Refining the ecological brain: Strong relation between the ventromedial prefrontal cortex and feeding ecology in five primate species

To survive in complex and seasonal environments, primates are thought to rely upon cognitive capacities such as decision-making and episodic memory, which enable them to plan their daily foraging path. According to the Ecological Brain hypothesis, feeding ecology has driven the expansion of the brain to support the corresponding development of cognitive skills. Recent works in cognitive neurosciences indicate that cognitive operations such as decision-making or subjective evaluation (which are contextual and dependent upon episodic memory), relied critically upon a small part of the frontal lobe, often referred to as the ventromedial prefrontal cortex (VMPFC). Several authors suggested that this area might be important for foraging, but this has never been tested. In the present study, we quantified the relation between the size of the VMPFC (along with other cerebral measures: the whole brain, the gyrus rectus and the somatosensory cortex) and key socio-ecological variables in five primate species (Macaca mulatta, Macaca fuscata, Gorilla gorilla, Pan troglodytes and Homo sapiens). We hypothesized that the size of the VMPFC would be greater in primates with a large dietary spectrum and complex foraging strategies. We also hypothesized that the impact of feeding ecology would be stronger on this specific region than on other regions (somatosensory cortex) or on more global cerebral measures (e.g., whole brain). In line with these hypotheses, we found that all cerebral measures were more strongly related to feeding ecology than group size, a proxy for social complexity. As expected, the VMPFC volume is more precisely related to feeding ecology than the whole brain, and appears to be critically related to dietary quality. Thus, combining a comparative approach with predictions coming both from behavioral ecology and cognitive neurosciences, our study provides evidence that feeding ecology played a key role in the development of specific cognitive skills, which rely upon the expansion of a specific cortical area.

[1]  Sereina M. Graber,et al.  Life history, cognition and the evolution of complex foraging niches. , 2016, Journal of human evolution.

[2]  Chet C. Sherwood,et al.  Exceptional Evolutionary Expansion of Prefrontal Cortex in Great Apes and Humans , 2017, Current Biology.

[3]  E. Fehr,et al.  The neurobiology of rewards and values in social decision making , 2014, Nature Reviews Neuroscience.

[4]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[5]  J. Price,et al.  Architectonic subdivision of the human orbital and medial prefrontal cortex , 2003, The Journal of comparative neurology.

[6]  M. Petrides,et al.  Quantitative demonstration of comparable architectonic areas within the ventromedial and lateral orbital frontal cortex in the human and the macaque monkey brains , 2010, The European journal of neuroscience.

[7]  F. Marlowe Hunter‐gatherers and human evolution , 2005 .

[8]  K. Berridge Motivation concepts in behavioral neuroscience , 2004, Physiology & Behavior.

[9]  Klaus Zuberbühler,et al.  Evidence for a spatial memory of fruiting states of rainforest trees in wild mangabeys , 2006, Animal Behaviour.

[10]  Bolton K. H. Chau,et al.  Inverted activity patterns in ventromedial prefrontal cortex during value-guided decision-making in a less-is-more task , 2017, Nature Communications.

[11]  P. Harvey,et al.  Mosaic evolution of brain structure in mammals , 2000, Nature.

[12]  R. Passingham,et al.  The Neurobiology of the Prefrontal Cortex: Anatomy, Evolution, and the Origin of Insight , 2012 .

[13]  Jon H Kaas,et al.  Evolution of somatosensory and motor cortex in primates. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[14]  Lesley K Fellows,et al.  Contrasting Effects of Medial and Lateral Orbitofrontal Cortex Lesions on Credit Assignment and Decision-Making in Humans , 2017, The Journal of Neuroscience.

[15]  Richard W. Byrne,et al.  Travel routes and planning of visits to out-of-sight resources in wild chacma baboons, Papio ursinus , 2007, Animal Behaviour.

[16]  Kevin N Laland,et al.  Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates , 2017, Proceedings of the National Academy of Sciences.

[17]  Robert Barton,et al.  Comparative Primate Socioecology: The evolutionary ecology of the primate brain , 1999 .

[18]  van Schaik,et al.  The Primate Origins of Human Nature , 2016 .

[19]  Judith M Burkart,et al.  Social learning and evolution: the cultural intelligence hypothesis , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  R. Adolphs,et al.  Toward a Neural Basis for Social Behavior , 2013, Neuron.

[21]  H. Meunier,et al.  What, where and when: spatial foraging decisions in primates , 2018, Biological reviews of the Cambridge Philosophical Society.

[22]  Mathias Pessiglione,et al.  A Critical Role for the Hippocampus in the Valuation of Imagined Outcomes , 2013, PLoS biology.

[23]  Robin I. M. Dunbar,et al.  Social network size in humans , 2003, Human nature.

