Toward an evolutionary perspective on conceptual representation: species-specific calls activate visual and affective processing systems in the macaque.
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.
Gil-da-Costa
Ricardo
R
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, USA.
Braun
Allen
A
Lopes
Marco
M
Hauser
Marc D
MD
Carson
Richard E
RE
Herscovitch
Peter
P
Martin
Alex
A
D000161:Acoustic Stimulation; D000818:Animals; D005075:Biological Evolution; D001921:Brain / Q000502:physiology*; D003210:Concept Formation / Q000502:physiology*; D004594:Electrophysiology; D005260:Female; D008253:Macaca mulatta / Q000502:physiology*; D008279:Magnetic Resonance Imaging; D008297:Male; D049268:Positron-Emission Tomography; D013045:Species Specificity; D014796:Visual Perception / Q000502:physiology*; D014828:Vocalization, Animal