor exploration that can support continuous learning and optimization of performance.

Monkeys and college students: similar in non-verbal math

This work from Cantlon and Brannon suggests that humans and nonhuman primates share a cognitive system for nonverbal arithmetic, suggesting an evolutionary link in their cognitive abilities., full text in PLoS Biology, here is the abstract:

Adult humans possess mathematical abilities that are unmatched by any other member of the animal kingdom. Yet, there is increasing evidence that the ability to enumerate sets of objects nonverbally is a capacity that humans share with other animal species. That is, like humans, nonhuman animals possess the ability to estimate and compare numerical values nonverbally. We asked whether humans and nonhuman animals also share a capacity for nonverbal arithmetic. We tested monkeys and college students on a nonverbal arithmetic task in which they had to add the numerical values of two sets of dots together and choose a stimulus from two options that reflected the arithmetic sum of the two sets. Our results indicate that monkeys perform approximate mental addition in a manner that is remarkably similar to the performance of the college students. These findings support the argument that humans and nonhuman primates share a cognitive system for nonverbal arithmetic, which likely reflects an evolutionary link in their cognitive abilities.