[24]  R. Martin,et al.  Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable data set. , 2008, Journal of human evolution.

[25]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[26]  S. Jelbert,et al.  Beyond brain size , 2017, bioRxiv.

[27]  C. Janson,et al.  Integrating information about location and value of resources by white-faced saki monkeys (Pithecia pithecia) , 2007, Animal Cognition.

[28]  Robin I. M. Dunbar,et al.  Primate cognition: from ‘what now?’ to ‘what if?’ , 2003, Trends in Cognitive Sciences.

[29]  John M. Pearson,et al.  Neuronal basis of sequential foraging decisions in a patchy environment , 2011, Nature Neuroscience.

[30]  E. Koechlin,et al.  Managing competing goals — a key role for the frontopolar cortex , 2017, Nature Reviews Neuroscience.

[31]  D. Lieberman,et al.  Impact of meat and Lower Palaeolithic food processing techniques on chewing in humans , 2016, Nature.

[32]  C. V. van Schaik,et al.  The Expensive Brain: a framework for explaining evolutionary changes in brain size. , 2009, Journal of human evolution.

[33]  Timothy E. J. Behrens,et al.  Online evaluation of novel choices by simultaneous representation of multiple memories , 2013, Nature Neuroscience.

[34]  R. Macarthur,et al.  On Optimal Use of a Patchy Environment , 1966, The American Naturalist.

[35]  M. E. Thompson,et al.  Energetics of feeding, social behavior, and life history in non-human primates , 2017, Hormones and Behavior.

[36]  Torsten Rohlfing,et al.  The INIA19 Template and NeuroMaps Atlas for Primate Brain Image Parcellation and Spatial Normalization , 2012, Front. Neuroinform..

[37]  P. Goldman-Rakic,et al.  Myelo‐ and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[38]  L. Lefebvre,et al.  Brains, Innovations and Evolution in Birds and Primates , 2004, Brain, Behavior and Evolution.

[39]  P. C. Lee,et al.  Ecology and energetics of encephalization in hominid evolution. , 1991, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  Mathias Pessiglione,et al.  Primate ventromedial prefrontal cortex neurons continuously encode the willingness to engage in reward directed behavior , 2016, bioRxiv.

[41]  R. Byrne,et al.  Spatio‐temporal complexity of chimpanzee food: How cognitive adaptations can counteract the ephemeral nature of ripe fruit , 2016, American journal of primatology.

[42]  Paul H. Harvey,et al.  Primates, brains and ecology , 2009 .

[43]  Lydia Ng,et al.  Allen Brain Atlas: an integrated spatio-temporal portal for exploring the central nervous system , 2012, Nucleic Acids Res..

[44]  Neil Burgess,et al.  Medial Prefrontal Cortex: Adding Value to Imagined Scenarios , 2015, Journal of Cognitive Neuroscience.

[45]  P. Hof,et al.  Brain organization of gorillas reflects species differences in ecology. , 2015, American journal of physical anthropology.

[46]  H. Barbas,et al.  Cortical Connections Position Primate Area 25 as a Keystone for Interoception, Emotion, and Memory , 2018, The Journal of Neuroscience.

[47]  M. Rushworth,et al.  Valuation and decision-making in frontal cortex: one or many serial or parallel systems? , 2012, Current Opinion in Neurobiology.

[48]  C. V. van Schaik,et al.  How humans evolved large brains: Comparative evidence , 2014, Evolutionary anthropology.

[49]  J. Price,et al.  Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey , 1994, The Journal of comparative neurology.

[50]  Timothy Edward John Behrens,et al.  Dissociable contributions of ventromedial prefrontal and posterior parietal cortex to value-guided choice , 2014, NeuroImage.

[51]  T. Insel,et al.  Subcortical projections of area 25 (subgenual cortex) of the macaque monkey , 2000, The Journal of comparative neurology.

[52]  G. V. Van Hoesen,et al.  Prefrontal cortex in humans and apes: a comparative study of area 10. , 2001, American journal of physical anthropology.

[53]  N. Cooper,et al.  Phylogenetic signal in primate behaviour, ecology and life history , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  Herman Pontzer,et al.  Energy Expenditure in Humans and Other Primates: A New Synthesis , 2015 .

[55]  M. Symonds,et al.  A Primer on Phylogenetic Generalised Least Squares , 2014 .

[56]  Andrew M. Clark,et al.  Interaction Between Orbital Prefrontal and Rhinal Cortex Is Required for Normal Estimates of Expected Value , 2013, The Journal of Neuroscience.

[57]  Jan Peters,et al.  Episodic Future Thinking Reduces Reward Delay Discounting through an Enhancement of Prefrontal-Mediotemporal Interactions , 2010, Neuron.

