Computation by oscillations: Implications of experimental data for theoretical models of grid cells

Giocomo, Lisa M.; Hasselmo, Michael E.

doi:10.1002/hipo.20501

Cited by 65 publications

(120 citation statements)

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“…This model provides an alternate implementation of the oscillatory interference model Burgess, 2008) that is compared to the implementation using membrane potential oscillations Hasselmo et al, 2007;Giocomo and Hasselmo, 2008a).…”

Section: Introductionmentioning

confidence: 99%

“…Previous modeling showed that membrane potential oscillations in entorhinal neurons might also contribute to grid cell firing Giocomo et al, 2007;Hasselmo et al, 2007;Giocomo and Hasselmo, 2008a). Entorhinal Layer II stellate cells show subthreshold membrane potential oscillations when depolarized near firing threshold (Alonso and Llinas, 1989;Alonso and Klink, 1993;Giocomo et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

“…These subthreshold oscillations can influence the timing of action potentials and network oscillations (Alonso and Garcia-Austt, 1987;Acker et al, 2003). The frequency of membrane potential oscillations differs systematically along the dorsal to ventral axis of the medial entorhinal cortex Giocomo and Hasselmo, 2008a). Previous modeling showed how these differences in membrane potential oscillation frequency could underlie differences in grid cell spatial periodicity along the dorsal to ventral axis Giocomo et al, 2007;Hasselmo et al, 2007;Giocomo and Hasselmo, 2008a).…”

Section: Introductionmentioning

confidence: 99%

“…The frequency of membrane potential oscillations differs systematically along the dorsal to ventral axis of the medial entorhinal cortex Giocomo and Hasselmo, 2008a). Previous modeling showed how these differences in membrane potential oscillation frequency could underlie differences in grid cell spatial periodicity along the dorsal to ventral axis Giocomo et al, 2007;Hasselmo et al, 2007;Giocomo and Hasselmo, 2008a). The oscillations appear to be due to a hyperpolarization-activated cation current known as the h-current (Dickson et al, 2000) that differs in time constant along the dorsal to ventral axis (Giocomo and Hasselmo, 2008b).…”

Section: Introductionmentioning

confidence: 99%

“…The oscillations appear to be due to a hyperpolarization-activated cation current known as the h-current (Dickson et al, 2000) that differs in time constant along the dorsal to ventral axis (Giocomo and Hasselmo, 2008b). In contrast to stellate cells, membrane potential oscillations do not usually appear in Layer II and III pyramidal cells (Alonso and Klink, 1993), but are observed in Layer V pyramidal cells, where they may be caused by M-current (Yoshida and Alonso, 2007;Giocomo and Hasselmo, 2008a). Membrane potential oscillations do not appear in neurons of the lateral entorhinal cortex (Tahvildari and Alonso, 2005), and grid cells do not appear in lateral entorhinal cortex (Hargreaves et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

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Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

2008

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ABSTRACT:This article presents a model of grid cell firing based on the intrinsic persistent firing shown experimentally in neurons of entorhinal cortex. In this model, the mechanism of persistent firing allows individual neurons to hold a stable baseline firing frequency. Depolarizing input from speed-modulated head direction cells transiently shifts the frequency of firing from baseline, resulting in a shift in spiking phase in proportion to the integral of velocity. The convergence of input from different persistent firing neurons causes spiking in a grid cell only when the persistent firing neurons are within similar phase ranges. This model effectively simulates the two-dimensional firing of grid cells in open field environments, as well as the properties of theta phase precession. This model provides an alternate implementation of oscillatory interference models. The persistent firing could also interact on a circuit level with rhythmic inhibition and neurons showing membrane potential oscillations to code position with spiking phase. These mechanisms could operate in parallel with computation of position from visual angle and distance of stimuli. In addition to simulating two-dimensional grid patterns, models of phase interference can account for context-dependent firing in other tasks. In network simulations of entorhinal cortex, hippocampus, and postsubiculum, the reset of phase effectively replicates context-dependent firing by entorhinal and hippocampal neurons during performance of a continuous spatial alternation task, a delayed spatial alternation task with running in a wheel during the delay period (Pastalkova et al., Science, 2008), and a hairpin maze task.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

2008

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A metric for space

2008

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ABSTRACT:Not all areas of neuronal systems investigation have matured to the stage where computation can be understood at the microcircuit level. In mammals, insights into cortical circuit functions have been obtained for the early stages of sensory systems, where signals can be followed through networks of increasing complexity from the receptors to the primary sensory cortices. These studies have suggested how neurons and neuronal networks extract features from the external world, but how the brain generates its own codes, in the higher-order nonsensory parts of the cortex, has remained deeply mysterious. In this terra incognita, a path was opened by the discovery of grid cells, place-modulated entorhinal neurons whose firing locations define a periodic triangular or hexagonal array covering the entirety of the animal's available environment. This array of firing is maintained in spite of ongoing changes in the animal's speed and direction, suggesting that grid cells are part of the brain's metric for representation of space. Because the crystal-like structure of the firing fields is created within the nervous system itself, grid cells may provide scientists with direct access to some of the most basic operational principles of cortical circuits. V

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Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex

et al. 2008

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ABSTRACT:Grid cells are topographically organized in the sense that, within the dorsal part of the medial entorhinal cortex, the scale of the grid increases systematically with anatomical distance from the dorsal border of this brain area. The ventral limit of the spatial map is currently not known. To determine if the grid map extends into the intermediate and ventral parts of the medial entorhinal cortex, we recorded activity from entorhinal principal cells at multiple dorsoventral levels while rats shuttled back and forth on an 18 m long linear track. The recordings spanned a range of more than 3 mm, covering approximately three quarters of the dorsoventral extent of the medial entorhinal cortex. Distinct periodic firing fields were observed at all recording levels. The average interpeak distance between the fields increased from $50 cm in the most dorsal part to $3 m at the most ventral recording positions. The increase in grid scale was accompanied by a decrease in the frequency of theta modulation and the rate of phase precession. The increase in average spacing and field size was approximately linear but this relationship coincided with a substantial increase in the variability of each measure. Taken together, the observations suggest that the spatial scale of the grid representation increases progressively along most of the dorsoventral axis of the medial entorhinal cortex, mirroring the topographical scale expansion observed in place cells in the hippocampus. V V C 2008 Wiley-Liss, Inc.

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Computation by oscillations: Implications of experimental data for theoretical models of grid cells

Cited by 65 publications

References 73 publications

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

Grid cell mechanisms and function: Contributions of entorhinal persistent spiking and phase resetting

A metric for space

Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex

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