Spatial modulation of hippocampal activity in freely moving macaques

D, Mao; Avila, Eric; Caziot, Baptiste; Laurens, Jean; Dickman, J. David; Angelaki, Dora E.

doi:10.1016/j.neuron.2021.09.032

Cited by 87 publications

(159 citation statements)

References 85 publications

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“…Visuo-oculomotor and HC regions are structurally connected through a distributed set of polysynaptic routes (Shen et al, 2016), setting the stage for a functional connection between the areas. In line with this notion, previous work demonstrated that saccades coordinate neuronal activity in the HC (Doucet et al, 2020; Hoffman et al, 2013; Jutras et al, 2013; Mao et al, 2021; Staudigl et al, 2022) and other medial temporal lobe regions (Ringo et al, 1994; Sobotka et al, 1997; Sobotka and Ringo, 1997), as well as the functional connectivity between regions (Sobotka et al, 2002; Staudigl et al, 2022). Our results support and expand these findings, showing that the VC (and to a lesser degree the FEF) drove HC activity by means of excitatory coupling when participants made saccades.…”

Section: Discussionmentioning

confidence: 75%

“…During free viewing, saccadic eye movements target distinct features of the visual scene to accumulate information (Henderson, 2017; Pertzov et al, 2009; Renninger et al, 2007) in support of memory (Bicanski and Burgess, 2019; Fehlmann et al, 2020; Lucas et al, 2019; Meister and Buffalo, 2016; Olsen et al, 2016). Direct electrophysiological recordings from both humans and non-human primates uncovered that saccades affect neuronal activity in the hippocampus (Doucet et al, 2020; Hoffman et al, 2013; Mao et al, 2021; Staudigl et al, 2022), surrounding medial temporal lobe regions (Ringo et al, 1994; Sobotka et al, 1997; Sobotka and Ringo, 1997), and the functional connectivity between them (Sobotka et al, 2002; Staudigl et al, 2022). Jutras and colleagues (2013) demonstrated that saccades induced a phase reset of hippocampal theta oscillations (3-12 Hz) when monkeys visually scanned images and that the reliability of this effect predicted subsequent recognition memory (Jutras et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

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Saccades are coordinated with directed circuit dynamics and stable but distinct hippocampal patterns that promote memory formation

Wagner

Jensen

Doeller

et al. 2022

Preprint

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During natural viewing, humans explore their environment by moving the eyes - a process that involves saccades to guide attention and shape memory. Saccades are controlled by visuo-oculomotor regions and are known to impact medial temporal lobe processing, but the circuit dynamics in humans are unclear. Here, we asked which of the functional routes between the visual cortex, frontal eye fields, and the hippocampus facilitates memory encoding during visual exploration and whether saccades affect neural representations. Forty-eight human participants underwent functional magnetic resonance imaging (fMRI) and continuous monitoring of eye gaze while studying scenes and performing a recognition memory test thereafter. We discovered saccade-related excitatory coupling from the visual cortex and frontal eye fields towards the hippocampus, independent of memory. This was complemented by hippocampal inhibition of the visual cortex that determined whether participants would later remember or forget. Moreover, saccades were associated with overall stable but distinct hippocampal voxel patterns during memory formation and the degree of pattern distinctiveness positively scaled with inhibition along the hippocampus-to-visual cortex route. This suggests that eye movements are timed to the orchestration of circuit connectivity and neural representations, setting the stage for memory formation.

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Section: Discussionmentioning

confidence: 75%

Section: Introductionmentioning

confidence: 99%

Saccades are coordinated with directed circuit dynamics and stable but distinct hippocampal patterns that promote memory formation

Wagner

Jensen

Doeller

et al. 2022

Preprint

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“…Units in the hippocampus of Egyptian fruit bats and big brown bats show conjunctive sensitivity to location and head direction when the bats are engaged in crawling behavior (Rubin et al, 2014), similar to the units that were classified as “partially active” in our model. These units also show similarities to hippocampal cells in macaques which are selective to the monkey’s heading direction and position (Mao et al, 2021). Finally, the vector-like representations share properties with the egocentric cue direction cells discovered by (Wilber et al, 2014) in the parietal cortex while engaged in an aiming task.…”

