Axo-Axonal Coupling

Schmitz, Dietmar; Schuchmann, Sebastian; Fisahn, André; Draguhn, Andreas; Buhl, Eberhard H.; Petrasch‐Parwez, Elisabeth; Dermietzel, Rolf; Heinemann, Uwe; Traub, Roger D.

doi:10.1016/s0896-6273(01)00410-x

Cited by 399 publications

(114 citation statements)

References 53 publications

(3 reference statements)

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“…The reduction in gamma power by the gap-junction blocking agent carbenoxolone suggested that the axons of layer II͞III are electrically coupled, as appears to be the case for pyramidal neurons in hippocampus (27,32). Finally, although not a comprehensive computational model of neocortical networks as yet, the model predicted accurately the physiological and pharmacological experimental data presented, and suggested that RS neurons and FRB neurons are electrically interconnected, and that such interconnections are critical for persistent neocortical gamma oscillations.…”

Section: Discussionmentioning

confidence: 84%

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A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro

Cunningham

Whittington

Bibbig

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

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152

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Basic cellular and network mechanisms underlying gamma frequency oscillations (30 -80 Hz) have been well characterized in the hippocampus and associated structures. In these regions, gamma rhythms are seen as an emergent property of networks of principal cells and fast-spiking interneurons. In contrast, in the neocortex a number of elegant studies have shown that specific types of principal neuron exist that are capable of generating powerful gamma frequency outputs on the basis of their intrinsic conductances alone. These fast rhythmic bursting (FRB) neurons (sometimes referred to as ''chattering'' cells) are activated by sensory stimuli and generate multiple action potentials per gamma period. Here, we demonstrate that FRB neurons may function by providing a large-scale input to an axon plexus consisting of gap-junctionally connected axons from both FRB neurons and their anatomically similar counterparts regular spiking neurons. The resulting network gamma oscillation shares all of the properties of gamma oscillations generated in the hippocampus but with the additional critical dependence on multiple spiking in FRB cells.G amma frequency oscillations are readily recordable from scalp and depth electroencephalogram electrodes placed over or in the neocortex of humans and laboratory animals. They occur spontaneously at low amplitude or transiently at larger amplitudes in response to sensory stimuli (1, 2). Their role in processing of sensory information has been proposed to involve the establishment of a temporal framework within which longrange synchronization of individual neuronal elements coding for specific sensory events can occur (3). Qualitatively similar oscillations also occur in the hippocampus (4) and entorhinal cortex (5), where their generation can be ascribed to the phasic or tonic (or a combination of both) excitation of fast spiking (FS) interneurons, the outputs of which, in turn, provide a temporal framework for controlling the outputs of principal cells (6, 7).Although much is known of the mechanisms underlying gamma oscillations in the archicortex and entorhinal cortex, relatively little evidence is available to suggest a mechanism (or mechanisms) involved in generating neocortical gamma oscillations. What is known is that specific neurons exist within the neocortical mantle that are capable of generating outputs within the gamma frequency range on the basis of intrinsic properties alone (in the absence of influences from local networks). Such neurons exhibit fast rhythmic bursting (FRB), with interburst frequencies of 20 Hz and upward, in response to depolarizing current injection alone (8-10). These FRB neurons (sometimes called ''chattering cells'') have also been shown to participate in visually evoked gamma (25-70 Hz) oscillations in vivo (8), with the FRB cells morphologically identified as spiny layer II͞III pyramidal neurons. Other principal neocortical neurons also possess the ability to generate activity within the gamma band on the basis of intrinsic properties alone in layer IV ...

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Section: Discussionmentioning

confidence: 84%

“…In the model, RS spikelets occurred on average at 2.2 Hz (12 cells) and corresponded to axonal spikes that conducted antidromically with decrement (ref. 27 and Fig. 2 A), whereas axonal spikes in FRB cells mainly led to full spikes or multiplets, presumably because of the relative depolarization and altered intrinsic currents in FRB cells.…”

Section: Resultsmentioning

confidence: 95%

A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro

Cunningham

Whittington

Bibbig

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

177

152

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“…The model simulations predicted that, if ectopic spikes provided the main driving force for the generation of the rhythm, then conduction of these spikes through gap junctions forming an axonal plexus would be a critical component of the mechanism. Dye coupling within layer V neuron populations has been observed in adult cortex (22) and the huge incidence of spikelets, associated with axo-axonic dye coupling and gap junctional communication in hippocampus (23)(24), suggested such a mechanism possibly may underlie the beta2 rhythm. Both octanol (1 mM, data not shown) and carbenoxolone (0.2 mM, Fig.…”

Section: Resultsmentioning

confidence: 99%

“…In addition, layer V neurons form a major input pathway to basal ganglia, which also demonstrate beta rhythms (10). Here, we demonstrate an in vitro model that shows that a beta2 rhythm (20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) can be specifically generated in layer V of neocortex in a manner independent of gamma rhythmogenesis and of glutamatergic synaptic excitation. Beta2 generation in layer V stands in contrast to cortical gamma rhythms that have been shown to originate in layers II͞III in in vitro models (11) and may underlie cortico-cortical synchronization (12).…”

mentioning

confidence: 76%

“…Here we show an in vitro model of concurrent but independently generated gamma (30-70 Hz) rhythms in layer II͞III and beta2 (20)(21)(22)(23)(24)(25)(26)(27)(28)(29)(30) 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.…”

mentioning

confidence: 99%

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

Roopun

Middleton²,

Cunningham³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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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 ...

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The emerging functions of oligodendrocytes in regulating neuronal network behaviour

Hoz

Simons

2014

BioEssays

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Myelin is required for efficient nerve conduction, but not all axons are myelinated to the same extent. Here we review recent studies that have revealed distinct myelination patterns of different axonal paths, suggesting that myelination is not an all or none phenomenon and that its presence is finely regulated in central nervous system networks. Whereas powerful reductionist biology has led to important knowledge of how oligodendrocytes function by themselves, little is known about their role in neuronal networks. We still do not understand how oligodendrocytes integrate information from neurons to adapt their function to the need of the system. An intricate cross talk between neurons and glia is likely to exist and to determine how neuronal circuits operate as a whole. Dissecting these mechanisms by using integrative systems biology approaches is one of the major challenges ahead.

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Axo-Axonal Coupling

Cited by 399 publications

References 53 publications

A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro

A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro

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

The emerging functions of oligodendrocytes in regulating neuronal network behaviour

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