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Object exploration and reactions to spatial and nonspatial changes in hooded rats following damage to parietal cortex or hippocampal formation.

Hooded rats with bilateral lesions of the anterior part of the hippocampal formation (HIP), anterior region of the posterior parietal cortex (APC), or posterior region of the posterior parietal cortex (PPC) were compared with controls for their exploration of 5 objects in an open field, habituation of locomotion and object investigation, and response to spatial and nonspatial change. First, all groups displayed habituation of both locomotor and exploratory activity. Second, controls selectively reexplored displaced objects, and APC-lesioned rats reexplored all objects, whereas PPC- and HIP-lesioned rats failed to react to the spatial change. Third, a novel object induced reexploration in all groups. The results are consistent with the roles of the HIP and PPC in spatial information processing. Moreover, the APC and PPC are involved in attentional effortful processing and visuospatial information processing necessary for spatial representation, respectively.

Contribution of Multiple Sensory Information to Place Field Stability in Hippocampal Place Cells

Hippocampal place cells in rats display spatially selective firing in relation to both external and internal cues. In the present study, we assessed the effects of removing visual and/or olfactory cues on place field stability. Place cell activity was recorded as rats searched for randomly scattered food in a cylinder. During an initial recording session, the lights were on and the only available cue was a single white cue card. Following this session, three sessions were run in a row with the cue card removed. In addition, the lights were either turned off or left on and the floor was either cleaned or left unchanged, thus creating four conditions: dark/cleaning, dark/no cleaning, light/cleaning, and light/no cleaning. A fifth session was run with the cue card back on the cylinder wall and the lights turned on. The rat remained in the cylinder during all sessions without being removed at any time. In the dark/cleaning and light/cleaning conditions, most place fields were not stable (i.e., abruptly shifted position). In addition, half of the cells stopped firing in the dark/cleaning condition. In contrast, in the dark/no cleaning and light/no cleaning conditions, most place fields remained stable across sessions. These results suggest that 1) rats are not able to rely on only movement‐related information to maintain a stable place representation, 2) visual input is necessary for the firing of a large number of cells, and 3) olfactory information can be used to compensate for the lack of visuospatial information. Hippocampus 2000;10:64–76.

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.

The differences shown by C57BL/6 and DBA/2 inbred mice in detecting spatial novelty are subserved by a different hippocampal and parietal cortex interplay

Inbred C57BL/6 (C57) and DBA/2 (DBA) mice with hippocampus, posterior parietal cortex or sham lesions were placed in an open-field containing five objects and their reactivity to the displacement (spatial novelty) or the substitution (object novelty) of some of these objects was examined. C57 mice reacted to spatial novelty by exploring more the displaced than the non-displaced objects while DBA mice did not show any consistent reaction. In the highly reactive C57 strain, the peak of exploratory responses directed towards the displaced objects was completely abolished by hippocampal and posterior parietal cortex lesions. In the non-reactive DBA strain, hippocampal lesions induced an aspecific decreased interest towards the two categories of objects while posterior parietal cortex lesions did not produce any behavioral modification. The high reactivity of C57 mice to spatial change appears to be subserved by the conjunctive participation of the hippocampus and the posterior parietal cortex. Conversely, the deficit shown by DBA mice in that situation seems to be related to: (i) a poorly functional hippocampus; and (ii) the non-involvement of the posterior parietal cortes. The present data suggest that the participation of the posterior parietal cortes to the detection of spatial novelty may depend on the degree of functionality of the hippocampus.

Distinct Roles of Medial and Lateral Entorhinal Cortex in Spatial Cognition

It is known that the entorhinal cortex plays a crucial role in spatial cognition in rodents. Neuroanatomical and electrophysiological data suggest that there is a functional distinction between 2 subregions within the entorhinal cortex, the medial entorhinal cortex (MEC), and the lateral entorhinal cortex (LEC). Rats with MEC or LEC lesions were trained in 2 navigation tasks requiring allothetic (water maze task) or idiothetic (path integration) information processing and 2-object exploration tasks allowing testing of spatial and nonspatial processing of intramaze objects. MEC lesions mildly affected place navigation in the water maze and produced a path integration deficit. They also altered the processing of spatial information in both exploration tasks while sparing the processing of nonspatial information. LEC lesions did not affect navigation abilities in both the water maze and the path integration tasks. They altered spatial and nonspatial processing in the object exploration task but not in the one-trial recognition task. Overall, these results indicate that the MEC is important for spatial processing and path integration. The LEC has some influence on both spatial and nonspatial processes, suggesting that the 2 kinds of information interact at the level of the EC.

