Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex

626

708

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.psychology | behavior | comparative methods | inhibitory control | executive function S ince Darwin, understanding the evolution of cognition has been widely regarded as one of the greatest challenges for evolutionary research (1). Although researchers have identified surprising cognitive flexibility in a range of species (2-40) and potentially derived features of human psychology (41-61), we know much less about the major forces shaping cognitive evolution (62-71). With the notable exception of Bitterman's landmark studies conducted several decades ago (63, 72-74), most research comparing cognition across species has been limited to small taxonomic samples (70, 75). With limited comparable experimental data on how cognition varies across species, previous research has largely relied on proxies for cognition (e.g., brain size) or metaanalyses when testing hypotheses about cognitive evolution (76-92). The lack of cognitive data collected with similar methods across large samples of species precludes meaningful species comparisons that can reveal the major forces shaping cognitive evolution across species, including humans (48,70,89,(93)(94)(95)(96)(97)(98). SignificanceAlthough scientists have identified surprising cognitive flexibility in animals and potentially unique features of human psychology, we know less about the selective forces that favor cognitive evolution, or the proximate biological mechanisms underlying this process. We tested 36 species in two problemsolving tasks measuring self-control and evaluated the leading hypotheses regarding how ...

Section: Discussionmentioning

confidence: 99%

The evolution of self-control

MacLean¹,

Hare

Nunn³

et al. 2014

626

708

“…The summary measure can then be used to compare the functional coupling pattern of each human region with those of all 448 regions in the macaque and vice versa. The Manhattan distance has previously been used to compare the coupling patterns of brain areas across species (17)(18)(19). It is a useful metric for comparing connectivity because it is summarizes the whole pattern of coupling for an area.…”

Section: Methodsmentioning

confidence: 99%

“…A formal comparison between human and macaque coupling patterns was performed by calculating the summed absolute difference [the "Manhattan" or "city-block" distance (17)(18)(19) of the coupling scores]. This process yielded a summary measure of the difference in coupling patterns for each pair of areas in the two species (e.g., for human "task-positive ACC" compared with monkey ROI number 267 the summed absolute difference between coupling profiles is 34.78).…”

Section: Methodsmentioning

confidence: 99%

“…Such interactions are reliant on anatomical connections between areas (15) and determine the information an area has access to and the way it can influence other areas, and thereby behavior. Each region of the brain has a defining set of interactions, a connectional or interactional "finger-print" (16), that can be compared across species (17)(18)(19). We focused on areas throughout the entire medial and orbital frontal lobe, including the ACC, lOFC, vmPFC, and frontal pole (FP) that have been related to decision making in humans and monkeys.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Connectivity reveals relationship of brain areas for reward-guided learning and decision making in human and monkey frontal cortex

Neubert

Mars

Sallet

et al. 2015

Self Cite

347

388

Reward-guided decision-making depends on a network of brain regions. Among these are the orbitofrontal and the anterior cingulate cortex. However, it is difficult to ascertain if these areas constitute anatomical and functional unities, and how these areas correspond between monkeys and humans. To address these questions we looked at connectivity profiles of these areas using resting-state functional MRI in 38 humans and 25 macaque monkeys. We sought brain regions in the macaque that resembled 10 human areas identified with decision making and brain regions in the human that resembled six macaque areas identified with decision making. We also used diffusion-weighted MRI to delineate key human orbital and medial frontal brain regions. We identified 21 different regions, many of which could be linked to particular aspects of reward-guided learning, valuation, and decision making, and in many cases we identified areas in the macaque with similar coupling profiles.orbitofrontal cortex | anterior cingulate cortex | decision making | resting state functional connectivity | comparative anatomy A s humans we make decisions by taking into account different types of information, weighing our options carefully, and eventually coming to a conclusion. We then learn from witnessing the outcome of our decisions. Human functional MRI (fMRI) has had a major impact on elucidating the neural networks mediating decision making and learning, but key insights can only be obtained in neural recording, stimulation, and focal lesion studies conducted in animal models, such as the macaque. Combining insights from human fMRI and animal studies is, however, not straightforward because there is uncertainty about basic issues, such as anatomical and functional correspondences between species (1). For example, although there are many reports of decision value-related activity in the human ventromedial prefrontal cortex (vmPFC) (2, 3), it is unclear whether they can be related to reports of reward-related activity either on the ventromedial surface of the frontal lobe (4, 5), in the adjacent medial orbitofrontal sulcus (6), or indeed to any macaque brain area. It is claimed that some areas implicated in rewardguided decision making and learning, such as parts of anterior cingulate cortex (ACC), are not found in macaques (7), but such theories have never been formally tested.In addition, there is uncertainty about the basic constituent components of decision-making and learning circuits. To return to the example of the vmPFC, although this region is often contrasted with similarly large subdivisions of the frontal cortex, such as the lateral orbitofrontal cortex (lOFC) and ACC (8), it is unclear whether, and if so how, it should be decomposed into further subdivisions. Moreover, there are sometimes fundamental disagreements about how brain areas contribute to decision making and learning. For example, it has been claimed both that the ACC does (9-11) and does not (12) contribute to reward-based decision making and that it is concerned with dist...

“…More recent studies demonstrate activity in BLA tracks the value of rewards and punishments (18), predicts risky financial decisions (19), reflects internal motivational goals (20), and correlates with vigilance and attention (21). BLA also signals social information, such as facial expressions and the direction of gaze, and has been implicated in theory of mind and emotional empathy (22)(23)(24)(25)(26). Notably, oxytocin (OT), a neurohypophysial hormone that modulates many social behaviors (27), appears to do so via the amygdala in humans and nonhuman primates (28-30).…”

mentioning

confidence: 99%

Neural mechanisms of social decision-making in the primate amygdala

Chang

Fagan

Toda

et al. 2015

127

117

Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.amygdala | social decision | value mirroring | oxytocin | hierarchical modeling H ow we treat others impacts not only their well-being but our own. Human society depends on cooperation, charity, and altruism, as well as institutions to regulate selfish biases. In humans, these behaviors involve perspective-taking, empathy, and theory of mind (1, 2), and the rudiments of these capacities appear to mediate complex social behavior in animals (3). Recent research has sketched a rough outline of the neural circuits that contribute to complex social behavior (4, 5). These comprise a set of domaingeneral brain areas, including the ventromedial prefrontal cortex and ventral striatum, that process information about reward and punishment and contribute to decision-making, and a set of specialized areas, including the temporoparietal junction and medial prefrontal cortex, that process specifically social information (4, 6). How social and nonsocial signals in these circuits are integrated to mediate decisions with respect to others remains imperfectly understood, in part, due to the indirect nature of hemodynamic signals measured in human neuroimaging experiments that constitute the bulk of this research. Recent advances in the development of neurophysiological and neuropharmacological models of social decision-making, however, permit more direct inquiry into the neural mechanisms mediating other-regarding behavior (7-11).The amygdala, especially the basolateral division (BLA), has been implicated in both decision-making and social perception, inviting the possibility that it contributes to decision-making with respect to others (12)(13)(14)(15)(16)(17). This set of nuclei is well known for contributions to emotional experience and expression, especia...