Section: Discussionmentioning

confidence: 87%

Navigation task and action space drive the emergence of egocentric and allocentric spatial representations

Vijayabaskaran

Cheng

2022

Preprint

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In general, strategies for spatial navigation could employ one of two spatial reference frames: egocentric or allocentric. Notwithstanding intuitive explanations, it remains unclear however under what circumstances one strategy is chosen over another, and how neural representations should be related to the chosen strategy. Here, we first use a deep reinforcement learning model to investigate whether a particular type of navigation strategy arises spontaneously during spatial learning without imposing a bias onto the model. We then examine the spatial representations that emerge in the network to support navigation. To this end, we study two tasks that are ethologically valid for mammals – guidance, where the agent has to navigate to a goal location fixed in allocentric space, and aiming, where the agent navigates to a visible cue. We find that when both navigation strategies are available to the agent, the solutions it develops for guidance and aiming are heavily biased towards the allocentric or the egocentric strategy, respectively, as one might expect. Nevertheless, the agent can learn both tasks using either type of strategy. Furthermore, we find that place-cell-like allocentric representations emerge preferentially in guidance when using an allocentric strategy, whereas egocentric vector representations emerge when using an egocentric strategy in aiming. We thus find that alongside the type of navigational strategy, the nature of the task plays a pivotal role in the type of spatial representations that emerge.

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“…Historically, most hippocampal place cell studies have been conducted in freely moving rats and mice and there has been some question as to whether place cells behave similarly in primates. In the first study of spatial coding in freely moving macaques, Mao et al (36) found hippocampal neurons that were more complex than those described in rodents and which were tuned to many different spatial variables, including horizontal position, head height, linear speed, azimuth head direction, head tilt, head-facing location in 3 dimensions, egocentric boundary (i.e., relative to the arena boundary) and angular head velocity. They observed that the firing of hippocampal neurons was mainly modulated by position (26%), speed (22%), and head direction (41%), with 26% exhibiting conjunctive firing.…”

Section: Reproduced From Nguyen Et Al ( )mentioning

confidence: 99%

“…lateralized, even in rats. Perhaps the most important study is that by Mao et al (36), which demonstrates for the first time that the nature of spatially-responsive hippocampal neurons in primates may be much more complex than predicted from studies in rats and mice and that therefore the effects of vestibular loss may be similarly complex.…”

Section: Reproduced From Nguyen Et Al ( )mentioning

confidence: 99%

Recent developments in the understanding of the interactions between the vestibular system, memory, the hippocampus, and the striatum

Smith

2022

Front. Neurol.

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Over the last two decades, evidence has accumulated to demonstrate that the vestibular system has extensive connections with areas of the brain related to spatial memory, such as the hippocampus, and also that it has significant interactions with areas associated with voluntary motor control, such as the striatum in the basal ganglia. In fact, these functions are far from separate and it is believed that interactions between the striatum and hippocampus are important for memory processing. The data relating to vestibular-hippocampal-striatal interactions have considerable implications for the understanding and treatment of Alzheimer's Disease and Parkinson's Disease, in addition to other neurological disorders. However, evidence is accumulating rapidly, and it is difficult to keep up with the latest developments in these and related areas. The aim of this review is to summarize and critically evaluate the relevant evidence that has been published over the last 2 years (i.e., since 2021), in order to identify emerging themes in this research area.

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Spatial modulation of hippocampal activity in freely moving macaques

Cited by 87 publications

References 85 publications

Saccades are coordinated with directed circuit dynamics and stable but distinct hippocampal patterns that promote memory formation

Saccades are coordinated with directed circuit dynamics and stable but distinct hippocampal patterns that promote memory formation

Navigation task and action space drive the emergence of egocentric and allocentric spatial representations

Recent developments in the understanding of the interactions between the vestibular system, memory, the hippocampus, and the striatum

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