Pierre-Pascal Lenck-Santini

Goal-Related Activity in Hippocampal Place Cells

Place cells are hippocampal neurons whose discharge is strongly related to a rats location in its environment. The existence of place cells has led to the proposal that they are part of an integrated neural system dedicated to spatial navigation, an idea supported by the discovery of strong relationships between place cell activity and spatial problem solving. To further understand such relationships, we examined the discharge of place cells recorded while rats solved a place navigation task. We report that, in addition to having widely distributed firing fields, place cells also discharge selectively while the hungry rat waits in an unmarked goal location to release a food pellet. Such firing is not duplicated in other locations outside the main firing field even when the rats behavior is constrained to be extremely similar to the behavior at the goal. We therefore propose that place cells provide both a geometric representation of the current environment and a reflection of the rats expectancy that it is located correctly at the goal. This on-line feedback about a critical aspect of navigational performance is proposed to be signaled by the synchronous activity of the large fraction of place cells active at the goal. In combination with other (prefrontal) cells that provide coarse encoding of goal location, hippocampal place cells may therefore participate in a neural network allowing the rat to plan accurate trajectories in space.

Spatial navigation and hippocampal place cell firing: the problem of goal encoding.

Place cells are hippocampal neurons whose discharge is strongly related to a rats 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.

Sensory and memory properties of hippocampal place cells.

The rat hippocampus contains place cells whose firing is location-specific. These cells fire only when the rat enters a restricted region of the environment called the firing field. In this review, we examine the sensory information that is fundamental to the place cell system for producing spatial firing. While visual information takes precedence in the control of firing fields when it is available, local (olfactory and/or tactile) cues combined with motion-related cues can permit stable spatial firing. Motion-related cues are integrated by hippocampal place cells, but in the absence of external cues do not support stable firing over long periods. While firing fields are based on a variety of sensory cues, they do not strictly depend on such cues. Rather, sensory information is important for activating the representation appropriate to the current environment as reflected by the firing properties of place cell ensembles. Specific sensory channels as well as the memory properties of place cells can support ongoing firing under manipulations of the environment. These memory features raise the question of the role of the place cell system in the acquisition, storage and retrieval of spatial information. Based on the existing literature about the effects of hippocampal lesions and about the metabolic activations in spatial memory tasks, we suggest that a function of the place cell system is to automatically provide the organism with information about its current location so as to allow for the rapid acquisition of novel information.

Place-cell firing does not depend on the direction of turn in a Y-maze alternation task.

Hippocampal place cells were recorded while rats solved a continuous spatial alternation task requiring short‐term spatial memory. All cells that had a firing field on the stem of the Y‐shaped maze were found to have a very similar pattern of discharge whether the rat was about to make a right or a left turn, and whether the preceding turn was a right or a left turn. Thus, the view that place cells encode a variety of events (including the direction of turns) useful for solving memory tasks is not well supported by the present data. We suggest several possible explanations to account for the discrepancy with other recent studies showing turn‐related modulation of place‐cell activity.

Place cells, neocortex and spatial navigation: a short review

Hippocampal place cells are characterized by location-specific firing, that is each cell fires in a restricted region of the environment explored by the rat. In this review, we briefly examine the sensory information used by place cells to anchor their firing fields in space and show that, among the various sensory cues that can influence place cell activity, visual and motion-related cues are the most relevant. We then explore the contribution of several cortical areas to the generation of the place cell signal with an emphasis on the role of the visual cortex and parietal cortex. Finally, we address the functional significance of place cell activity and demonstrate the existence of a clear relationship between place cell positional activity and spatial navigation performance. We conclude that place cells, together with head direction cells, provide information useful for spatially guided movements, and thus provide a unique model of how spatial information is encoded in the brain.

Properties of place cell firing after damage to the visual cortex.

Hippocampal place cells were recorded while rats with lesions of the striate visual cortex foraged for food pellets in a cylindrical arena. Compared to control rats, rats with striate damage had place cells whose firing was less well organized in space, according to a measurement of spatial coherence. More importantly, the spatial location of firing fields in rats with striate lesions was poorly controlled by three‐dimensional objects, unlike the fields of either normal sighted rats or early blind rats. These findings suggest a possible contribution of the striate visual cortex to the selection of cues used for anchoring place cell firing fields in space.