A beta2-frequency (20-30 Hz) oscillation in nonsynaptic networks of somatosensory cortex

Abstract

Beta2 frequency (20-30 Hz) oscillations appear over somatosensory and motor cortices in vivo during motor preparation and can be coherent with muscle electrical activity. We describe a beta2 frequency oscillation occurring in vitro in networks of layer V pyramidal cells, the cells of origin of the corticospinal tract. This beta2 oscillation depends on gap junctional coupling, but it survives a cut through layer 4 and, hence, does not depend on apical dendritic electrogenesis. It also survives a blockade of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors or a blockade of GABA(A) receptors that is sufficient to suppress gamma (30-70 Hz) oscillations in superficial cortical layers. The oscillation period is determined by the M type of K+ current.

Fig. 1.

Beta2 rhythms are generated in deep layers of cortex. (A) Spectrograms of field rhythms generated in somatosensory cortex slices by 400 nM kainate. Superficial layers generated gamma frequency (30–50 Hz) signals (layer II/III). Deep layers concurrently generated beta2 frequency signals (layer V, 20–30 Hz). Layer IV recordings show both frequency bands coexisting. Below each spectrogram are representative field potential traces (Scale bars: 0.2 mV, 100 ms). (B) Surgical separation of deep from superficial layers at the layer IV/V border abolished neither rhythm. Cartoon illustrates the electrode position for the power spectra taken from 60-s epochs of field potential data in the superficial layers (a–c, black lines) and deep layers (d and e, red lines).

Fig. 2.

Antidromic-appearing activity in LV IB cells predominates during beta2 rhythms. (A Left) Example trace (2.5-s) from an electrophysiologically and anatomically identified layer V IB cell reveals combinations of spikelets, single spikes, and spike bursts at beta2 frequencies (mean resting membrane potentials −55 mV). Power spectra show the frequency content of concurrently recorded IB cell (blue, IB) and layer V field (black, ec). (A Right) Field and tufted IB cell data are accurately predicted from antidromic spiking in model. (Scale bars: 10 mV, experiment intracellular; 100 μV, experiment field; 15 mV, model; 500 ms. (B) Expanded timescale examples of layer V IB cell activity during field beta rhythms. (Scale bars: 10 mV, experiment; 15 mV model; 10 ms.) (C) Beta2 frequency is correlated with g_K(M)-mediated control of burst duration. (C Left) Mean peak frequency (n = 5) of layer V field potentials. The decrease in population frequency with M current reduction (linopirdine 0–20 μM) was accompanied by increased IB cell burst duration. Examples are shown with 2 and 20 μM linopirdine. (C Right) Peak population frequency of model IB cells by using different g_K(M) from 5% to 50% of control. Example bursts were taken with IB cell g_K(M) = 50% and 5% of control. (Scale bars: 30 mV, experiment; 40 mV, model; 10 ms.)

Fig. 3.

Beta2 rhythms in nonsynaptic networks of IB cells. (A Left) Mean power spectra derived from 60-s epochs of oscillation from layer V field potentials (n = 5) showed blockade of beta2 activity by the gap junction blocker carbenoxolone (control, black; 0.2 mM carbenoxolone, red). Example traces show layer V beta2 activity (ec) and antidromic-appearing activity in an IB cell (IB) before and 1 h after carbenoxolone. (A Right) Corresponding model spectra and IB activity in the presence (black line) and absence (red line) of gap junctional conductances. (Scale bars: 20 mV, experiment; 25 mV, model; 0.5 s.) (B Left) Beta2 rhythms can be elicited in the absence of the main fast excitatory and inhibitory synaptic transmission pathways. Experimental data shows mean power spectrum (derived from n = 5, 2-s epochs of data) of layer V population activity in the presence of blockers for AMPA, kainate, NMDA, and GABA receptors (20 μM NBQX, 50 μM dAP5, 20 μM bicuculline, and 10 μM CGP55845); there was also bath application of 4-aminopyridine (40 μM) to increase neuronal excitability, compensating for the blockade of the original kainate receptor-mediated drive. Example traces show that, in these nonsynaptic conditions, activity is dominated by antidromically appearing full and partial spikes in IB cells. (B Right) The model can reproduce this beta2 rhythm accurately in the absence of synaptic conductances, when axonal R_m is doubled. The model full and partial spikes indeed are antidromic. (Scale bars: 20 mV, experiment; 25 mV, model; 500 ms.)