Role of the parietal cortex in long-term representation of spatial information in the rat

https://doi.org/10.1016/j.nlm.2008.08.005Get rights and content

Abstract

The processing of spatial information in the brain requires a network of structures within which the hippocampus plays a prominent role by elaborating an allocentric representation of space. The parietal cortex has long been suggested to have a complementary function. An overview of lesion and unit recording data in the rat indicates that the parietal cortex is involved in different aspects of spatial information processing including allocentric and egocentric processing. More specifically, the data suggest that the parietal cortex plays a fundamental role in combining visual and motion information, a process that would be important for an egocentric-to-allocentric transformation process. Furthermore, the parietal cortex may also have a role in the long-term storage of representation although this possibility needs further evidence. The data overall show that the parietal cortex occupies a unique position in the brain at the interface of perception and representation.

Introduction

Spatial behaviors are essential to survival of most animal species. Evolution yielded the emergence of spatial strategies that allow animals to maintain their navigational capability and their spatial memory in spite of environmental modifications. Understanding how the brain processes spatial information has motivated a huge amount of work. It is now well established that the processing of spatial information in the brain requires a network of cortical and subcortical structures within which the hippocampus plays a central role by implementing an allocentric representation of space. One of the most striking evidence in favor of such a role comes from the existence in CA1 and CA3 of pyramidal neurons characterized by location-specific firing, the so-called place cells (O’Keefe and Dostrovsky, 1971, O’Keefe and Nadel, 1978). The discovery of place cells in the 1970s has had a great conceptual influence and contributed to promote a “hippocampus-centered” view of the processing of spatial information in the brain. However, that a phylogenetically preserved, paleocortical structure such as the hippocampus could be the neural substrate of high level cognitive processes implicitly raised the question of the role of the neocortex in rodents. In this respect, the influence of Lashley’s theories was still perceptible in the 1970s (McDaniel et al., 1979, Thomas, 1970, Thomas and Weir, 1975). As the main proponent of a holistic view of cortical functions in learning twenty years before, Lashley had postulated that cortical areas do not have specific functions as far as learning is concerned and can substitute for each other when a lesion is made (equipotentiality principle). Several decades later, this theory motivated studies that examined the effects of lesioning various parts of the cortex on learning performance. Lesions of the posterior association cortex, frontal cortex and temporal cortex produced different effects on various learning tasks thus questioning Lashley’s equipotentiality principle and perhaps more importantly, suggesting a specific contribution of the posterior association cortex (McDaniel and Thomas, 1978, Thomas, 1970, Thomas and Weir, 1975). In the context of a strong disagreement in the literature regarding the existence of a posterior association cortex in the rat, these seminal studies are among the first to propose that this region has a distinct role in spatial learning and memory. This renewal of interest for the parietal cortex in the rat produced a large number of studies that sought to characterize this cortical area both neuroanatomically and functionally. The results provide a great deal of evidence in favor of a role in the formation of long-term spatial representations. This aim of this review is to summarize this evidence and to suggest possible directions for further work.

Section snippets

The parietal cortex is involved in multimodal processing: Anatomical evidence

The hypothesis of the existence of a posterior association cortex (hereafter referred to as parietal cortex) in the rat has been initially founded on neuroanatomical bases. Using cytoarchitectonic characteristics, Krieg described a parietal region subdivided into six areas (Krieg, 1946), three primary somatosensory areas (labeled 1, 2, 3 according to Brodmann’s nomenclature) and three areas putatively involved in multisensory integration (labeled 7, 39, 40). Subsequently, Krieg’s area 7 was

Effects of parietal cortex lesions in the processing of allocentric information

Parietal cortex lesion studies were performed not only to uncover the role of this structure in spatial learning but also to discriminate it from that of the hippocampus. The possibility that the cognitive map or at least an elementary form was elaborated in the parietal cortex before being fully realized in the hippocampus was raised. To investigate the contribution of the parietal cortex in long-term representation of spatial information, a number of studies examined the effects of parietal

Effects of parietal cortex lesions in the processing of egocentric information

As in allocentric tasks, parietal cortex lesions produced variable effects in egocentric tasks. Once again, the diversity of the tasks used may account for such inconsistency. Actually, egocentric tasks include a heterogenous amount of behavioral situations ranging from visually guided navigation in the water maze to path integration in an arena. Thus, these tasks involve different sensory inputs and processes that may be mediated by different brain structures. It not surprising therefore that

Acquisition vs. retention: A role in memory storage?

