The Hippocampus as a Cognitive Map

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Subsequently, Brotons-Mas et al. The remaining cells showed some degree of remapping, with some units replicating their locational firing across specific light-to-dark conditions, whereas others were strongly affected by light—dark transitions. Brotons-Mas et al.

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Subiculum units showed strongly heterogeneous spatial coding, with place cells, barrier- or perimeter-related cells, as well as boundary-vector cells Lever et al. Adding to this remarkable heterogeneity of cell types, Olson et al. In these experiments, rats foraged in environments with multiple, interconnected paths, of which many had branch-points enabling movement trajectories in opposite directions.

Olson et al.

The Hippocampus as a Cognitive map - John O'Keefe & Lynn Nadel

Moreover, these firing preferences were preserved during maze rotations, indicating these cells responded to the larger spatial allocentric context, rather than the track itself. These firing preferences were absent during recordings in a trajectory-unconstrained, open-field, circular arena Olson et al.

There have been relatively few studies of the subiculum during brain imaging in humans, partly because it is a difficult structure localize using conventional functional magnetic resonance imaging fMRI techniques. Two recent studies point to roles for the human subiculum in scene discrimination and head direction processing. Hodgetts et al. These data suggest a role for the subiculum in both mnemonic and spatial processing in humans. Meanwhile, a very early study in humans Vitte et al. It will be particularly interesting to analyze the nature extent of subicular and thalamic activation in humans with ultrahigh field fMRI resulting from caloric stimulation of the vestibular system.

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Tentatively, we can conclude that the subiculum appears to code space in a flexible manner, being involved in the processing of allocentric information, external cues, and path integration, thus broadly supporting spatial navigation. It almost certainly has roles in other forms of memory, given its close connectivity to both the hippocampus proper and the anterior thalamic nuclei, although these roles have not yet been fully explored.

An example has been suggested by Deadwyler and Hampson , who found that CA1 and subiculum acted in a complementary fashion to bridge temporal gaps during the performance of a spatial delayed nonmatch-to-sample task. It has been known for some time that the anterodorsal nucleus of the thalamus contains a substantial population of head-direction cells Blair and Sharp, ; Taube, ; Goodridge and Taube, These cells are thought to contribute to path integration Frohardt et al.

Meanwhile, head-direction cells have also been recorded in the anteroventral thalamic nucleus Tsanov et al. Along with the anterodorsal nucleus, the adjacent laterodorsal thalamic nucleus also contains a significant concentration of head-direction cells Mizumori and Williams, Again, like the anterodorsal thalamic nucleus, it is reciprocally linked with the retrosplenial cortex, postsubiculum, and presubiculum van Groen and Wyss, ; Clark and Harvey, Unlike the anterior thalamic nuclei, the laterodorsal nucleus appears to lack inputs from the mammillary bodies, while potentially being more dependent on its visual inputs Mizumori and Williams, ; Clark and Harvey, Lesions of the rat laterodorsal nucleus cause mild deficits in location learning in the water maze van Groen et al.

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Transient laterodorsal lesions can disrupt hippocampal place cells and impair spatial learning Mizumori et al. For these reasons, this nucleus appears to parallel the anterodorsal thalamic nucleus, being distinguished by its greater visual inputs. Returning to the rostral thalamus, much less is known regarding spatial coding in the other anterior thalamic nuclei and other rostral thalamic nuclei, i.

These additional thalamic sites are, however, of particular interest as the subiculum provides dense, direct inputs to the anteromedial and anteroventral nuclei, contrasting with the projections from the postsubiculum and presubiculum to the anterodorsal thalamic nuclei Meibach and Siegel, ; van Groen and Wyss, a , b ; Bubb et al. Of the various midline nuclei, nucleus reuniens stands out because of its inputs from the subiculum and CA1, as well as its dense, direct projections to the hippocampus, especially to CA1 Herkenham, ; Vertes et al.

