Gamma oscillations in the entorhinal cortex of the freely behaving rat - PubMed (original) (raw)

Gamma oscillations in the entorhinal cortex of the freely behaving rat

J J Chrobak et al. J Neurosci. 1998.

Abstract

Gamma frequency field oscillations (40-100 Hz) are nested within theta oscillations in the dentate-hilar and CA1-CA3 regions of the hippocampus during exploratory behaviors. These oscillations reflect synchronized synaptic potentials that entrain the discharge of neuronal populations within the approximately 10-25 msec range. Using multisite recordings in freely behaving rats, we examined gamma oscillations within the superficial layers (I-III) of the entorhinal cortex. These oscillations increased in amplitude and regularity in association with entorhinal theta waves. Gamma waves showed an amplitude minimum and reversed in phase near the perisomatic region of layer II, indicating that they represent synchronized synaptic potentials impinging on layer II-III neurons. Theta and gamma oscillations in the entorhinal cortex were coupled with theta and gamma oscillations in the dentate hilar region. The majority of layer II-III neurons discharged irregularly but were phase-related to the negative peak of the local (layer II-III) gamma field oscillation. These findings demonstrate that layer II-III neurons discharge in temporally defined gamma windows (approximately 10-25 msec) coupled to the theta cycle. This transient temporal framework, which emerges in both the entorhinal cortex and the hippocampus, may allow spatially distributed subpopulations to form temporally defined ensembles. We speculate that the theta-gamma pattern in the discharge of these neurons is essential for effective neuronal communication and synaptic plasticity in the perforant pathway.

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Figures

Fig. 1.

Fig. 1.

Gamma and theta waves in the entorhinal cortex.A, Depth (left) profile of entorhinal theta waves. A 16-site silicon probe (13 most ventral sites shown) was used to record field and unit activity concurrently at multiple laminar sites within the entorhinal cortex. The span of the recorded area is indicated by lines in B. Note the gradual decrease in amplitude and phase shift of theta, which then reverses in phase near the superficial aspect of layer II (compare trace 1 with traces 4–13). B, Image (right) is a Nissl-stained section illustrating the position of the 16-site recording probe within the superficial layers of the entorhinal cortex. rs, Rhinal sulcus;para, parasubiculum; ld, lamina dissecans; I–V, specific lamina. C, Power spectra of EEG extracts during different behaviors. Large peaks at theta frequency (8–9 Hz bins) were present during_RUNNING_ and REM sleep but not during slow wave sleep (SWS; these peaks are cut off to emphasize gamma power). The asterisk indicates the third harmonic of theta frequency peak (absent during SWS). Note similar gamma peaks during RUNNING and_REM_ sleep and absence of gamma frequency peak during_SWS_ episode. The _y_-scale (POWER) is linear.

Fig. 2.

Fig. 2.

Depth versus amplitude profiles of theta and gamma oscillations in the entorhinal cortex. A, B, Averaged extracellular field potentials illustrating theta and gamma oscillations across layers I–III of the entorhinal cortex. The averager was triggered by the positive peaks of filtered (1–20 Hz; 50–150 Hz) waves recorded from site 1 (bottom trace). The wide null zone of gamma waves is attributable to the oblique penetration of the recording silicon probe (shown in Fig. 1).C, Corresponding current source density analysis of gamma oscillation. Cold colors; Sinks; hot colors, sources. D–G, Laminar distribution of power, coherence, and phases of theta and gamma oscillations. Coherence and phase measurements are relative to site 2 from_bottom_. The values indicate summed values from the spectra from 6 to 12 Hz (theta) and 40 to 120 Hz (gamma). Note phase reversal of gamma oscillation between layers I and II.

Fig. 3.

Fig. 3.