[58]  T. Bugnyar,et al.  Cognition without Cortex , 2016, Trends in Cognitive Sciences.

[59]  K. Laland,et al.  Social intelligence, innovation, and enhanced brain size in primates , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Richard E. Passingham,et al.  Is the Prefrontal Cortex Especially Enlarged in the Human Brain? Allometric Relations and Remapping Factors , 2014, Brain, Behavior and Evolution.

[61]  Carel P. van Schaik,et al.  Explaining brain size variation: from social to cultural brain , 2012, Trends in Cognitive Sciences.

[62]  Timothy E. J. Behrens,et al.  Review Frontal Cortex and Reward-guided Learning and Decision-making Figure 1. Frontal Brain Regions in the Macaque Involved in Reward-guided Learning and Decision-making Finer Grained Anatomical Divisions with Frontal Cortical Systems for Reward-guided Behavior , 2022 .

[63]  Robin I. M. Dunbar Neocortex size as a constraint on group size in primates , 1992 .

[64]  K. Milton,et al.  Foraging behaviour and the evolution of primate intelligence. , 1988 .

[65]  H. Damasio,et al.  Dissociation Of Working Memory from Decision Making within the Human Prefrontal Cortex , 1998, The Journal of Neuroscience.

[66]  Robert O Deaner,et al.  Overall Brain Size, and Not Encephalization Quotient, Best Predicts Cognitive Ability across Non-Human Primates , 2007, Brain, Behavior and Evolution.

[67]  Robin I. M. Dunbar,et al.  Understanding primate brain evolution , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[68]  Candy Rowe,et al.  A critique of comparative studies of brain size , 2007, Proceedings of the Royal Society B: Biological Sciences.

[69]  A. Rosati Foraging Cognition: Reviving the Ecological Intelligence Hypothesis , 2017, Trends in Cognitive Sciences.

[70]  Timothy E. J. Behrens,et al.  Neural Mechanisms of Foraging , 2012, Science.

[71]  Scott A. Williams,et al.  Primate brain size is predicted by diet but not sociality , 2017, Nature Ecology &Evolution.

[72]  H. Eichenbaum,et al.  Can We Reconcile the Declarative Memory and Spatial Navigation Views on Hippocampal Function? , 2014, Neuron.

[73]  Klaus Zuberbühler,et al.  Primates Take Weather into Account when Searching for Fruits , 2006, Current Biology.

[74]  C. Chapman,et al.  Constraints on Group Size in Red Colobus and Red-tailed Guenons: Examining the Generality of the Ecological Constraints Model , 2000, International Journal of Primatology.

[75]  M. Rushworth,et al.  Connectivity reveals relationship of brain areas for reward-guided learning and decision making in human and monkey frontal cortex , 2015, Proceedings of the National Academy of Sciences.

[76]  Robin I. M. Dunbar Social Brain Hypothesis , 1998, Encyclopedia of Evolutionary Psychological Science.

[77]  B. Richmond,et al.  Ventromedial and Orbital Prefrontal Neurons Differentially Encode Internally and Externally Driven Motivational Values in Monkeys , 2010, The Journal of Neuroscience.

[78]  J. Beehner,et al.  Measuring social complexity , 2015, Animal Behaviour.

[79]  V. Michel,et al.  An Automatic Valuation System in the Human Brain: Evidence from Functional Neuroimaging , 2009, Neuron.

[80]  Eli M. Swanson,et al.  Brain size predicts problem-solving ability in mammalian carnivores , 2016, Proceedings of the National Academy of Sciences.

[81]  K. Milton Distribution Patterns of Tropical Plant Foods as an Evolutionary Stimulus to Primate Mental Development , 1981 .

[82]  Daniel Sol,et al.  Brain Size Predicts the Success of Mammal Species Introduced into Novel Environments , 2008, The American Naturalist.

[83]  L. Sailer,et al.  Measuring the relationship between dietary quality and body size in primates , 2006, Primates.

[84]  Luke J. Matthews,et al.  The 10kTrees website: A new online resource for primate phylogeny , 2010 .

[85]  Leah Krubitzer,et al.  Topographic Maps within Brodmann's Area 5 of macaque monkeys. , 2012, Cerebral cortex.

[86]  Tommy C. Blanchard,et al.  Reward Value Comparison via Mutual Inhibition in Ventromedial Prefrontal Cortex , 2014, Neuron.

[87]  Nicole Zweifel,et al.  Development of foraging skills in two orangutan populations: needing to learn or needing to grow? , 2016, Frontiers in Zoology.

[88]  Timothy E. J. Behrens,et al.  Choice, uncertainty and value in prefrontal and cingulate cortex , 2008, Nature Neuroscience.