Generation of theta rhythm in medial entorhinal cortex of freely moving rats

The anterior thalamic nuclei are assumed to support episodic memory with anterior thalamic dysfunction a core feature of diencephalic amnesia. To date, the electrophysiological characterization of this region in behaving rodents has been restricted to the anterodorsal nucleus. Here we compared single-unit spikes with population activity in the anteroventral nucleus (AV) of freely moving rats during foraging and during naturally occurring sleep. We identified AV units that synchronize their bursting activity in the 6–11 Hz range. We show for the first time in freely moving rats that a subgroup of AV neurons is strongly entrained by theta oscillations. This feature together with their firing properties and spike shape suggests they be classified as “theta” units. To prove the selectivity of AV theta cells for theta rhythm, we compared the relation of spiking rhythmicity to local field potentials during theta and non-theta periods. The most distinguishable non-theta oscillations in rodent anterior thalamus are sleep spindles. We therefore compared the firing properties of AV units during theta and spindle periods. We found that theta and spindle oscillations differ in their spatial distribution within AV, suggesting separate cellular sources for these oscillations. While theta-bursting neurons were related to the distribution of local field theta power, spindle amplitude was independent of the theta units' position. Slow- and fast-spiking bursting units that are selectively entrained to theta rhythm comprise 23.7% of AV neurons. Our results provide a framework for electrophysiological classification of AV neurons as part of theta limbic circuitry.

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Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats

Journal of Neuroscience ◽

10.1523/jneurosci.02-03-00292.1982 ◽

1982 ◽

Vol 2 (3) ◽

pp. 292-302 ◽

Cited By ~ 239

Author(s):

SJ Mitchell ◽

JN Rawlins ◽

O Steward ◽

DS Olton

Keyword(s):

Entorhinal Cortex ◽

Theta Rhythm ◽

Septal Area ◽

Radial Arm Maze ◽

Medial Entorhinal Cortex ◽

Medial Septal Area

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Contribution of synapses in the medial supramammillary nucleus to the frequency of hippocampal theta rhythm in freely moving rats

Hippocampus ◽

10.1002/hipo.450050605 ◽

1995 ◽

Vol 5 (6) ◽

pp. 534-545 ◽

Cited By ~ 60

Author(s):

Neil McNaughton ◽

Barbara Logan ◽

Kiran S. Panickar ◽

Ian J. Kirk ◽

Wei-Xing Pan ◽

...

Keyword(s):

Theta Rhythm ◽

Hippocampal Theta Rhythm ◽

Freely Moving Rats ◽

Supramammillary Nucleus ◽

Freely Moving ◽

Hippocampal Theta

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Structural modularity and grid activity in the medial entorhinal cortex

Journal of Neurophysiology ◽

10.1152/jn.00574.2017 ◽

2018 ◽

Vol 119 (6) ◽

pp. 2129-2144 ◽

Cited By ~ 5

Author(s):

Robert K. Naumann ◽

Patricia Preston-Ferrer ◽

Michael Brecht ◽

Andrea Burgalossi

Keyword(s):

Entorhinal Cortex ◽

Cell Types ◽

Modular System ◽

Anatomical Location ◽

Grid Cells ◽

Medial Entorhinal Cortex ◽

Freely Moving ◽

Open Question ◽

To Receive ◽

Cortical Architecture

Following the groundbreaking discovery of grid cells, the medial entorhinal cortex (MEC) has become the focus of intense anatomical, physiological, and computational investigations. Whether and how grid activity maps onto cell types and cortical architecture is still an open question. Fundamental similarities in microcircuits, function, and connectivity suggest a homology between rodent MEC and human posteromedial entorhinal cortex. Both are specialized for spatial processing and display similar cellular organization, consisting of layer 2 pyramidal/calbindin cell patches superimposed on scattered stellate neurons. Recent data indicate the existence of a further nonoverlapping modular system (zinc patches) within the superficial MEC layers. Zinc and calbindin patches have been shown to receive largely segregated inputs from the presubiculum and parasubiculum. Grid cells are also clustered in the MEC, and we discuss possible structure-function schemes on how grid activity could map onto cortical patch systems. We hypothesize that in the superficial layers of the MEC, anatomical location can be predictive of function; thus relating functional properties and neuronal morphologies to the cortical modules will be necessary for resolving how grid activity maps onto cortical architecture. Imaging or cell identification approaches in freely moving animals will be required for testing this hypothesis.

