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 ␣-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.gap junction ͉ intrinsic bursting ͉ layer 5 ͉ M current ͉ neocortex T he mammalian neocortex generates a broad range of electroencephalogram rhythms concurrently in the awake behaving state. Some rhythms are strongly associated with sensory processing (the gamma band; ref. 1), whereas others are associated with cortical outputs (the beta band; ref.2). Here we show an in vitro model of concurrent but independently generated gamma (30-70 Hz) rhythms in layer rhythms in layer V somatosensory cortex. The beta2 rhythm occurred robustly in layer V intrinsically bursting (IB) neurons, in the form of bursts admixed with spikelets, and single action potentials. It was blocked by reducing gap junction conductance with carbenoxolone and was unaffected by blockade of synaptic transmission sufficient to ablate the layer II͞III gamma rhythm. It also could be seen in the absence of synaptic transmission with axonal excitability enhanced with 4-aminopyridine, suggesting a nonsynaptic rhythm mediated by axonal excitation. A network model, based on the hypothesis of electrical coupling via axons, is consistent with this hypothesis. The frequency of this network beta2 rhythm was set by the magnitude of M current in IB neurons. Our data suggest the possibility that a normally occurring cortical network oscillation involved in motor control could be generated largely or entirely by nonsynaptic mechanisms.Electroencephalogram beta oscillations, particularly those in the higher beta2 frequency range, have been recorded over premotor, supplementary motor, somatosensory, and other parietal cortical areas, in rats (3), monkeys (2, 4, 5), and humans (6). The oscillations are associated with sensory cues requiring sustained motor response and occur during the anticipatory period leading up to directed movement after such a sensory cue. The origin of these in vivo beta rhythms is unclear; however, pyramidal tract neurons (lying in layer V; ref. 7) and motor cortex local field potentials exhibit coherence at beta2 frequencies with hand and forearm electromyographic activity, in monkeys performing a precision grip task (8, 9), suggesting that beta2 oscillations originate in layer V in vivo. In addition, layer V neurons form a major input pathway to basal ganglia, which also demonstrate ...

Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3

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Neurophysiologic correlates of fMRI in human motor cortex

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Gap junctions on hippocampal mossy fiber axons demonstrated by thin-section electron microscopy and freeze–fracture replica immunogold labeling

“…The role of axonal gap junctions has been investigated in relation to physiological and possibly pathological alterations of electrical activities of the brain, including ␤2 oscillations (20-30 Hz), ␥ oscillations (30-70 Hz), and very fast oscillations (Ͼ100 Hz) (6)(7)(8)(9)(10)(11)35). Oscillations at 250-300 Hz have been recorded in sclerotic human hippocampus, surgically removed and studied in vitro (36).…”

“…Schmitz and colleagues (7) provided electrophysiological and dye coupling evidence for axoaxonic gap junctions in CA1 and CA3 pyramidal cells as well as in dentate granule cells. Subsequently, both modeling and in vitro experimental data suggested that axonal gap junctions could account for very fast oscillations (Ͼ70 Hz), including Ϸ200-Hz ripples (8,9) as well as play a critical role in the generation of persistent ␥ (30-70 Hz) (10) and neocortical ␤2 (20-30 Hz) oscillations (11). However, definitive ultrastructural evidence for gap junctions in cortical principal cells has been elusive.…”