Relation of entorhinal theta to entorhinal gamma.A, Single sweep illustrating theta and gamma waves in the entorhinal cortex at six recording positions along the axis of a 16-site recording probe. Six black traces are gamma-filtered (50–150 Hz); two gray traces show concurrent theta waves (1–20 Hz). Numerals at_right_ refer to recording positions on silicon probe. Theta records at positions 1 (layer I) and_8_ (layer III) are from same sites as gamma traces shown. Note amplitude variation of gamma oscillation at different recording sites. Note also the prominent relation between phase of theta and the amplitude gamma waves. B, Averaged (n = 402) extracellular field potentials (wide band) as triggered from negative peaks of local gamma oscillation (at site 3). Note the sudden phase reversal of gamma waves between sites 1 and 2. C, arrow, Recording site 1; asterisk, tissue tear.

Fig. 4.

Fig. 4.

Synchrony between theta and gamma oscillations recorded within layers I–III of caudalateral entorhinal cortex and ipsilateral dentate region. A, Averaged field potentials (n = 366) from the dentate hilar region (gray traces) and layer III of EC (black trace), triggered by negative peaks of dentate gamma oscillation (short trace; filtered 50–150 Hz).B, Averaged field potentials (n = 262) from EC layers III and I (black traces) and ipsilateral dentate hilus (gray trace) triggered by negative peaks (layer III) of entorhinal gamma oscillation (short trace; filtered 50–150 Hz). C, Cross-correlogram between entorhinal gamma waves and dentate gamma oscillation. The 0 (reference) point was the negative peak of filtered layer III gamma waves. Arrows point to multiple peaks in cross-correlogram, emphasizing the transient synchronicity in the entorhinal and hippocampal oscillators.

Fig. 5.

Fig. 5.

Neuronal activity in layers II and III is phase-locked to gamma waves. A, Adjacent Nissl-stained sections illustrating tip of electrode near layer II of the entorhinal cortex taken from brain pictured at B. B, Silicon probe as it emerges from sectioned rat brain during histological processing. Inset, Probe in relation to edge of brain (arrows are placed at ventral brain surface). No reversal of gamma oscillation was observed along any of 16 dorsoventral sites along this probe, which recorded from layers II–V of the entorhinal cortex. C, Relationship between simultaneously recorded single units and local gamma oscillation, recorded with the lower eight recording sites of the silicon probe in layers II and III. Arrows point to two single units (verified by the absence of spikes ≥1 msec in autocorrelograms); a third single unit from site number 15 was also recorded, which did not discharge in trace shown. Top trace (from site 13), Single 50 msec gamma wave epoch (50–150 Hz). Traces 9–16, Unit filtered traces (0.5–5 KHz). Note prominent single units during this 50 msec sweep in traces 11 and_13_, as well as their phase relationship to gamma field oscillation. D, Cross-correlograms between units_11_, 13, and 15 (not present in trace shown in C) and gamma field oscillation. Note discharge peaks of units in relation to average gamma wave (top trace). Traces at_right_ of each correlogram illustrate unfiltered (wide-band) average of first 30 discriminated waveforms (top) and last 30 discriminated waveforms (bottom).

Fig. 6.

Fig. 6.

Relationship of putative interneuron of layer II to local theta and gamma oscillations. A1, A2, Two 400 msec sweeps from single recording electrode in layer II of the entorhinal cortex. Top trace is filtered for unit activity (0.5–5 KHz), middle for gamma oscillation (50–150 Hz), and lower gray trace for theta (1–20 Hz). Note rhythmic trains of firing in A1 in association with nested theta–gamma cycles, as well as a more continous discharge pattern in A2. B, Relationship of single-unit activity to local field gamma oscillation. Top gray trace, Average wide-band trace (1 Hz–5 kHz), triggered from negative peak of local gamma oscillation (n = 244).Bottom, Cross-correlogram showing prominent theta–gamma modulation of unit discharge. Inset at_right_, Autocorrelogram of this unit.Inset, Unfiltered (1 Hz–5 kHz) average of first 30 discriminated waveforms (top) and last 30 discriminated waveforms (bottom). Note short duration (<0.5 msec) of the action potential.

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