Based on their respective connectivity, it had previously been predicted that the anterior thalamic nuclei process information with high spatial and temporal resolution Aggleton et al. Our current findings strongly support the first prediction but appear to substantially moderate the second prediction, because they show the widespread presence of a diverse population of spatially-responsive neurons in these midline nuclei.

In nucleus reuniens, for example, there is an unexpected population of cells coding for head direction Jankowski et al. The head-direction cells found in nucleus reuniens are similar in a great many respects to those found in other regions that show head-direction coding: they are not affected by changing visual conditions from light to dark and back to light, or by changing arena shape; they do not remap across days, maintaining a constant orientation.

They are also present from the first exposure to the recording environment. Interestingly, theta-cycle skipping cells are also present in nucleus reuniens, similar to the theta-skipping cells found in entorhinal cortex e. Finally, nucleus reuniens head-direction cells are not place cells: they are not spatially-modulated in the sense of having a place-related signal Jankowski et al. Nucleus reuniens also provides a substantial anatomical output to hippocampal area CA1, offering a means by which it can modulate spatial coding in the hippocampus proper.

For example, combined lesions of the rhomboid nucleus and nucleus reuniens ReRh seemingly spare CA1 place cell spatial characteristics in familiar environments, but affect firing in unfamiliar environments Cholvin et al. In that experiment, after ReRh lesions, spatial coherence decreased for the first exploration session in a novel environment. Recordings conducted over a 5-day period then showed that ReRh lesions result in a marked and enduring decrease in place field stability and lower firing variability Cholvin et al.

These data suggest that inputs from ReRh modulate spatial remapping in the hippocampus; it may be that the head directional signal provides a stabilizing directional signal while exploring unfamiliar environments. Jankowski et al. In the parataenial nucleus The percentages of place cells recorded in nucleus reuniens was 2. The variation in the percentage of place cells present across these nuclei suggests that the spatial code is more or less sparse for the differing nuclei.

More than this, the phenotypic characteristics of the place cells vary in these differing nuclei, with the place fields of cells in nucleus reuniens being the largest and, thereby, carrying the lowest spatial information. Meanwhile, the place fields in the parataenial nucleus occupy the smallest percentage of the recording arena, carrying the highest spatial information.

The anteromedial nucleus occupies an intermediate position. In other words, across these anatomically-closely-related nuclei, there appears to be a spatial information content gradient.

Transformation of the Hippocampal Cognitive Map

In addition to place cells, there is also a population of neurons that respond to the presence of impassable perimeters in the recording arena. These neurons are found in nucleus reuniens and the anteromedial thalamic nucleus Jankowski et al. Temporal evolution analyses suggest that the perimeter cells and place cells in these nuclei appear on the first exposure of the animal to the arena. Finally, as noted above, recordings in the anteromedial nucleus of the thalamus also disclose a population of head-direction cells in a hitherto unsuspected and untheorized-about location.

These head-direction cells are active also from the first exposure of the animal to the arena, suggesting that early pre-processing of spatial information occurs rapidly in subcortical brain structures. Perimeters are an important part of the environment, as they formally shape the geometry of the perceptible environment, as well as constraining behavioral trajectories.

Perimeters can comprise vertical walls, vertical drops, watercourses, etc. Matulewicz et al. Moreover, the firing patterns of these perimeter-responsive units were stable across multiple sleep-wake cycles, and were independent of either light or dark conditions, suggesting that these units are not directly modulated by visual input. These neurons respond to perimeter modifications by remapping their firing when two walls of the four present in a rectangular recording arena are removed from recording session to recording session.

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Further experiments will be required to further explore potential coding differences induced by distal landmarks and proximal tactile cues, under conditions where these information types are explicitly opposed to each other. Overall, recordings within the various rostral thalamic nuclei reveal the presence of spatially-responsive cells.

The origin of their spatial signals is not yet known, leaving us with at least three hypotheses to entertain.