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.

Hippocampal-parietal cortical interactions in spatial cognition.

Growing evidence suggests that the associative parietal cortex (APC) of the rat is involved in the processing of spatial information. This observation raises the issue of the respective functions of the APC and the hippocampus in spatial processing as well as of their possible interactions. In this paper, we review neuroanatomical, electrophysiological, and behavioral data that support the existence of such functional interactions. Our hypothesis is that the APC is involved in the initial combination of visuospatial information and self‐motion information necessary for the integration of egocentrically acquired information into allocentrically coded information, the latter step being completed in the hippocampus. The dialogue between the hippocampus and the APC is therefore crucial, particularly when the elaboration and/or updating of an allocentric representation depends on complex combinations of visuospatial and self‐motion information. Hippocampus 10:491–499, 2000

Effects of lesions of the associative parietal cortex on the acquisition and use of spatial memory in egocentric and allocentric navigation tasks in the rat.

It has been hypothesized that the rat associative parietal cortex (APC) is involved in the association between visuospatial and locomotion-generated (kinesthetic) information. To study the kinesthetic component, APC-lesioned and control rats were trained in total darkness to reach a submerged platform in the Morris water maze. In the egocentric task, the relative position of the starting point and the platform was constant all over training. Parietal rats have been found impaired in acquisition and to a less extent in retention of this task. In the allocentric task, rats were then trained in the standard version of the navigation task. A mild deficit was observed in acquisition of this task because the APC-lesioned rats displayed longer escape latencies but control-like search patterns. These results suggest that the APC is involved in the coding of kinesthetic information that plays an important role in place navigation.

Cerebellum Shapes Hippocampal Spatial Code

Cerebellar protein kinase C–dependent mechanisms process self-motion information needed for spatial representation and accurate navigation. Spatial representation is an active process that requires complex multimodal integration from a large interacting network of cortical and subcortical structures. We sought to determine the role of cerebellar protein kinase C (PKC)–dependent plasticity in spatial navigation by recording the activity of hippocampal place cells in transgenic L7PKCI mice with selective disruption of PKC-dependent plasticity at parallel fiber–Purkinje cell synapses. Place cell properties were exclusively impaired when L7PKCI mice had to rely on self-motion cues. The behavioral consequence of such a deficit is evidenced here by selectively impaired navigation capabilities during a path integration task. Together, these results suggest that cerebellar PKC-dependent mechanisms are involved in processing self-motion signals essential to the shaping of hippocampal spatial representation.

Unstable CA1 place cell representation in rats with entorhinal cortex lesions

Recent studies emphasize the importance of the entorhinal cortex in spatial representation and navigation. Furthermore, evidence is accumulating to show that spatial processing depends on interactions between the entorhinal cortex and the hippocampus. To investigate these interactions, we examined the effects of entorhinal cortex lesions on the activity of hippocampal CA1 place cells. Rats received bilateral radiofrequency lesions of the entorhinal cortex or sham lesions before place cell recording. Place cells were recorded as the rats performed a pellet‐chasing task in a cylinder containing three cue‐objects. Entorhinal cortex lesions did not abolish place cell spatial firing but reduced noticeably discharge rate and field size. Most importantly, the lesions affected firing field stability when cells were recorded both in constant conditions and following cue manipulations (object rotation, object removal). These findings indicate that the entorhinal cortex is necessary for the stability of hippocampal representations across exposures to a familiar environment. Consistent with the recent discovery of grid cells in the medial entorhinal cortex, our results suggest that the entorhinal cortex contributes to providing a spatial framework that would enable the hippocampus to maintain stable environment‐specific representations.