There is a large consensus that a dialog between the neocortex and the hippocampus is essential for the formation of long-term memory (McClelland, McNaughton, & O’Reilly, 1995). The hippocampus would be necessary for rapid acquisition of new information and short term storage whereas the neocortex would be involved in the storage of remote memories (Frankland & Bontempi, 2005). The parietal cortex has been hypothesized to be activated during consolidation (Maviel, Durkin, Menzaghi, & Bontempi,

Neural activity in the parietal cortex: Unit recordings

Only a very few studies have managed to record unit activity in the parietal cortex in the rat. McNaughton and collaborators recorded parietal neurons as the rats performed a radial maze task. They found that a substantial number of cells exhibited movement correlates, discriminating between right turns, left turns and forward motion. Interestingly, there were cells that appeared to be modulated by a combination of motion and spatial correlates. For examples, some cells were preferentially

The role of the parietal cortex in the formation of spatial representation

Overall, lesion and electrophysiological studies provide a complex pattern of results that may reflect the multiple facets of parietal cortex functioning. It may also reflect neuroanatomical heterogeneity of this area. Note that little is known about the organization of inputs and outputs within the cortex parietal. It is likely that there is a subregional specificity. For example, a subregion may be preferentially involved in the processing of sensory information (e.g. visual) and another

The parietal cortex as an element of the cortical-hippocampal interaction

Understanding the role of the parietal cortex in spatial information processing requires taking into account its interactions with other cortical and subcortical regions. The data demonstrate that the parietal is functionally related to the hippocampus, thus supporting the idea that the parietal cortex is part of a functional network that allows continuous dialog between the neocortex and the hippocampus. The data also indicate that the parietal cortex and the hippocampus have distinct roles in

References (75)

  • W.F. McDaniel et al.

    Thalamocortical projections of the temporal and parietal association cortices in the rat

    Neuroscience Letters

    (1978)
  • W.F. McDaniel et al.

    Unilateral injury of posterior parietal cortex and spatial learning in hooded rats

    Behavioural Brain Research

    (1995)
  • C.L. Nelson et al.

    Prefrontal cortical modulation of acetylcholine release in posterior parietal cortex

    Neuroscience

    (2005)
  • D.A. Nitz

    Tracking route progression in the posterior parietal cortex

    Neuron

    (2006)
  • J. O’Keefe et al.

    The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely moving rat

    Brain Research

    (1971)
  • C. Parron et al.

    Reevaluation of the spatial memory deficits induced by hippocampal inactivation reveals the need for cortical co-operation

    Behavioural Brain Research

    (2001)
  • C. Parron et al.

    Entorhinal cortex lesions impairs the use of distal but not proximal landmarks during navigation in the rat

    Behavioural Brain Research

    (2004)
  • C. Parron et al.

    Cooperation between the hippocampus and the entorhinal cortex in spatial memory: A disconnection study

    Behavioural Brain Research

    (2006)
  • J.L. Rogers et al.

    Hippocampal-parietal cortex interactions: Evidence from a disconnection study in the rat

    Behavioural Brain Research

    (2007)
  • E. Save et al.

    Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation

    Behavioural Brain Research

    (2000)
  • P.F. Smith et al.

    The effects of vestibular lesions on hippocampal function in rats

    Progress in Neurobiology

    (2005)
  • J.S. Taube

    Head direction cells and the neurophysiological basis for a sense of direction

    Progress in Neurobiology

    (1998)
  • B. Bontempi et al.

