Single neurons in the human medial temporal lobe flexibly shift representations across spatial and memory tasks

Abstract

Investigations into how individual neurons encode behavioral variables of interest have revealed specific representations in single neurons, such as place and object cells, as well as a wide range of cells with conjunctive encodings or mixed selectivity. However, as most experiments examine neural activity within individual tasks, it is currently unclear if and how neural representations change across different task contexts. Within this discussion, the medial temporal lobe is particularly salient, as it is known to be important for multiple behaviors including spatial navigation and memory, however the relationship between these functions is currently unclear. Here, to investigate how representations in single neurons vary across different task contexts in the medial temporal lobe, we collected and analyzed single-neuron activity from human participants as they completed a paired-task session consisting of a passiveviewing visual working memory and a spatial navigation and memory task. Five patients contributed 22 paired-task sessions, which were spike sorted together to allow for the same putative single neurons to be compared between the different tasks. Within each task, we replicated concept-related activations in the working memory task, as well as target-location and serial-position responsive cells in the navigation task. When comparing neuronal activity between tasks, we first established that a significant number of neurons maintained the same kind of representation, responding to stimuli presentations across tasks. Further, we found cells that changed the nature of their representation across tasks, including a significant number of cells that were stimulus responsive in the working memory task that responded to serial position in the spatial task. Overall, our results support a flexible encoding of multiple, distinct aspects of different tasks by single neurons in the human medial temporal lobe, whereby some individual neurons change the nature of their feature coding between task contexts.

Hippocampal spatial view cells, place cells, and concept cells: View representations

“…Interesting evidence that in humans medial temporal lobe neurons can respond differently in different tasks (navigation vs. n-back memory) was presented in this Special Issue (Donoghue et al, 2023). There is some consistent evidence in macaques, as follows.…”

“…Several contributions to the Special Issue of Hippocampus (2023) provide evidence that many primate hippocampal neurons respond to the location being viewed "out there," not the place where the individual is located (Corrigan et al, 2023;Rolls, 2023b;Wirth, 2023;Zhu et al, 2023). Complementary evidence is also available for humans, in that in another paper in this Special Issue of Hippocampus, it was found that significant numbers of spatial view cells but not a significant number of place cells were found in the medial temporal lobe in a VR navigation task to the remembered location in a scene of a Treasure Chest (Donoghue et al, 2023). The spatial coordinates of these view cell representations are considered next.…”

“…The task dependence of hippocampal neurons in macaques is echoed by the findings in humans (Donoghue et al, 2023). However, the finding that individual human medial temporal lobe neurons can respond to different task variables in different tasks (Donoghue et al, 2023) needs further comment.…”

“…They were not able to determine what coordinate framework (allocentric or egocentric) was being used. In humans, the 'target neurons' found in the medial temporal lobe in the Treasure Hunt task (Donoghue et al, 2023;Tsitsiklis et al, 2020) can be considered as being responsive to spatial views. The responses of these spatial-target cells are consistent with allocentric encoding, since they responded to a specific viewed spatial location in the environment, from multiple different subject places, such that the egocentric orientation of the subject with respect to the target location varied.…”

“…In these cases, identifiable environmental features identify each location, and spatial view cells encode the features in these locations, and their spatial overlap with features of nearby locations. The mechanism proposed is the learning of spatial associations in a continuous attractor network (Rolls et al, 2008;Rolls, Deco, et al, 2023a;Stringer et al, 2005) using spatial view cells (Donoghue et al, 2023;Georges-François et al, 1999;Robertson et al, 1998;Rolls, 2022;Rolls et al, 1998;Rolls, Robertson, & Georges-François, 1997;Rolls & Wirth, 2018;Tsitsiklis et al, 2020;Wirth et al, 2017) in the parahippocampal scene (or place) area, which in turn connects to the hippocampus to provide the "where" component of episodic memory (Rolls, 2023b;Rolls et al, 2022b;Rolls, Deco, et al, 2023a). A model of navigation towards viewed locations in scenes with intermediate viewed locations that use spatial view cells, and that can include whole body motion/body turn ("speed") cells (O'Mara et al, 1994), has been described (Rolls, 2021b).…”