The hippocampus comprises two neural signals—place cells and θ oscillations—that contribute to facets of spatial navigation. Although their complementary relationship has been well established in rodents, their respective contributions in the primate brain during free navigation remains unclear. Here, we recorded neural activity in the hippocampus of freely moving marmosets as they naturally explored a spatial environment to more explicitly investigate this issue. We report place cells in marmoset hippocampus during free navigation that exhibit remarkable parallels to analogous neurons in other mammalian species. Although θ oscillations were prevalent in the marmoset hippocampus, the patterns of activity were notably different than in other taxa. This local field potential oscillation occurred in short bouts (approximately .4 s)—rather than continuously—and was neither significantly modulated by locomotion nor consistently coupled to place-cell activity. These findings suggest that the relationship between place-cell activity and θ oscillations in primate hippocampus during free navigation differs substantially from rodents and paint an intriguing comparative picture regarding the neural basis of spatial navigation across mammals.
Faces and voices are the dominant social signals used to recognize individuals amongst human and nonhuman primates. Yet, evidence that information across these signals can be integrated into a modality-independent representation of individual identity in the primate brain has been reported only in human patients. Here we show that, like humans, single neurons in the marmoset monkey hippocampus exhibit invariant neural responses when presented with the faces or voices of specific individuals. However, we also identified a population of single neurons in hippocampus that were responsive to the cross-modal identity of multiple conspecifics, not only a single individual. An identity network model revealed population-level, cross-modal representations of individuals in hippocampus, underscoring the broader contributions of many neurons to encode identity. This pattern was further evidenced by manifold projections of population activity which likewise showed separability of individuals, as well as clustering for family members, suggesting that multiple learned social categories are encoded as related dimensions of identity in hippocampus. The constellation of findings presented here reveal a novel perspective on the neural basis of identity representations in primate hippocampus as being both invariant to modality and comprising multiple levels of acquired social knowledge.
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