Beta Oscillations and Hippocampal Place Cell Learning during Exploration of Novel Environments

Berke et al. (2008) reported that beta oscillations occur during the learning of hippocampal place cell receptive fields in novel environments. Place cell selectivity can develop within seconds to minutes, and can remain stable for months. Paradoxically, beta power was very low during the first lap of exploration, grew to full strength as a mouse traversed a lap for the second and third times, and became and remained low again after the first two minutes of exploration. Beta oscillation power also correlated with the rate at which place cells became spatially selective, and not with theta oscillations. We explain such beta oscillations as a consequence of how place cell receptive fields may be learned as spatially selective categories due to feedback interactions between entorhinal cortex and hippocampus. Top-down attentive feedback helps to ensure rapid learning and stable memory of place cells. Beta oscillations are generated when top-down feedback mismatches bottom-up data as place cell receptive fields are refined. Beta oscillations do not occur on the first trial because adaptive weights in feedback pathways are all sufficiently large then to match any input pattern. On subsequent trials, adaptive weights become pruned as they learn to match the sharpening receptive fields of the place cell categories, thereby causing mismatches until place cell receptive fields stabilize.National Science Foundation (SBE-0354378

Linear Self-Motion Cues Support the Spatial Distribution and Stability of Hippocampal Place Cells

The vestibular system provides a crucial component of place-cell and head-direction cell activity [1-7]. Otolith signals are necessary for head-direction signal stability and associated behavior [8, 9], and the head-direction signal's contribution to parahippocampal spatial representations [10-14] suggests that place cells may also require otolithic information. Here, we demonstrate that self-movement information from the otolith organs is necessary for the development of stable place fields within and across sessions. Place cells in otoconia-deficient tilted mice showed reduced spatial coherence and formed place fields that were located closer to environmental boundaries, relative to those of control mice. These differences reveal an important otolithic contribution to place-cell functioning and provide insight into the cognitive deficits associated with otolith dysfunction

Parallel and convergent processing in grid cell, head-direction cell, boundary cell, and place cell networks.

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 Conflict of interest: The authors have declared no conflicts of interest for this article. For further resources related to this article, please visit the WIREs website

Coordinated grid and place cell replay during rest

Hippocampal replay has been hypothesized to underlie memory consolidation and navigational planning, yet the involvement of grid cells in replay is unknown. During replay we found grid cells to be spatially coherent with place cells, encoding locations 11 ms delayed relative to the hippocampus, with directionally modulated grid cells and forward replay exhibiting the greatest coherence with the CA1 area of the hippocampus. This suggests grid cells are engaged during the consolidation of spatial memories to the neocortex