    Time-dependent reorganization of brain circuitry underlying long-term memory storage

    Nature

    (1999)
  • N. Burgess et al.

    Integrating hippocampal and spatial functions: A spatial point of view

  • R.D. Burwell et al.

    Cortical afferents of the perirhinal, postrhinal, and entorhinal cortices of the rat

    Journal of Comparative Neurology

    (1998)
  • R. Cabeza et al.

    The parietal cortex and episodic memory: An attentional circuit

    Nature Reviews Neuroscience

    (2008)
  • L.L. Chen et al.

    Head-direction cells in the rat posterior cortex. II. Contribution of visual and idiothetic information to the directional firing

    Experimental Brain Research

    (1994)
  • L.L. Chen et al.

    Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation

    Experimental Brain Research

    (1994)
  • L.L. Chen et al.

    Head-centered representation and spatial memory in rat posterior parietal cortex

    Psychobiology

    (1998)
  • Y.H. Cho et al.

    Involvement of entorhinal cortex or parietal cortex in long-term spatial discrimination memory in rats: Retrograde amnesia

    Behavioral Neuroscience

    (1996)
  • Y.H. Cho et al.

    Retrograde and anterograde amnesia for spatial discrimination in rats: Role of hippocampus, entorhinal cortex and parietal cortex

    Psychobiology

    (1995)
  • J. Cho et al.

    Head direction, place, and movement correlates for cells in the rat retrosplenial cortex

    Behavioral Neuroscience

    (2001)
  • W.E. DeCoteau et al.

    Effects of hippocampal and parietal cortex lesions on the processing of multiple-object scenes

    Behavioral Neuroscience

    (1998)
  • B.V. DiMattia et al.

    Spatial cognitive maps: Differential role of posterior parietal cortex and hippocampal formation

    Behavioral Neuroscience

    (1988)
  • P.W. Frankland et al.

    The organization of recent and remote memories

    Nature Reviews Neuroscience

    (2005)
  • N.J. Goodrich-Hunsaker et al.

    Human topological task adapted for rats: Spatial information processes of the parietal cortex

    Neurobiology of Learning and Memory

    (2008)
  • N.J. Goodrich-Hunsaker et al.

    Dissociating the role of the parietal cortex and dorsal hippocampus for spatial information processing

    Behavioral Neuroscience

    (2005)
  • Cited by (61)

    • Structural Differences in Hippocampal and Entorhinal Gray Matter Volume Support Individual Differences in First Person Navigational Ability

      2018, Neuroscience
      Citation Excerpt :

      The posterior thalamus has projections to the superficial layers of the posterior parietal cortex (Avendaño et al., 1990). Animal models demonstrate that the posterior parietal cortex supports representations of space for movements within an egocentric coordinate frame (Sato et al., 2006; Save and Poucet, 2009; Whitlock et al., 2012). Human neuroimaging data from Spiers and Maguire (2006) demonstrated that the posterior parietal cortex was recruited during active navigation to a goal, suggesting a role in the coding and monitoring of response-based spatial information concerning distant locations.

    • Applications of the Morris water maze in translational traumatic brain injury research

      2018, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      Although both are involved in processing complex spatial information, there are many conflicting perspectives on the relative roles of the parietal cortex and hippocampus in spatial information encoding during tasks such as the MWM, and full discussion goes beyond the scope of this review (but see (Kesner, 2009; Rogers and Kesner, 2006; Save and Poucet, 2009)). Nevertheless, it is agreed that cognitive mapping in spatial tasks such as MWM involve complex interactions between the hippocampus and cortex (among other regions), with the cortex likely making associations between motion and visual information during the early steps of spatial map formation (Save and Poucet, 2009) and continuing to play a critical role in path integration during navigation (Save and Poucet, 2009; Whitlock et al., 2008), and long-term memory representation (Kesner, 2009). The MWM has been a valuable tool in the study of cognitive deficits after TBI in rodents, and provides an excellent experimental context for the evaluation of potential therapeutic agents.

    View all citing articles on Scopus
    View full text