Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Grid Cells dissociated from Head Turning



Science 29 April 2011:  Vol. 332 no. 6029 pp. 595-599
Reduction of Theta Rhythm Dissociates Grid Cell Spatial Periodicity from Directional Tuning

Mark P. Brandon, Andrew R. Bogaard, Christopher P. Libby, Michael A. Connerney, Kishan Gupta, and Michael E. Hasselmo

Center for Memory and Brain, Department of Psychology, Graduate Program for Neuroscience, Boston University, 2 Cummington Street, Boston, MA 02215, USA.


Grid cells recorded in the medial entorhinal cortex of freely moving rats exhibit firing at regular spatial locations and temporal modulation with theta rhythm oscillations (4 to 11 hertz). We analyzed grid cell spatial coding during reduction of network theta rhythm oscillations caused by medial septum (MS) inactivation with muscimol. During MS inactivation, grid cells lost their spatial periodicity, whereas head-direction cells maintained their selectivity. Conjunctive grid–by–head-direction cells lost grid cell spatial periodicity but retained head-direction specificity. All cells showed reduced rhythmicity in autocorrelations and cross-correlations. This supports the hypothesis that spatial coding by grid cells requires theta oscillations, and dissociates the mechanisms underlying the generation of entorhinal grid cell periodicity and head-direction selectivity.

The role of oscillations in neural coding is controversial. Theta frequency oscillations (4 to 11 Hz) play an important role in memory behavior and code spatial location by the precession of spike timing relative to theta oscillations (theta phase precession) in the hippocampus and medial entorhinal cortex (MEC). However, disagreement remains about whether theta oscillations are critical to spatial coding by neurons. Grid cells in the MEC provide a powerful example for testing the theoretical role of oscillations in neural coding. Some computational models of grid cells use network theta rhythm oscillations to generate grid cell spatial periodicity. These models simulate the phase of spike timing in grid cells and have successfully predicted that the spatial scale of grid cell firing correlates with measures of intrinsic rhythmicity. Recent models also show the potential role of theta oscillations for updating position in attractor dynamic models of grid cells. In rats, we tested the role of theta rhythm oscillations in the spatial coding of grid cells by testing the spatial periodicity of grid cells during pharmacological disruption of theta rhythm oscillations.

The combined data suggest that grid cell spatial periodicity is not essential for place cell responses in familiar environments, which is consistent with studies suggesting that the development of place cell responses does not depend on the development of grid cell responses.

These data support the hypothesized role of theta rhythm oscillations in the generation of grid cell spatial periodicity or at least a role of MS input. The loss of grid cell spatial periodicity could contribute to the spatial memory impairments caused by lesions or inactivation of the MS. These data support a role of neuronal oscillations in the coding of spatial information.

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