A neural code for egocentric spatial maps in the human medial temporal lobe

Abstract

Spatial navigation relies on neural systems that encode spatial information relative to the external world or in relation to the navigating organism. Ever since the proposal of cognitive maps, the neuroscience of spatial navigation has focused on allocentric (world-referenced) neural representations such as place cells. Here, using single-neuron recordings during virtual 30 navigation, we reveal a neural code of egocentric (self-centered) spatial information in the human brain: We describe "anchor cells", which represent egocentric directions towards local "anchor points" distributed across the environmental center and periphery. Anchor-cell activity was abundant in parahippocampal cortex, signaled anchor-point distances, and showed memory modulation. Anchor cells may thus facilitate egocentric navigation 35 strategies, may assist in transforming percepts into allocentric spatial representations, and may underlie the first-person perspective in episodic memories. One Sentence Summary:Anchor cells in the human brain provide the neural basis for a self-centered coordinate 40 system during spatial navigation.3 Main text:Detailed neural representations of space form the neurobiological basis of successful navigation and accurate spatial memory. Traditionally, the neuroscience of spatial navigation has focused on allocentric representations, which encode spatial information in relation to the 45 external world: the place field of a place cell may be located in the "northeast" corner of an environment (1, 2), a head-direction cell may activate whenever navigating "south" (3), and a boundary vector/border cell may respond to a spatial boundary located "west" (4, 5). However, spatial environments are primarily experienced from a first-person, egocentric perspective -requiring neural codes that provide spatial information in relation to the self. 50 Via transformation circuits (6, 7), egocentric representations (8-10) may then be converted into their allocentric counterparts (4, 5, 11) for abstract knowledge and long-term storage (12).Despite abundant behavioral evidence that humans employ egocentric spatial information to accomplish wayfinding (12-15), little is known about the neural basis of egocentric spatial 55 representations in humans. Here, we hypothesized that neurons in human medial temporal lobe (MTL) keep track of the instantaneous relationship between the navigating subject and proximal areas of the environment. Specifically, we targeted the identification of "anchor cells" whose activity encodes the subject's egocentric direction towards local reference points (termed "anchor points"). Such a coding scheme would be instrumental for egocentric 60 navigation, because it provides orientation in relation to the proximal spatial layout.To detect and characterize human anchor cells, we recorded single-neuron activity from the MTL of ten neurosurgical epilepsy patients (table S1), while patients performed an objectlocation memory task in a virtual environment (Fig. 1, A and B). In this task (16), patients learne...

Post-encoding modulation of spatial memory by a GABAA-agonist

“…Subsequent fMRI-experiments in humans with a highly similar task showed that sequence-based navigation activates the left and landmark-based navigation activates the right hippocampus (Iglói et al, 2010). The impairments observed here fit these observations and further suggest that hippocampus-dependent networks provide computations relevant to early consolidation of allocentric as well as egocentric memory representations (Kunz et al, 2020;Johnsen and Rytter, 2021;Samanta et al, 2021). Alternatively, at least in our task, administration of propofol may have affected a central spatio-temporal binding process that yields seemingly distinct behavioral manifestations -depending on the particular navigational context imposed by the experimenter.…”

“…It is however unclear whether these representational modes can be clearly dissociated at the neural level (Ekstrom et al, 2014(Ekstrom et al, , 2017Alexander et al, 2020;Ladyka-Wojcik and Barense, 2021). While hippocampus and adjacent regions of the medial temporal lobe have traditionally been associated with allocentric spatial representations, recent research in animals and humans suggests an important role for egocentric memory as well (Kunz et al, 2020;Johnsen and Rytter, 2021;Samanta et al, 2021).…”

Hippocampal place cells use vector computations to navigate

“…The Honeycomb maze reveals the 2D nature of the pre-choice 'subjunctive' representation. 8 and in humans performing a multiple object-in-location VR test 11 . In the present experiment, these occurred in only 14% of the cells during a foraging task, fewer than half of the percentage seen during the navigation task, and further, were not clustered around the concurrent navigation goal.…”

“…When a goal is introduced, place cells become directional 8 and their fields move in the direction of the goal when it is moved 9 . Recent work has shown that cells in the dorsal hippocampus encode heading towards a goal and other locations in the bat 10 , mouse7 and human 11 .…”

Egocentric Asymmetric Coding in Sensory Cortical Border Cells

“…Vector coding (such as distance and direction) in spatial cognition is common for neurons within and around the hippocampal formation, far from the sensory periphery (Bicanski and Burgess, 2020). The spatial receptive fields (“vector codes”) of these neurons, are often expressed in the allocentric coordinates, such as in the cases of boundary vector cells (Lever et al, 2009), border cells (Solstad et al, 2008), landmark vector cells (Deshmukh and Knierim, 2013), object vector cells (Hoydal et al, 2019), visual cue cells (Kinkhabwala et al, 2020), human anchor cells (Kunz et al, 2021), border-elicited theta oscillation (Stangl et al, 2021), primate border cells (Killian et al, 2012) and vector trace cells (Poulter et al, 2021). Recently, egocentric representations of space have been reported in the PPC, RSC, lateral EC (LEC), postrhincal cortex, postsubiculum and dorsomedial striatum (Gofman et al, 2019; LaChance et al, 2019; Peyrache et al, 2017; Wang et al, 2018).…”