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  • Review Article
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Primate brains in the wild: the sensory bases for social interactions

Nature Reviews Neuroscience volume 5, pages 603–616 (2004)Cite this article

Key Points

  • Primates have evolved to detect and process behaviourally relevant stimuli, and are specialized for social behaviour. A comparative and neuroethological approach to the study of primates should produce new insights into the neural bases of sociality. The most important, and best understood, sensory modalities in primates are vision and hearing.

  • Primates are the only mammals to have marked sex differences in colouration. These sex-specific colours, such as the blue scrota of vervet monkeys and the red faces of rhesus monkeys, can denote hierarchical status and in some cases might influence females' choice of mate.

  • Primates can visually recognize individual conspecifics and their interrelationships. They also show some apparent understanding of the significance of gaze direction for future actions and for understanding about objects.

  • The clearest link between visual socioecology and neurobiology is the 'face cells' of the temporal cortex, which respond selectively to faces or facial features. The inferior temporal cortex seems to be important for processing facial identity, and the superior temporal sulcus for processing facial expressions and gaze direction.

  • Primates can also use auditory signals — vocalizations — to identify other individuals and their relationships, or to distinguish group members from foreign individuals. They can also determine the dominance and reproductive status of signallers, and judge group size. Many primate species also produce copulation calls that might be important for attracting mates.

  • Male primates often perform elaborate displays that involve repeated vocalizations. As well as attracting mates, these calls can intimidate rivals and signify dominance. If such calls are costly to produce, they can serve as an accurate indicator of fitness.

  • Our understanding of the neural correlates of auditory behaviour is largely based on studies of the squirrel monkey, although other species have been investigated more recently. Temporal features of vocalizations seem to be important for driving responses in the primary auditory cortex. In higher cortical areas, neurons often respond to more complex sounds.

  • Visual and auditory communication must also be considered in combination. Monkeys can match specific calls with the appropriate facial expressions without training.

  • Hauser proposed a 'socioecologically sensible neuroscience' that requires researchers to take account of the fact that an animal's brain is exquisitely suited to the socioecological problems faced by that species. It is important to bring together ethology and sensory neuroscience, and to compare primates that have different lifestyles, to understand the evolution of primate brains.

Abstract

Each organism in the animal kingdom has evolved to detect and process a specific set of stimuli in its environment. Studies of an animal's socioecology can help us to identify these stimuli, as well as the natural behavioural responses that they evoke and control. Primates are no exception, but many of our specializations are in the social domain. How did the human brain come to be so exquisitely tuned to social interactions? Only a comparative approach will provide the answer. Behavioural studies are shedding light on the sensory bases for non-human primate social interactions, and data from these studies are paving the way for investigations into the neural bases of sociality.

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Figure 1: Sexual colouration.
Figure 2: The eyes have it.
Figure 3: Current models of temporal lobe cortical anatomy.
Figure 4: Relationship between reaction times and the latency of one neuron in the inferior temporal gyrus of a monkey performing a delayed match-to-sample task.
Figure 5: Individual variation in vocalizations.
Figure 6: Multimodal vocalizations.

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Acknowledgements

We thank Joost Maier and Kari Hoffman for their comments on the manuscript. We dedicate this review to Marc Hauser, our advisor, mentor and colleague. We hope this review will contribute to his vision of an ethologically-sound systems neuroscience.

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Authors and Affiliations

  1. Max Planck Institute for Biological Cybernetics, Spemannstrasse 38, Tübingen, 72076, Germany

    Asif A. Ghazanfar

  2. Department of Psychology, Yale University, Box 208205, New Haven, 06520-8205, Connecticut, USA

    Laurie R. Santos

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  1. Asif A. Ghazanfar
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Correspondence to Asif A. Ghazanfar.

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FURTHER INFORMATION

Encyclopedia of Life Sciences

Apes

New World Monkeys

Old World Monkeys

Glossary

MIDDLE TEMPORAL VISUAL AREA

An extrastriate visual cortical area that is important for the analysis of visual motion.

MEYNERT CELLS

Specialized pyramidal neurons found in the primary visual cortex.

BETZ CELLS

Giant pyramidal neurons that are located in layer V of the primary motor cortex. Their axons project to the spinal cord, terminating directly on motor neurons.

MACHIAVELLIAN AGENT

An agent that can make or break alliances to serve his/her selfish needs.

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Ghazanfar, A., Santos, L. Primate brains in the wild: the sensory bases for social interactions. Nat Rev Neurosci 5, 603–616 (2004). https://doi.org/10.1038/nrn1473

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