Consistency of Spatial Representations in Rat Entorhinal Cortex Predicts Performance in a Reorientation Task

• Published in: Current biology Vol. 27; no. 23; pp. 3658 - 3665.e4
• Main Authors: Weiss, Shahaf, Talhami, Ghadeer, Gofman-Regev, Xenia, Rapoport, Sophia, Eilam, David, Derdikman, Dori
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 04.12.2017
• Subjects: Animals; behavior; cognitive map; entorhinal; Entorhinal Cortex - physiology; grid cells; head-direction cells; Male; MEC; memory systems; Orientation, Spatial - physiology; Rats - physiology; Rats, Long-Evans; reorientation; signal reliability; Space Perception - physiology; spatial disorientation; spatial perception; spatial disorientation; head-direction cells; memory systems; grid cells; MEC; entorhinal; spatial perception; behavior; signal reliability; cognitive map; reorientation
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2017.10.015

Goal-directed behavior can be affected by environmental geometry. A classic example is the rectangular arena reorientation task, where subjects commonly confuse opposite but geometrically identical corners [1]. Until recently, little was known about how environmental geometry shapes spatial representations in a neurobehavioral context [2] (although see [3]). In the present study, we asked: Under what circumstances does the internal cognitive map predict behavior? And when does it fail to do so? To this end, we developed a variant of the classical reorientation task that allows for investigation of temporal dynamics of reorientation. We recorded head-direction (HD) cells and grid cells in the medial entorhinal cortex (MEC) of rats before, during, and after performing the task. MEC cells showed a bimodal response of being either aligned or rotated, relative to the free-foraging open-field sessions. Alignment was remarkably stable between disorientations and indicative of corner choice as a function of current and past alignment of spatial representations. Accordingly, when the cells showed consistent and properly aligned readout across multiple trials, behavioral choices were better predicted by HD and grid cell readout, with a probability of more than 70%. This was not the case when the cells did not show a stable consistent readout. Our findings indicate that entorhinal spatial representations predict corner choice, contingent on the stability and reliability of their readout. This work sets the stage for further studies on the link between the reliability of the neuronal signal and behavior, with implications for many brain systems in many organisms. •Entorhinal grid and head-direction maps show remarkable stability•Disorientation occasionally leads to rotation of these maps•Behavior does not influence the rotation of entorhinal maps•Use of entorhinal maps for wayfinding is dependent on memory of signal reliability Using a variation of the reorientation task, Weiss et al. find a role for the stability of orientation signals in the entorhinal cortex of rats. Alignment and stability of past and present representations predict corner choice and highlight the connection between reliability of the neuronal signal and behavioral decisions.