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WIREs Cogn Sci
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Parallel and convergent processing in grid cell, head‐direction cell, boundary cell, and place cell networks

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The brain is able to construct internal representations that correspond to external spatial coordinates. Such brain maps of the external spatial topography may support a number of cognitive functions, including navigation and memory. The neuronal building block of brain maps are place cells, which are found throughout the hippocampus of rodents and, in a lower proportion, primates. Place cells typically fire in one or few restricted areas of space, and each area where a cell fires can range, along the dorsoventral axis of the hippocampus, from 30 cm to at least several meters. The sensory processing streams that give rise to hippocampal place cells are not fully understood, but substantial progress has been made in characterizing the entorhinal cortex, which is the gateway between neocortical areas and the hippocampus. Entorhinal neurons have diverse spatial firing characteristics, and the different entorhinal cell types converge in the hippocampus to give rise to a single, spatially modulated cell type—the place cell. We therefore suggest that parallel information processing in different classes of cells—as is typically observed at lower levels of sensory processing—continues up into higher level association cortices, including those that provide the inputs to hippocampus. WIREs Cogn Sci 2014, 5:207–219. doi: 10.1002/wcs.1272 This article is categorized under: Neuroscience > Physiology
Examples of cell types with spatial tuning in the hippocampus and in parahippocampal cortices. The left column displays data from each cell type during exploration of an open field arena. Within this column, the spatial selectivity of each cell type is shown by plotting the location of each spike (in red) onto the trajectory of the animal (in black). The central panels are color‐coded firing rate maps of the same arena with high firing rates in red and low firing rates in blue. Finally, the right panels are polar plots showing firing rate as a function of the head direction of the animal during exploration in the environment. The right columns indicate in which regions each spatially tuned cell type is found. Grid cells fire in multiple spatial locations that form a triangular ‘grid’ of the environment. Grid cells are found in the presubiculum, parasubiculum, and all layers of the medial entorhinal cortex. Head‐direction cells fire throughout the environment but only when the animal is facing a specific direction. Head‐direction cells are found in the presubiculum, parasubiculum, and layers III, V, and VI of the medial entorhinal cortex. Conjunctive cells fire in a triangular grid pattern only when the animal is facing a specific direction. Similar to head‐direction cells, conjunctive cells are found in the presubiculum, parasubiculum and layers III, V, and VI of the medial entorhinal cortex. Boundary/border cells fire when the animal is located at a specific distance from a wall in the environment. These cells are found in the subiculum (not shown), presubiculum, parasubiculum, and all layers of the medial entorhinal cortex. Place cells generally fire in a single or few locations within the environment, independent of the animal's head direction in the open field. These cells are found in the dentate gyrus, CA3, and CA1 of the hippocampus.
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Main connections between rodent higher association cortices. The parahippocampal region includes the perirhinal and postrhinal cortices, the medial and lateral areas of the entorhinal cortex, the pre‐ and parasubiculum, and the hippocampal formation includes dentate gyrus, CA3, CA1, subiculum. Extrinsic connections with other areas in the neocortex and thalamus are also represented. The arrows indicate strong to moderate connections between regions based on anatomical studies using retrograde and anterograde tracers (see Refs ). In the hippocampal system, regions highlighted in red contain large proportions of spatially modulated cells such as place cells in the hippocampus and grid cells, head‐direction cells, and boundary cells in parahippocampal regions. In the postrhinal cortex, cells with a broad spatial selectivity were described. The neocortical regions are defined as in Ref . Neocortical regions project to parahippocampal cortices, in particular to the postrhinal and perirhinal cortices in a relatively segregated way: cingulate, parietal, occipital, and temporal regions provide input to the postrhinal cortex while temporal, frontal, insular, and piriform regions project to the perirhinal cortex. Both postrhinal and perirhinal cortices give rise to strong backprojections to their neocortical afferent regions. Classically, efferent connections from the postrhinal and perirhinal cortices were described to target the medial and lateral subdivisions of the entorhinal cortex, respectively. However, the postrhinal cortex also projects to the lateral entorhinal cortex (LEC), but to a lesser extent than to the medial entorhinal cortex (MEC), and the perirhinal cortex targets both LEC and MEC in a similar way. Connections are also found between postrhinal and perirhinal cortex as well as between MEC and LEC. In addition, the postrhinal cortex and MEC are strongly interconnected with the pre‐ and parasubiculum, which receive projections mainly from the thalamus. Projections from MEC and LEC provide the main cortical input to the hippocampus. These projections, which form the perforant path, arise from the superficial layers of the entorhinal cortex (layer II and III) and are topologically organized. Layer II projects to the dentate gyrus and CA3 while layer III projects to CA1. In the dentate gyrus and CA3, projections from MEC and LEC converge to the same neurons. However, in CA1 and the subiculum, there is a clear segregation of medial and lateral inputs in the transverse axis: MEC projects predominantly to proximal CA1, which connects to the distal subiculum, and LEC projects predominantly to distal CA1, which connects to the proximal subiculum (proximal and distal indicate relative proximity to CA3). MEC and LEC also project directly to their respective target regions in the subiculum (not depicted). CA1 and subiculum reciprocate the connections with MEC and LEC and target the deep layers (V and VI). The subiculum receives the main output of the hippocampal system and projects to the thalamus and the neocortex. In addition, projections from the entorhinal cortex to the hippocampus are organized along its longitudinal axis such that the dorsal band of the entorhinal cortex projects to dorsal part of the hippocampus (blue) and the ventral band of the entorhinal targets ventral regions of the hippocampus (green). At every level of the hippocampal system, there are strong backprojections to the afferent regions. Even in the hippocampus, the unidirectional polysynaptic circuit (dentate gyrus to CA3 to CA1) has been reconsidered based on evidence of projections from CA3 to the dentate and from CA1 to CA3 (not depicted). Roman numerals refer to cortical layers.
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Feedforward and parallel models of place cell firing. (a) Feedforward models. Top to bottom: Models of place cells have shown how place cell firing fields could arise from the feedforward influence of grid cells with different spatial scales and spatial phases. Models of grid cells have shown how grid cell firing fields could arise from integrating head‐direction inputs in combination with either oscillatory interference or attractor dynamics within entorhinal cortex. Models have shown how head‐direction cells could arise from input from angular velocity cells. (b) Possible parallel networks contributing to spatial processing. In addition to the feedforward circuit shown in (a), parallel systems through the entorhinal cortex are shown. For example, place cells in the hippocampus may arise from the inputs of boundary cells in the medial entorhinal cortex, as proposed by the model of boundary vector cells. These boundary vector cells may arise from visual features coding the distance and angle to boundaries in the environment. On the right, odor and object responses found in the hippocampus may arise from representations of odors and objects coded in the lateral entorhinal cortex. In addition to feedforward influences, feedback connections from the hippocampus to the entorhinal cortex may play an important role in updating and aligning the representations of locations by grid cells and boundary vector cells, as well as in updating the context of odor and object responses.
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