Toward an evolutionary perspective on conceptual representation: Species-specific calls activate visual and affective processing systems in the macaque

doi:10.1073/pnas.0408077101

Toward an evolutionary perspective on conceptual representation: Species-specific calls activate visual and affective processing systems in the macaque

^*National Institute on Deafness and Other Communication Disorders, ^†National Institute of Mental Health, and ^¶Positron Emission Tomography Department, Clinical Center, National Institutes of Health, Bethesda, MD 20892; ^‡Department of Psychology, Harvard University, Cambridge, MA 02138; and ^§Program in Biology and Medicine, Gulbenkian Science Institute, 2780 Oeiras, Portugal

Communicated by Leslie G. Ungerleider, National Institutes of Health, Bethesda, MD, October 29, 2004 (received for review August 17, 2004)

Abstract

Non-human primates produce a diverse repertoire of species-specific calls and have rich conceptual systems. Some of their calls are designed to convey information about concepts such as predators, food, and social relationships, as well as the affective state of the caller. Little is known about the neural architecture of these calls, and much of what we do know is based on single-cell physiology from anesthetized subjects. By using positron emission tomography in awake rhesus macaques, we found that conspecific vocalizations elicited activity in higher-order visual areas, including regions in the temporal lobe associated with the visual perception of object form (TE/TEO) and motion (superior temporal sulcus) and storing visual object information into long-term memory (TE), as well as in limbic (the amygdala and hippocampus) and paralimbic regions (ventromedial prefrontal cortex) associated with the interpretation and memory-encoding of highly salient and affective material. This neural circuitry strongly corresponds to the network shown to support representation of conspecifics and affective information in humans. These findings shed light on the evolutionary precursors of conceptual representation in humans, suggesting that monkeys and humans have a common neural substrate for representing object concepts.

Footnotes

↵ ∥ To whom correspondence should be addressed at: Laboratory of Brain and Cognition, National Institute of Mental Health, National Institutes of Health, Building 10, Room 4C-104, Bethesda, MD 20892-1366. E-mail: alexmartin{at}mail.nih.gov.
Author contributions: R.G.-d.-C., A.B., M.D.H., and A.M. designed research; R.G.-d.-C. and M.L. performed research; R.G.-d.-C., A.B., and A.M. analyzed data; R.G.-d.-C., A.B., M.D.H., and A.M. wrote the paper; R.G.-d.-C. and M.L. performed animal training; M.D.H. supplied the species-specific stimuli (coos and screams); and R.E.C. and P.H. provided assistance with the PET design and scanning.
Abbreviations: FEF, frontal eye fields; MST, medial superior temporal; MT, middle temporal; PET, positron-emission tomography; rCBF, regional cerebral blood flow; STG, superior temporal gyrus; STS, superior temporal sulcus; VMPFC, ventral medial prefrontal cortex.