Spatial Navigation and Hippocampal Place Cell Firing: The Problem of Goal Encoding

Abstract

Place cells are hippocampal neurons whose discharge is strongly related to a rat's location in the environment. The existence of such cells, combined with the reliable impairments seen in spatial tasks after hippocampal damage, has led to the proposal that place cells form part of an integrated neural system dedicated to spatial navigation. This hypothesis is supported by the strong relationships between place cell activity and spatial problem solving, which indicate that the place cell representation must be both functional and in register with the surroundings for the animal to perform correctly in spatial tasks. The place cell system nevertheless requires other essential elements to be competent, such as a component that specifies the overall goal of the animal and computes the path required to take the rat from its current location to the goal. Here, we propose a model of the neural network responsible for spatial navigation that includes goal coding and path selection. In this model, the hippocampal formation allows for place recognition, and stores the set of places that can be accessed from each position in the environment. The prefrontal cortex is responsible for encoding goal location and for route planning. The nucleus accumbens translates paths in neural space into appropriate locomotor activity that moves the animal towards the goal in real space. The complete model assumes that the hippocampal output to nucleus accumbens and prefrontal cortex provides information for generating solutions to spatial problems. In support of this model, we finally present preliminary evidence that the goal representation necessary for path planning might be encoded in the prelimbic/infralimbic region of the medial prefrontal cortex.

Goal-Related Activity in Hippocampal Place Cells

“…Such goal signals would nicely complement information provided by cells in the medial prefrontal cortex, recently shown to provide coarse encoding of goal location and hypothesized to participate in path planning (Poucet et al, 2000(Poucet et al, , 2004Hok et al, 2005). That hippocampal place cells also have a goal signal, albeit quite different in nature, suggests that both structures could participate in a distributed neural network that allows the rat to plan accurate trajectories in space.…”

Coding for spatial goals in the prelimbic/infralimbic area of the rat frontal cortex

“…Because the PL͞IL area of mPFC receives direct projections from the ventral hippocampus (7,8), the merging of goal information with hippocampal information about the rat's current location could bias downstream areas, such as the ventral striatum, toward the selection of the motor output most relevant for reaching the goal. In conclusion, PL͞IL neurons have properties expected of cells encoding spatial goals, a key component necessary for computing optimal paths in the environment (24). Although neurons with similar characteristics might exist in other brain areas, it is interesting to observe that they were found in a structure that has strong connections to the hippocampus and is separately implicated in planning (25).…”

Anterior Hippocampus and Goal-Directed Spatial Decision Making

“…The ventral/anterior hippocampus is closely connected to medial prefrontal areas (Fanselow and Dong, 2010;Royer et al, 2010) where goal-responsive cells have been reported in rodents (Hok et al, 2005(Hok et al, , 2007. Thus, anterior hippocampal and medial prefrontal areas may conspire to support representations of goal proximity (Gaussier et al, 2002;Killcross and Coutureau, 2003;Poucet et al, 2004;Doeller et al, 2008).…”