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Head-direction cells escaping attractor dynamics in the parahippocampal region

10.1101/268110 ◽

2018 ◽

Author(s):

Olga Kornienko ◽

Patrick Latuske ◽

Laura Kohler ◽

Kevin Allen

Keyword(s):

Entorhinal Cortex ◽

Computational Models ◽

Head Direction ◽

Grid Cells ◽

Visual Landmarks ◽

Head Direction Cells ◽

Medial Entorhinal Cortex ◽

Attractor Dynamics ◽

Freely Moving ◽

Uniform Population

AbstractNavigation depends on the activity of head-direction (HD) cells. Computational models postulate that HD cells form a uniform population that reacts coherently to changes in landmarks. We tested whether this applied to HD cells of the medial entorhinal cortex and parasubiculum, areas where the HD signal contributes to the periodic firing of grid cells. Manipulations of the visual landmarks surrounding freely-moving mice altered the tuning of HD cells. Importantly, these tuning modifications were often non-coherent across cells, refuting the notion that HD cells form a uniform population constrained by attractor-like dynamics. Instead, examination of theta rhythmicity 1revealed two types of HD cells, theta rhythmic and non-rhythmic cells. Larger tuning alterations were observed predominantly in non-rhythmic HD cells. Moreover, only non-rhythmic HD cells reorganized their firing associations in response to visual land-mark changes. These findings reveal a theta non-rhythmic HD signal whose malleable organization is controlled by visual landmarks.

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Slow gamma rhythms in CA3 are entrained by slow gamma activity in the dentate gyrus

Journal of Neurophysiology ◽

10.1152/jn.00499.2016 ◽

2016 ◽

Vol 116 (6) ◽

pp. 2594-2603 ◽

Cited By ~ 12

Author(s):

Yi-Tse Hsiao ◽

Chenguang Zheng ◽

Laura Lee Colgin

Keyword(s):

Dentate Gyrus ◽

Entorhinal Cortex ◽

Place Cell ◽

Gamma Activity ◽

Causality Analysis ◽

Medial Entorhinal Cortex ◽

Granger Causality Analysis ◽

Hippocampal Area ◽

Gamma Rhythms ◽

Freely Moving

In hippocampal area CA1, slow (∼25–55 Hz) and fast (∼60–100 Hz) gamma rhythms are coupled with different CA1 afferents. CA1 slow gamma is coupled to inputs from CA3, and CA1 fast gamma is coupled to inputs from the medial entorhinal cortex (Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. Nature 462: 353–357, 2009). CA3 gives rise to highly divergent associational projections, and it is possible that reverberating activity in these connections generates slow gamma rhythms in the hippocampus. However, hippocampal gamma is maximal upstream of CA3, in the dentate gyrus (DG) region (Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. J Neurosci 15: 47–60, 1995). Thus it is possible that slow gamma in CA3 is driven by inputs from DG, yet few studies have examined slow and fast gamma rhythms in DG recordings. Here we investigated slow and fast gamma rhythms in paired recordings from DG and CA3 in freely moving rats to determine whether slow and fast gamma rhythms in CA3 are entrained by DG. We found that slow gamma rhythms, as opposed to fast gamma rhythms, were particularly prominent in DG. We investigated directional causal influences between DG and CA3 by Granger causality analysis and found that DG slow gamma influences CA3 slow gamma. Moreover, DG place cell spikes were strongly phase-locked to CA3 slow gamma rhythms, suggesting that DG excitatory projections to CA3 may underlie this directional influence. These results indicate that slow gamma rhythms do not originate in CA3 but rather slow gamma activity upstream in DG entrains slow gamma rhythms in CA3.

