Spatial encoding in primate hippocampus during free navigation

Courellis, Hristos; Nummela, Samuel U.; Metke, Michael; Diehl, Geoffrey W.; Bussell, Robert H.; Cauwenberghs, Gert; Miller, Cory T.

doi:10.1371/journal.pbio.3000546

Cited by 78 publications

(96 citation statements)

References 90 publications

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“…Hence, visual inputs posterior of the precuneus (and the retrosplenial cortex just anterior to it) may hold precursor representations for egocentric vector coding neurons. In primates, which have a greater reliance on vision, spatial view cells [G] 93 have been found in the hippocampus, alongside place cells 94 . The former may be the product of a coordinate transform 95 , similar to that proposed for boundary and object vector cells.…”

Section: [H2] Sensory Input Underlying Egocentric Codingmentioning

confidence: 99%

Neuronal vector coding in spatial cognition

2020

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Several types of neurons involved in spatial navigation and memory encode the distance and direction (that is, the vector) between an agent and items in its environment. Such vectorial information provides a powerful basis for spatial cognition by representing the geometric relationships between the self and the external world. Here, we review the explicit encoding of vectorial information by neurons in and around the hippocampal formation, far from the sensory periphery. The parahippocampal, retrosplenial and parietal cortices, as well as the hippocampal formation and striatum, provide a plethora of examples of vector coding at the single neuron level. We provide a functional taxonomy of cells with vectorial receptive fields as reported in experiments and proposed in theoretical work. The responses of these neurons may provide the fundamental neural basis for the (bottom-up) representation of environmental layout and (top-down) memoryguided generation of visuo-spatial imagery and navigational planning. [H1] Introduction Place cells fire whenever an animal traverses a specific location in an environment (the spatial receptive field [G] of that neuron, also known as its 'place field', FIG. 1a). Since the discovery of place cells in the rat hippocampus by O'Keefe and Dostrovsky 1 , researchers have uncovered a multitude of additional spatially-selective cell types in rodents: that is, neurons whose receptive fields reference some aspect of an organism's location, state of motion, pose or its relationship to environmental features (such as boundaries, landmarks and other objects). The spatial receptive fields of some of these cells correspond to vectors, indicating the distance and direction in space (relative to the animal's current location) within which the presence of an environmental feature will drive the neuron to fire. Such 'vectorial codes' for space have received comparatively less attention than the coding performed by place cells or other well-known spatially-selective cell types, such as grid cells [G] 2 (FIG. 1a) and head direction cells [G] 3,4. Vectorial codes for space are expressed by boundary vector cells 5,6 , border cells 7,8 , landmark vector cells 9 and object vector cells 10 in allocentric (that is, world-centered) coordinates. Just like place fields, the receptive fields of these vector-coding cells do not reflect the orientation of the animal but do rotate together with the prominent environmental features that control head direction cell firing 11. Egocentric counterparts of some of these cells-in which the direction of receptive fields are referenced relative to the facing direction of the agent-have also been found 12-15 , as well as cells that exhibit head direction-modulated boundary responses 16,17 .

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Section: [H2] Sensory Input Underlying Egocentric Codingmentioning

confidence: 99%

Neuronal vector coding in spatial cognition

2020

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“…One potential reason why phase precession has not previously been observed in humans is because human theta oscillations often appear at a slower and broader range of frequencies compared to those seen in rodents 43,62,63 . We specifically assessed phase precession relative to the broader range of theta frequency (2-10 Hz) fluctuations of the LFP, in line with the recent discoveries of phase precession in bats 55 and marmosets 64 -two animals with similarly heterogeneous theta oscillations. Our findings are also consistent with findings from rodents, who continue to show phase precession even when LFP theta power and theta-modulated spiking are reduced 25,65,66 .…”

Section: Discussionmentioning

confidence: 99%

Phase precession in the human hippocampus and entorhinal cortex

Qasim

Fried

Jacobs

2020

Preprint

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Knowing where we are, where we have been, and where we are going is critical to many behaviors, including navigation and memory. One potential neuronal mechanism underlying this ability is phase precession, in which spatially tuned neurons represent sequences of positions by activating at progressively earlier phases of local network theta (~5-10~Hz) oscillations. Phase precession may be a general neural pattern for representing sequential events for learning and memory. However, phase precession has never been observed in humans. By recording human single-neuron activity during spatial navigation, we show that spatially tuned neurons in the human hippocampus and entorhinal cortex exhibit phase precession. Furthermore, beyond the neural representation of locations, we show evidence for phase precession related to specific goal-states. Our findings thus extend theta phase precession to humans and suggest that this phenomenon has a broad functional role for the neural representation of both spatial and non-spatial information.

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“…While self-position may not be robustly encoded by the NHP's hippocampus, as it is in rodents (Courellis et al, 2019), cells that are distinctly tuned to other aspects of experience have been reported in NHP (i.e. cells tuned to reward locations and objects) .…”

Section: Comparison To Rodent Swrmentioning

confidence: 95%

Unexpected changes in learned task contingencies trigger sharp wave ripples in the primate hippocampus during virtual navigation

McIntosh¹,

Corrigan²,

Gulli³

et al. 2020

Preprint

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The hippocampi and mesial temporal lobes play a central role in episodic memory and associative learning. It is unclear how unexpected experience influences learning. Hippocampal sharp wave ripples (SWR) are an electrical biomarker of memory consolidation. We tracked when and where SWR occur during 2 tasks. Local field potentials were recorded in the hippocampi, entorhinal cortices and amygdalae of non-human primates (NHP; n=3) performing reversal and associative learning tasks in a 3D virtual environment. Our results show hippocampal SWR occurred when learned task contingencies were unexpectedly altered. Surprise rewards and reward denial were associated with SWR rates 9.8x and 8.0x greater than expected rewards. The highest density of SWR occurred in zones where errors were made. SWR were preceded by event-related potentials in the amygdala but not entorhinal cortex. Our results suggest that SWR generation in primates may prioritize behaviourally relevant experience for commitment to memory to allow flexible learning.

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Spatial encoding in primate hippocampus during free navigation

Cited by 78 publications

References 90 publications

Neuronal vector coding in spatial cognition

Neuronal vector coding in spatial cognition

Phase precession in the human hippocampus and entorhinal cortex

Unexpected changes in learned task contingencies trigger sharp wave ripples in the primate hippocampus during virtual navigation

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