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Title: Gaze-informed, task-situated representation of space in primate hippocampus during virtual navigation}
Article:
Abstract:
To elucidate how gaze informs the construction of mental space during wayfinding in visual species like primates, we jointly examined navigation behavior, visual exploration, and hippocampal activity as macaque monkeys searched a virtual reality maze for a reward. Cells sensitive to place also responded to one or more variables like head direction, point of gaze, or task context. Many cells fired at the sight( and in anticipation) of a single landmark in a viewpoint- or task-dependent manner, simultaneously encoding the animal’s logical situation within a set of actions leading to the goal. Overall, hippocampal activity was best fit by a fine-grained state space comprising current position, view, and action contexts. Our findings indicate that counterparts of rodent place cells in primates embody multidimensional, task-situated knowledge pertaining to the target of gaze, therein supporting self-awareness in the construction of space.
Introduction:
Place cells are the quintessential signature of hippocampal neural activity in rodents and code the animal’s position in an environment[1, 2]. These neurons’ place selectivity and directionality strongly depend on the visual and/or vestibular cues, as has recently been shown in virtual reality settings in rodents[3–7]. Place cells are observed too in humans navigating virtual environments[8, 9] and in other primates in real and virtual environments[10–12]. Yet, there is no consensus on how hippocampal place cells found in monkeys or humans precisely compare to place cells in rodents in the real or virtual world. Previous work[10, 11] suggested that, unlike in rodents, space in the primate hippocampus may be coded in a gnostic, landmark-centered representation. Neurons in the monkey hippocampus were shown to convey much more information about the spatial view than about the place, eye position, or head direction. Although there was some modulation of spatial view responsiveness by place[13], the animal’s target of gaze( i. e., what the animal was looking at) was paramount in explaining firing rate[10]. These observations contradict other studies in macaques[14–16] and in humans in virtual reality mazes[8, 9] describing robust place-coding activity. In the latter human single-cell studies[8, 9], some cells were sensitive to the conjunction of place and goal or place and view, demonstrating complex task-related coding. However, as eye tracking was not feasible in these studies, neural activity was not analyzed with respect to eye movements and visual exploration. Thus, it remains unclear how active vision informs the neural construction of space at the single-cell level in the primate. In the present study, we probed the nature of hippocampal coding in a goal-oriented task, separating goal and visual landmarks, and examined jointly how cells code for position, direction, and target of gaze. The goal-oriented setting enabled us to examine whether the task-related context of navigation modulated the activity of the cells. We thus analyzed firing in a discrete state space in which the animal’s trajectory in the maze is segmented into elemental transitions from one state in the environment to another[17–19]. Though our results are limited to virtual reality( VR), the recent use of this technique in humans[9] and in rodents[3–7, 20] provides an apt comparison of the hippocampal coding in an environment in which spatial information is principally derived from visual input. In this framework, our results give a comprehensive and thorough analysis of the variables controlling the activity of hippocampal cells, bridging the gap between studies in rodents and in primates—including humans—collected in real and virtual environments. We show how hippocampal cells code for the target of gaze in an informed manner, embedding self-position with respect to elements in the environment and to action context. Thereby, we bring a new perspective on models of hippocampal spatial function by focusing on the role of the idiosyncratic visual exploration in primates in constructing a representation of the world that is highly useful to wayfinding.
