Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference

Welday, Adam C.; Shlifer, I.G.; Bloom, M. L.; Zhang, K.; Blair, Hugh T.

doi:10.1523/jneurosci.0712-11.2011

Cited by 126 publications

(238 citation statements)

References 89 publications

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“…formation, including one based on attractors (30) and those based on oscillatory interference (6,(31)(32)(33). It seems possible that these temporal changes might be triggered by the release of a neuromodulator, such as ACh, which is implicated in novelty detection (34,35) and affects both the frequency of theta-band oscillations (36) and the resonant properties of mEC stellate cells (37).…”

Section: Discussionmentioning

confidence: 99%

Grid cell firing patterns signal environmental novelty by expansion

Barry

Ginzberg²,

O’Keefe

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

192

255

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The hippocampal formation plays key roles in representing an animal's location and in detecting environmental novelty to create or update those representations. However, the mechanisms behind this latter function are unclear. Here, we show that environmental novelty causes the spatial firing patterns of grid cells to expand in scale and reduce in regularity, reverting to their familiar scale as the environment becomes familiar. Simultaneously recorded place cell firing fields remapped and showed a smaller, temporary expansion. Grid expansion provides a potential mechanism for novelty signaling and may enhance the formation of new hippocampal representations, whereas the subsequent slow reduction in scale provides a potential familiarity signal.single unit | spatial memory | hippocampus G rid cells in the medial entorhinal cortex (mEC) of freely moving rodents exhibit a striking triangular grid-like firing pattern (1). Although the grid patterns are anchored to familiar environmental cues (1, 2), their maintenance in darkness and across different environments (1, 3) suggests that they provide a constant metric for self-motion (1, 3-7). Place cells in hippocampal regions CA1 and CA3 tend to fire in single firing fields (8), coding for self-location within an environment. Place cells create novel representations for new environments ("remapping") (3, 9, 10) providing a neural substrate for memory; they show attractor dynamics (11-13) and long-term plasticity (14), and they become increasingly stable and focal with prolonged experience of an environment (15,16). In contrast, grid cells are thought to retain their regular spatial structure, scale, and position relative to other grids in novel environments (1, 3), changing only their orientation and spatial offset relative to the environment and showing a brief reduction in spatial stability (1). Grid cells (1,7,17), in conjunction with other environmental inputs (6,(18)(19)(20)(21), are thought to provide an important input to hippocampal place cells. Conversely, direct and indirect projections from CA1 to the deep layers of the mEC (22, 23) have been proposed as a possibly route by which extrinsic sensory information might reach grids (21), a view supported by developmental and inactivation studies (24-26). Together, these points raise questions about the relationship between entorhinal and hippocampal activity; for example: Does stable grid cell firing co-occur with labile place fields, and what drives place cell remapping?In experiment 1, we investigated grid cell firing on first exposure to a new environment and as it became increasingly familiar during trials conducted on the same day and then on subsequent days. In experiment 2, we replicated the experiment using different environments, while corecording grid cells and place cells from a second cohort of rats that had received bilateral mEC and hippocampal implants. Together, these experiments showed that grid cell firing patterns were spatially expanded and less regular in novel arenas than in a similarly size...

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Section: Discussionmentioning

confidence: 99%

Grid cell firing patterns signal environmental novelty by expansion

Barry

Ginzberg²,

O’Keefe

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

192

255

View full text Add to dashboard Cite

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“…In particular, most models do not incorporate intrinsic properties of neurons. The model presented in this article builds on previous models of grid cells, including the oscillatory interference model [3][4][5] and ring attractor model [6,28], but with a specific focus on addressing physiological data on intrinsic rebound spiking and theta cycle skipping not addressed by previous models. In particular, the model is motivated by the desire to address the correlation between grid cell properties and the presence and frequency of resonance in medial entorhinal neurons [29][30][31][32][33][34][35][36][37] and the potential functional role of rebound spiking of stellate cells owing to the hyperpolarization-activated cation current (h current) [37][38][39].…”

Section: Introductionmentioning

confidence: 99%

Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex

Hasselmo

2014

Phil. Trans. R. Soc. B

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Data show a relationship of cellular resonance and network oscillations in the entorhinal cortex to the spatial periodicity of grid cells. This paper presents a model that simulates the resonance and rebound spiking properties of entorhinal neurons to generate spatial periodicity dependent upon phasic input from medial septum. The model shows that a difference in spatial periodicity can result from a difference in neuronal resonance frequency that replicates data from several experiments. The model also demonstrates a functional role for the phenomenon of theta cycle skipping in the medial entorhinal cortex.

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“…Thus, the continuous attractor class of models favors representation of position immediately in two dimensions, with no intermediate one-dimensional stage, and did not predict band cells (but is not incompatible with the existence of band cells). The oscillatory interference model would be greatly supported by the existence of band cells, but alternate forms of the model may also be implemented without band cells (Welday et al 2011).…”

mentioning

confidence: 99%

Grids from bands, or bands from grids? An examination of the effects of single unit contamination on grid cell firing fields

Navratilova

Godfrey

McNaughton

2016

Journal of Neurophysiology

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Neural recording technology is improving rapidly, allowing for the detection of spikes from hundreds of cells simultaneously. The limiting step in multielectrode electrophysiology continues to be single cell isolation. However, this step is crucial to the interpretation of data from putative single neurons. We present here, in simulation, an illustration of possibly erroneous conclusions that may be reached when poorly isolated single cell data are analyzed. Grid cells are neurons recorded in rodents, and bats, that spike in equally spaced locations in a hexagonal pattern. One theory states that grid firing patterns arise from a combination of band firing patterns. However, we show here that summing the grid firing patterns of two poorly resolved neurons can result in spurious band-like patterns. Thus, evidence of neurons spiking in band patterns must undergo extreme scrutiny before it is accepted. Toward this aim, we discuss single cell isolation methods and metrics.

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Cosine Directional Tuning of Theta Cell Burst Frequencies: Evidence for Spatial Coding by Oscillatory Interference

Cited by 126 publications

References 89 publications

Grid cell firing patterns signal environmental novelty by expansion

Grid cell firing patterns signal environmental novelty by expansion

Neuronal rebound spiking, resonance frequency and theta cycle skipping may contribute to grid cell firing in medial entorhinal cortex

Grids from bands, or bands from grids? An examination of the effects of single unit contamination on grid cell firing fields

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