Cross-Modal Representation of Identity in Primate Hippocampus

Abstract

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.

Invariant crossmodal equivalence evokes visual imagery from sounds in rhesus monkeys

“…The fact that our monkeys learned numerous crossmodal associations should not be surprising since, in nature, monkeys recognize alarm calls about predators (Seyfarth et al, 1980). Moreover, there is evidence that neurons in the monkey's hippocampus respond invariantly to the face and voice of conspecifics in the colony (Tyree et al, 2023).…”

The neurobiology of vocal communication in marmosets

“…222 A recent study in marmosets suggests that the hippocampus may be integral to the cross-modal integration of faces and voices for cohesive representations of individual identity. 104 Tyree et al 104 showed that, like humans, 223 individual neurons in the marmoset were highly selective to specific individuals when seeing their faces or hearing their voices.…”

“…Both macaque 91 and marmoset 90 frontal lobes contain patches of face-selective cells, which are integrated with more extensive face processing and voice processing networks. 85,88,[216][217][218][219][220] Primates match the identity of an individual across their face and voice, 104,221 though data on how these social signals are integrated for social recognition at the neural level are only beginning to emerge. 222 A recent study in marmosets suggests that the hippocampus may be integral to the cross-modal integration of faces and voices for cohesive representations of individual identity.…”

“…Primates match the identity of an individual across their face and voice, 104,221 though data on how these social signals are integrated for social recognition at the neural level are only beginning to emerge 222 . A recent study in marmosets suggests that the hippocampus may be integral to the cross‐modal integration of faces and voices for cohesive representations of individual identity 104 . Tyree et al 104 .…”

“…Indeed, Jafari et al 88 report the activation of several subcortical areas in response to hearing vocalizations and suggest these are part of a larger vocal processing network. Other subcortical areas have been implicated in the integration of auditory information across modalities, such as the hippocampus integrating individual identity from faces and voices 104 and the amygdala extracting affective information from the auditory input. 105,106 However, only a limited number of studies have specifically targeted subcortical substrates in the context of vocalizations in marmosets.…”