The first is that the hippocampal and rostral thalamic spatial systems operate in parallel in a fashion similar to the accessory optic system ; the second is that one is subordinate to the other, for example, the hippocampal formation provides information necessary for the spatial activity observed in the rostral thalamus, or vice versa ; and third, that there are reciprocal and interdependent relationships between these spatial nodes.

Current findings only provide an incomplete data-set with regard to these three hypotheses. Most of the focus has been on the consequences of anterior thalamic lesions upon hippocampal and parahippocampal activity, stemming from the significance of the anterodorsal nucleus for head-direction signals Taube, Consequently, it is known that anterior thalamic lesions cause an absence of postsubiculum head-direction signals Goodridge and Taube, While postsubiculum lesions change the properties of anterodorsal head-direction cells, these spatial cells are still present Goodridge and Taube, , reflecting an asymmetric relationship.

Likewise, medial entorhinal cortex lesions leave anterior thalamic head direction activity largely unaffected Clark and Taube, Meanwhile, CA1 place cells appear largely unaffected after anterior thalamic lesions Calton et al. Consequently, with the exception of the head-direction network, little is known about the interdependencies of the various spatial cell types found in the hippocampal formation and anterior thalamus. The claustrum is an underexplored and enigmatic paracortical structure. The claustrum of the rat is a bilateral subcortical sheet of gray matter, spanning approximately the rostral half of the telencephalon, almost to the frontal poles, and caudally to the motor strip.

It is bordered by the orbitofrontal cortex, rostrally, both caudally and medially by the caudoputamen, and by the insular cortex laterally Buchanan and Johnson, ; Dillingham et al. Anatomically, the claustrum receives projections from the entire cortical mantle. These projections are organized in a topographic fashion, with association cortex projecting to the anterior claustrum and sensory cortices projecting to the posterior portion of the claustrum. In addition, there are also claustrum connections to and from the hippocampal formation, retrosplenial cortex, entorhinal cortex, and a wide variety of subcortical structures, although the existence of projections from the anterior thalamus to the claustrum continues to be a matter of debate Dillingham et al.

Comprehensive lesion investigations of the claustrum have yet to be undertaken for technical reasons: the claustrum is a difficult target for the injection-targeting used in lesion analyses, although chemogenetic approaches such as DREADDs may prove more tractable. There have been many hypotheses regarding the functions of the claustrum over the years, most notably that it orchestrates consciousness in the mammalian brain Crick and Koch, There have been intermittent anatomical explorations of the claustrum that conclude it does not comprise striatal tissue, but rather can be thought best of as a paracortical tissue.

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Functional investigations of the claustrum are relatively few in number; we briefly survey some relevant studies here. There have been very few lesion studies of the claustrum.

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Aclaustral humans are rarely reported: one study of a patient with striking, transient, but symmetric, bilateral, claustral lesions arising from mumps encephalitis Ishii et al. With the infection resolved, subsequent imaging showed no persisting lesions of the bilateral claustrum.

Design Principles of the Hippocampal Cognitive Map

Intriguingly, Cascella et al. The possible relationship between the claustrum and consciousness continues to receive interest. In an early report, Gabor and Peele found that electrical stimulation of the claustrum in the awake behaving cat resulted in a state of behavioral relaxation and subsequent induction of sleep.

Koubeissi et al. The patient had previously undergone a left hippocampal resection for epilepsy; she was seizure-free for 4 years, after which her seizures returned.

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Depth electrodes were implanted for seizure sampling. The patient returned to baseline as soon as the stimulation stopped with no recollection of the events during the stimulation period. Perhaps minor differences in electrode placement in the claustrum result in major differences for awareness, or perhaps there is an idiopathic and perhaps unique neurological circumstance in the earlier report. Or it might be the case that the claustrum plays a role in orchestrating some of the cortical changes occurring during the wake-sleep transition Renouard et al.

Olson and Graybiel suggested that there is a somatosensory map of the complete surface of the body, arranged longitudinally in the claustrum in the anesthetized cat preparation. Remedios et al.