Dataset Information

Spatial modulation of hippocampal activity in freely moving macaques.

ABSTRACT: The hippocampal formation is linked to spatial navigation, but there is little corroboration from freely moving primates with concurrent monitoring of head and gaze stances. We recorded neural activity across hippocampal regions in rhesus macaques during free foraging in an open environment while tracking their head and eye. Theta activity was intermittently present at movement onset and modulated by saccades. Many neurons were phase-locked to theta, with few showing phase precession. Most neurons encoded a mixture of spatial variables beyond place and grid tuning. Spatial representations were dominated by facing location and allocentric direction, mostly in head, rather than gaze, coordinates. Importantly, eye movements strongly modulated neural activity in all regions. These findings reveal that the macaque hippocampal formation represents three-dimensional (3D) space using a multiplexed code, with head orientation and eye movement properties being dominant during free exploration.

SUBMITTER: Mao D

PROVIDER: S-EPMC8571030 | biostudies-literature | 2021 Nov

REPOSITORIES: biostudies-literature

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Spatial modulation of hippocampal activity in freely moving macaques.

Mao Dun D Avila Eric E Caziot Baptiste B Laurens Jean J Dickman J David JD Angelaki Dora E DE

Neuron 20211012 21

The hippocampal formation is linked to spatial navigation, but there is little corroboration from freely moving primates with concurrent monitoring of head and gaze stances. We recorded neural activity across hippocampal regions in rhesus macaques during free foraging in an open environment while tracking their head and eye. Theta activity was intermittently present at movement onset and modulated by saccades. Many neurons were phase-locked to theta, with few showing phase precession. Most neuro ...[more]

PMID: 34644546

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Project description:Previous work has demonstrated remarkably reproducible and consistent hierarchies of neural timescales across cortical areas at rest. The question arises how such stable hierarchies give rise to adaptive behavior that requires flexible adjustment of temporal coding and integration demands. Potentially, this previously found lack of variability in the hierarchical organization of neural timescales could be a reflection of the structure of the laboratory contexts in which they were measured. Indeed, computational work demonstrates the existence of multiple temporal hierarchies within the same anatomical network when the input structure is altered. We posit that unconstrained behavioral environments where relatively little temporal demands are imposed from the experimenter are an ideal test bed to address the question of whether the hierarchical organization and the magnitude of neural timescales reflect ongoing behavioral demands. To tackle this question, we measured timescales of local field potential activity while rhesus macaques were foraging freely in a large open space. We find a hierarchy of neural timescales that is unique to this foraging environment. Importantly, although the magnitude of neural timescales generally expanded with task engagement, the brain areas' relative position in the hierarchy was stable across the recording sessions. Notably, the magnitude of neural timescales monotonically expanded with task engagement across a relatively long temporal scale spanning the duration of the recording session. Over shorter temporal scales, the magnitude of neural timescales changed dynamically around foraging events. Moreover, the change in the magnitude of neural timescales contained functionally relevant information, differentiating between seemingly similar events in terms of motor demands and associated reward. That is, the patterns of change were associated with the cognitive and behavioral meaning of these events. Finally, we demonstrated that brain areas were differentially affected by these behavioral demands - i.e., the expansion of neural timescales was not the same across all areas. Together, these results demonstrate that the observed hierarchy of neural timescales is context-dependent and that changes in the magnitude of neural timescales are closely related to overall task engagement and behavioral demands.

Dataset Information

Spatial modulation of hippocampal activity in freely moving macaques.

Publications

Spatial modulation of hippocampal activity in freely moving macaques.

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