Spatial representation by ramping activity of neurons in the retrohippocampal cortex

Abstract

Neurons in the retrohippocampal cortices play crucial roles in spatial memory. Many retrohippocampal neurons have firing fields that are selectively active at specific locations, with memory for rewarded locations associated with reorganisation of these firing fields. Whether this is the sole strategy for representing spatial memories is unclear. Here, we demonstrate that during a spatial memory task retrohippocampal neurons encode location through ramping activity that extends within segments of a linear track approaching and following a reward, with the rewarded location represented by offsets or switches in the slope of the ramping activity. These ramping representations could be maintained independently of trial outcome and cues that mark the reward location, indicating that they result from recall of the track structure. During recordings in an open arena, neurons that generated ramping activity during the spatial memory task were more numerous than grid or border cells, with a majority showing spatial firing that did not meet criteria for classification as grid or border representations. Encoding of rewarded locations through offsets and switches in the slope of ramping activity also emerged in recurrent neural networks trained to solve a similar location memory task. Impaired performance of these networks following disruption of outputs from ramping neurons is consistent with this coding strategy supporting navigation to recalled locations of behavioural significance. We hypothesise that retrohippocampal ramping activity mediates readout of learned models for goal-directed navigation.