Neurophysiological coding of space and time in the hippocampus, entorhinal cortex, and retrosplenial cortex

Abstract

Neurophysiological recordings in behaving rodents demonstrate neuronal response properties that may code space and time for episodic memory and goal-directed behaviour. Here, we review recordings from hippocampus, entorhinal cortex, and retrosplenial cortex to address the problem of how neurons encode multiple overlapping spatiotemporal trajectories and disambiguate these for accurate memory-guided behaviour. The solution could involve neurons in the entorhinal cortex and hippocampus that show mixed selectivity, coding both time and location. Some grid cells and place cells that code space also respond selectively as time cells, allowing differentiation of time intervals when a rat runs in the same location during a delay period. Cells in these regions also develop new representations that differentially code the context of prior or future behaviour allowing disambiguation of overlapping trajectories. Spiking activity is also modulated by running speed and head direction, supporting the coding of episodic memory not as a series of snapshots but as a trajectory that can also be distinguished on the basis of speed and direction. Recent data also address the mechanisms by which sensory input could distinguish different spatial locations. Changes in firing rate reflect running speed on long but not short time intervals, and few cells code movement direction, arguing against path integration for coding location. Instead, new evidence for neural coding of environmental boundaries in egocentric coordinates fits with a modelling framework in which egocentric coding of barriers combined with head direction generates distinct allocentric coding of location. The egocentric input can be used both for coding the location of spatiotemporal trajectories and for retrieving specific viewpoints of the environment. Overall, these different patterns of neural activity can be used for encoding and disambiguation of prior episodic spatiotemporal trajectories or for planning of future goal-directed spatiotemporal trajectories.

Boundary cells in the representation of episodes in the human hippocampus

“…The identification of Boundary cells in the MTL helps explicate the electro-physiological mechanisms supporting episodic memory, and their properties have the potential to inform models of mnemonic processing. Boundary cells may provide an “anchor” signal to promote context reinstatement in models such as the temporal context model (Alexander, Robinson, et al, 2020; Hinman et al, 2019; Julian et al, 2018). Boundary signals further establish important parallels between spatial navigation in rodent models and episodic associations in humans (Alexander, Robinson, et al, 2020; Barry et al, 2006; Horner et al, 2016; van Wijngaarden et al, 2020; Zheng et al, 2021).…”

“…Boundary cells may provide an “anchor” signal to promote context reinstatement in models such as the temporal context model (Alexander, Robinson, et al, 2020; Hinman et al, 2019; Julian et al, 2018). Boundary signals further establish important parallels between spatial navigation in rodent models and episodic associations in humans (Alexander, Robinson, et al, 2020; Barry et al, 2006; Horner et al, 2016; van Wijngaarden et al, 2020; Zheng et al, 2021). The significant theta phase locking among Boundary cells specifically during boundary representation may provide a direct mechanism for integration of episodic information with other populations in the MTL and cortex, potentially incorporating inter-regional phase amplitude coupling (D. X.…”

“…We note that these preliminary findings echo our own results in which boundary activity was a negative predictor of temporal clustering behavior. Such alternate paradigms may further explicate whether Boundary cells can fill a hypothesized role as an “anchor” signal in episodic representations (Alexander, Robinson, et al, 2020), as boundary information can theoretically provide an internal cue for guiding the “tracing” characteristic of episodic representations (Alexander, Robinson, et al, 2020; Bicanski & Burgess, 2020; Bicanski & Burgess, 2018). However, our own data do not test this idea, since the free recall paradigm cannot identify Boundary cell activity that is unique for different contexts.…”

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

“…During free navigation, both types of information are likely to be acquired simultaneously. 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).…”

Retrosplenial and hippocampal synchrony during retrieval of old memories in macaques

“…Both the hippocampus and retrosplenial cortex are important structures for forming long-lasting memories of spatiotemporally distinct events (1-2). The neural mechanisms within these structures that give rise to retrieval over large time spans is unclear, though the retrosplenial cortex may assume a greater, more independent role over time (3)(4)(5)(6)(7)(8)(9). Tests of this role have been limited by i. species-adapted tasks in rodents that use shorter delays and restricted memorandum, ii.…”