Discussion:
Our findings were obtained in VR, and this technique has recently been a welcome substitution for the real world when exploring the neural basis of spatial cognition in humans and in animals[3–8, 27–32], as it allows a fine control of the environment. Nevertheless, this technique raises interpretative issues as to how well navigation in VR reflects its real-world counterpart. In a virtual setup like ours or those used for human fMRI, subjects lack real inputs from motor, vestibular, and proprioceptive systems. Importantly, the optic flow activates a common neural circuitry with vestibular input that underlies self-motion encoding[33]. Our virtual setup, which primarily simulated extrafoveal territory( 70° FOV), shares common properties with stimuli that are known to produce vection-like phenomena[34]. It is thus likely to produce an illusion of self-motion. The animals’ anticipatory gaze behavior, similar to human drivers[21, 35], confirms this interpretation. Previous experiments using VR in monkeys had animals travel well-learned routes[27], execute repetitive motion sequences[28], or search explicit visual goals[36]. Our animals’ use of landmarks—inferring the position of a goal dissociated from the landmarks themselves as in triangulation, a hallmark of hippocampal function[22, 37]—is novel, and the first replication in the monkey of aptitudes already shown in rats[31] and humans[30, 32] in a VR world. The signature of hippocampal activity in rodents is the coding by place cells of the animal’s current position[1]. Previous results in primates, including humans, showed that hippocampal cells encoded spatial views[10, 11], place[9, 14–16, 28, 38], or a mixture of place and view[8]. In a controlled VR wayfinding setting, the present findings show that hippocampal cells display a fine-grained tuning that preferentially codes one of the landmarks being viewed by the animal and its current self-position relative to the landmark. This shows that primate hippocampal cells also carry position information as rodent place cells do. Beyond that, however, we found that this tuning included trajectory-related contextual aspects and was best captured in a state space because the cells showed higher spike information content when compared to other coding spaces such as self-position, head direction, or point of gaze. Crucially, analysis of the firing rate in the center of the maze showed that the context truly gave additional information compared to a simple combination of position and direction( Fig 4). Further, as shown in Fig 5 and Fig 6, we found more cells than expected by chance that coded a combination between landmark viewed and distance to the landmark or that discriminated trajectories bearing views of the same landmark. Lastly, we observed that gazing on landmarks increases the cells’ selectivity to the path or trajectory bearing the landmark( Fig 7). In combination, these results imply that hippocampal spatial memory involves more than a simple spatial relation to the environment but rather a sensorimotor trajectory scheme in a goal-reaching context. Hippocampal cells responding to the spatial views have been previously reported[10, 13]. The identity of the views represented in those cells had precedence over position in explaining their activity. While our cells bear a resemblance to the ones described by Rolls and colleagues[10, 13], we found that complementary information relevant to position and action was also robustly encoded in the cellsʼ firing. This difference might be due to the task we used, in which the current viewpoint guides the next actions of the animal. Such imperative contingencies were absent in the studies by Rolls and colleagues. Our findings echo findings in rodents in which the activity of place cells depends on the goal of the trajectory[39, 40] or its retrospective and prospective components[41]. In addition, our results imply that hippocampal cells in the primate represent more than the spatial view[10, 11] or its associated reward value[42]. How can we interpret our results with respect to the animal’s behavior? As the same viewpoint for the same landmark, same heading, and same prospective action can be reliably discriminated for different trajectories, cells do not code the sensorimotor properties of the task only. Rather, we hypothesize that cells embody a dynamic knowledge about the self-position with respect to the landmarks in a contextual fashion, depending on the current trajectory. In fact, this conclusion extends previous reports that the rat hippocampus shows trajectory-dependent firing[41, 43, 44]. To what extent these effects are due to interactions within a broader network such as the prefronto–thalamo–hippocampal circuit[44] remains to be examined in the monkey. Our findings also underscore the power of the relationship between visual exploration and hippocampal activity. Indeed, visual exploration of the environment led by saccades and fixations is part of the primate-specific repertoire of active sensing and is supported by dedicated visual processing areas shared by human and other primates[45, 46]. In VR studies like ours, directions can be primarily obtained by visual information only, and accordingly, we observed that the point of gaze importantly modulates the hippocampal activity, as already shown by Rolls et al.[11, 13]. This is seen both in single examples( Fig 2) and by the high number of cells with spike information modulated by the point of gaze( Fig 3). The temporal dynamics of cell activity with respect to the landmark-directed saccades reveals that firing mostly follows landmark appearance but precedes the eyes reaching the landmark, suggesting an anticipatory identification of the landmark( Fig 7E–7G). Although the selectivity of hippocampal cells to the identity of the fixated landmark is reminiscent of object fixation cells in the inferotemporal cortex[47–49], hippocampal cells discriminate positions from which the landmarks are gazed at( Figs 4, 5 and 6). Further, we showed the firing rate at fixation was greatly modulated by the time period during which the landmark was fixated, with activity decreasing as the landmark was fixated long after it was already visible. This pattern is coherent with a task-contextual modulation of the cells. Moreover, landmark and path selectivity tuning is enhanced through foveation, suggesting that gaze information enhances coding of self-position. In sum, our data suggest that the counterpart of place cells in primates, as compared to rodents, is expressed as activity related to point of gaze in conjunction with other variables essential to navigation, such as position and identity of visual elements at key instants of trajectory planning. Recent rodent studies in VR provide a useful common framework to situate our findings and make cross-species comparisons[3–5]. Approximately 50% of our cells showed spatial selectivity like that in rats[3–5] and similar to that obtained in real-world settings[3, 50, 51]. Our results further confirm that spatial coding can be obtained in absence of vestibular and proprioceptive input. In addition, the number of fields per cell( average = 2. 