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Model of gradual phase shift of theta rhythm in the rat

Journal of Neurophysiology ◽

10.1152/jn.1984.52.6.1051 ◽

1984 ◽

Vol 52 (6) ◽

pp. 1051-1065 ◽

Cited By ~ 76

Author(s):

L. W. Leung

Keyword(s):

Phase Shift ◽

Pyramidal Cell ◽

Theta Rhythm ◽

Dendritic Tree ◽

Pyramidal Cells ◽

Phase Reversal ◽

Freely Moving Rats ◽

Theta Frequency ◽

Freely Moving ◽

Somatic Inhibition

CA1 pyramidal cell is modeled by a linked series of passive compartments representing the soma and different parts of the dendritic tree. Intracellular postsynaptic potentials are simulated by conductance changes at one or more compartments. By assuming an infinite homogeneous extracellular medium and a particular geometrical arrangement of pyramidal cells, field potential profiles are generated from the current source-sinks of the compartments. The pyramidal cells are driven at the theta (theta)-frequency at different sites of the dendritic tree in order to simulate external driving of hippocampus by the septal cells. Inhibitory or excitatory driving at different sites gives extracellular dipole fields of different null zones and maxima. Phase reversal (180 degrees) of a dipole field generated by synchronous synaptic currents is completed within a depth of 150 micron. By driving two spatially distinct but overlapping dipole fields slightly phase-shifted (30-90 degrees) from each other, the resultant field shows a gradual phase shift of 180 degrees in over 400 micron depth and no (stationary) null zones. The latter field correspond to the theta-profiles seen in the freely moving rat. Somatic inhibition is proposed to be the synaptic process generating the theta-field potentials (named dipole I) in the urethananesthetized or curarized rat. Dipole I has amplitude maxima at the basal dendritic and the distal apical dendritic layers, with a distinct null zone and phase reversal at the apical side of the CA1 pyramidal cell layer. Rhythmic distal dendritic excitation, time-delayed to somatic inhibition, is proposed to be the additional dipole (dipole II) found in freely moving rats. The combination of dipoles I and II, phase-shifted from each other, causes the gradual theta-field phase shift. Experimental studies indicate that dipole I is atropine-sensitive and probably driven by a cholinergic septohippocampal input, whereas dipole II is atropine-resistant and may come from a pathway through both the septum and the entorhinal cortex. Variations of the phase profiles of the theta-field in freely moving rats by administration of anesthetic and cholinergic drugs and by normal changes in theta-frequency could be accounted for by the proposed model. Changes of the intracellular membrane potential, cellular firing rate, and evoked excitability at different phases of the theta-rhythm in anesthetized and freely moving rats can be predicted from the model, and they are in general agreement with the extant literature. In conclusion, theta-field is generated by a rhythmic somatic inhibition phase-shifted with a distal apical-dendritic excitation.(ABSTRACT TRUNCATED AT 400 WORDS)

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Object-vector coding in the medial entorhinal cortex

10.1101/286286 ◽

2018 ◽

Cited By ~ 14

Author(s):

Øyvind Arne Høydal ◽

Emilie Ranheim Skytøen ◽

May-Britt Moser ◽

Edvard I. Moser

Keyword(s):

Entorhinal Cortex ◽

Head Direction ◽

Test Arena ◽

Medial Entorhinal Cortex ◽

Vector Coding ◽

Neural Representations ◽

Object Locations ◽

Novel Objects ◽

Freely Moving ◽

Representations Of Space

SummaryMammals use distances and directions from local objects to calculate trajectories during navigation but how such vectorial operations are implemented in neural representations of space has not been determined. Here we show in freely moving mice that a population of neurons in the medial entorhinal cortex (MEC) responds specifically when the animal is at a given distance and direction from a spatially confined object. These ‘object-vector cells’ are tuned similarly to a spectrum of discrete objects, irrespective of their location in the test arena. The vector relationships are expressed from the outset in novel environments with novel objects. Object-vector cells are distinct from grid cells, which use a distal reference frame, but the cells exhibit some mixed selectivity with head-direction and border cells. Collectively, these observations show that object locations are integrated in metric representations of self-location, with specific subsets of MEC neurons encoding vector relationships to individual objects.

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