7) was greater than the number of fields described in the rat( about 1. 5), but our maze differs from the single alleys and square or round open fields in the foregoing studies. Studies conducted in real, complex environments bearing path repetitions observe many neurons bearing more than one place field[52–54]. The nature of our task environment may thus have played a role in the multiplicity of hippocampal fields. In rodents, direction selectivity was thought to be exclusive to one-dimensional mazes; however, it was recently demonstrated to be present in two-dimensional environments[3, 7]. Our setup did not allow us to characterize direction selectivity in a strict independent way because direction and position often covaried. Thus, our results on the matter have to be taken with a note of caution. However, firing in the center of the maze displayed direction-dependent activity. Taken together, these findings contradict earlier results showing consistently direction-independent responses in 2-D environments[55, 56] and further demonstrate that direction selectivity is an essential property of place cells—as recently shown in VR in the rat[3, 7] and in the real world in bats[57]—and can be independent from vestibular cues. Note that direction selectivity was not preserved across spatial positions, suggesting its sensitivity to other variables such as visual cues or actions. Hence, we also observed that selectivity is stronger at choice points than at other places. Lastly, the strength of our cells’ signals( amplitude of firing rate, number of cells recruited) is more on par with that in the rodent or bats than in previous VR monkey studies, which appeared to engage hippocampal activity rather poorly[28, 38]. Our animals had to learn anew the significance of the landmark configuration during each recording session, whereas the aforementioned studies relied on a shuttle behavior between fixed reward zones, suggesting that dissimilar learning requirements account for the different firing rates. Studies in humans of hippocampal neuronal activity during spatial navigation are rare. Two studies[8, 9] provide arguments for homologies in hippocampal processing between nonhuman to human primates. In particular, Ekstrom and colleagues[8] described many cells that showed an interaction between place, goal, and view. The state space–selective cells observed in our study bear resemblances to the conjunctive cells they reported. Such a relationship could account for the interaction of place and goal found in the human hippocampus[8]. This conjunctive type of coding appears ubiquitous across mammalians, as our findings are consistent with the encoding of task-related demands by hippocampal neurons in rodents[58]. In sum, we show that space representation in primates embodies self-position with respect to the target of gaze and further carries cognitive information with respect to the current trajectory to a goal. These results clarify ambiguous results previously obtained in primates that suggested hippocampal neurons did not convey self-position but instead a spatial view[10, 11] or conveyed self-position but no cognitive information[12]. They also bridge the gap between results in rats and humans by showing that place cells support self-position in a cognitive map in primates as well and clarify how this coding is constructed through visual exploration and self-movement. For long the dominant view of hippocampal function has been influenced by the concept of place selectivity, with the hippocampus viewed as a “neural GPS, ” highlighting the actual position of the animal on an internal map. In contrast, our results, clarifying and considerably extending the early advances of Rolls and colleagues, suggest a different view of the hippocampus wherein distinct elements of sensory, motor, and cognitive information are linked in order to build a memory( here, a space-related one). In this framework, place fields appear as a mere projection of this memory onto physical space. These results support a new view of hippocampal function and are of relevance for the understanding of the organization of human hippocampal function and memory.
In the brain of mammalian species , the hippocampus is a key structure for episodic and spatial memory and is home to neurons coding a selective location in space ( “place cells” ) . These neurons have been mostly investigated in the rat . However , species such as rodents and primates have access to different olfactory and visual information , and it is still unclear how their hippocampal cells compare . By analyzing hippocampal activity of nonhuman primates ( rhesus macaques ) while they searched a virtual environment for a reward , we show that space coding is more complex than a mere position or orientation selectivity . Rather , space is represented as a combination of visually derived information and task-related knowledge . Here , we uncover how this multidimensional representation emerges from gazing at the environment at key moments of the animal’s exploration of space . We show that neurons are active for precise positions and actions related to the landmarks gazed at by the animals . Neurons were even found to anticipate the appearance of landmarks , sometimes responding to a landmark that was not yet visible . Overall , the place fields of primate hippocampal neurons appear as the projection of a multidimensional memory onto physical space .