Initiation of Spontaneous Epileptiform Activity in the Neocortical Slice

Tsau, Yang; Guan, Li; Wu, Jian-Young

doi:10.1152/jn.1998.80.2.978

Cited by 66 publications

(50 citation statements)

References 20 publications

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“…This suggests that, in agreement with previous studies (Connors, 1984;Chervin et al, 1988;Telfeian and Connors, 1998;Tsau et al, 1998), suppression of GABA A receptors within the barrel cortex is sufficient to evoke paroxysmal activity.…”

Section: Gabaergic Modulation Of Signal Propagationsupporting

confidence: 90%

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Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

2000

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We used optical imaging of voltage-sensitive dye signals to study the spatiotemporal spread of activity in the mouse barrel cortex, evoked by stimulation of thalamocortical afferents in an in vitro slice preparation. Stimulation of the thalamus, at low current intensity, results in activity largely restricted to a single barrel, and to the border between layers Vb and VI. Low concentrations of the GABA A receptor antagonist bicuculline increase the amplitude of the optical signals, without affecting their spatiotemporal propagation. Higher concentrations of bicuculline result in paroxysmal activity, which propagates via intracolumnar and intercolumnar excitatory pathways. Enhancing the activity of NMDA receptors, by removing Mg 2ϩ from the extracellular solution, dramatically alters the spatiotemporal pattern of excitation: activity spreads to supragranular and infragranular layers and adjacent barrel columns. This enhanced propagation is suppressed by the NMDA receptor antagonist AP5. A similar enhancement of activity propagation can be produced by stimulating the thalamus with a short, high-frequency pulse train. Application of AP5 suppresses the frequency-dependent spread of activity. These findings indicate that the spatiotemporal spread of activity in the barrel cortex is altered by varying the temporal patterns of thalamic inputs, via an NMDA receptor-mediated mechanism, and suggest that a similar process occurs during repetitive whisking activity. Key words: somatosensory cortex; voltage-sensitive dyes; glutamate; NMDA; GABA; epilepsy; temporal coding; mouseProcessing of sensory information in the cerebral cortex can be described as a hierarchical process, in which inputs from "specific" thalamic nuclei are integrated by their postsynaptic cortical targets, which, in turn, provide inputs to neurons in other layers of the same functional column and subsequently to adjacent columns (Gilbert, 1992;Keller, 1995;Rauschecker et al., 1997). Although this hierarchical scheme is oversimplified in that it omits factors such as parallel processing and feedback interactions, it is thought to faithfully represent at least the initial stages of cortical sensory processing (Stone et al., 1979;Felleman and Van Essen, 1991;Iwamura, 1993).To understand the mechanisms underlying cortical sensory processing, it is necessary to determine how thalamic inputs are integrated by their postsynaptic cortical neurons and propagated via intracolumnar and intercolumnar cortical pathways. This requires methods to identify discrete functional columns and to reveal the spatiotemporal propagation of thalamic inputs within and among these columns. In the present study we took advantage of a functional imaging approach (see Orbach and Cohen, 1983;Cinelli and Salzberg, 1987;Yuste et al., 1997;Keller et al., 1998) to investigate intracortical processing of thalamic inputs in the somatosensory cortex and its modulation by glutamatergic and GABAergic processes.The somatosensory cortex of certain rodent species contains representations of the my...

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Section: Gabaergic Modulation Of Signal Propagationsupporting

confidence: 90%

“…Relatively long-term incubation of cortical slices in solutions containing low concentrations of Mg 2ϩ may evoke spontaneous epileptic activity (Tsau et al, 1998). In our preparation we did not observe paroxysmal activity in either the optical responses or the field potentials (n ϭ 17).…”

Section: Nmda Receptors Mediate Spread Of Activitymentioning

confidence: 46%

Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

2000

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“…The increase in velocity with onset latency in some slices may result from interactions between multiple initiation zones along the extent of the recording array (Tsau et al, 1998;Ma et al, 2004). In a few cases, the existence of such zones was readily apparent.…”

Section: Transition From Initiation To Propagationmentioning

confidence: 99%

Initiation, Propagation, and Termination of Epileptiform Activity in Rodent NeocortexIn VitroInvolve Distinct Mechanisms

Pinto¹,

Patrick²,

Huang³

et al. 2005

J. Neurosci.

197

173

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Waves of epileptiform activity in neocortex have three phenomenological stages: initiation, propagation, and termination. We use a well studied model of epileptiform activity in vitro to investigate directly the hypothesis that each stage is governed by an independent mechanism within the underlying cortical circuit. Using the partially disinhibited neocortical slice preparation, activity is induced and modulated using neurotransmitter receptor antagonists and is measured using both intracellular recordings and a linear array of extracellular electrodes. We find that initiation depends on both synaptic excitation and inhibition and entails a slow process of recruitment at discrete spatial locations within cortical layer 5 but not layer 2/3. Propagation depends on synaptic excitation but not inhibition and is a fast process that involves neurons across the spatial extent of the slice and in all cortical layers. Termination is modulated by synaptic excitation and inhibition. In space, termination occurs reliably at discrete locations. In time, termination is characterized by a strong depolarizing shift (block) and recovery of neurons in all cortical layers. These results suggest that the phenomenological stages of epileptiform events correspond to distinct mechanistic stages.

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“…Neuronal population wave activity in slices cut normal (perpendicular) to the surface of the cortex produce unidirectional traveling waves as if the cortical circuits were functionally onedimensional (Chagnac-Amitai and Connors, 1989;Wadman and Gutnick, 1993;Golomb and Amitai, 1997;Tsau et al, 1998;Wu et al, 1999Wu et al, , 2001Bao and Wu, 2003). Population oscillatory wave activity in slices cut tangentially to the surface of the cortex (Fleidervish et al, 1998) can generate activities that suggest that the cortical circuits are functionally two-dimensional.…”

Section: Waves and Oscillationsmentioning

confidence: 99%

Spiral Waves in Disinhibited Mammalian Neocortex

Huang¹,

Troy²,

Yang³

et al. 2004

J. Neurosci.

374

292

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Spiral waves are a basic feature of excitable systems. Although such waves have been observed in a variety of biological systems, they have not been observed in the mammalian cortex during neuronal activity. Here, we report stable rotating spiral waves in rat neocortical slices visualized by voltage-sensitive dye imaging. Tissue from the occipital cortex (visual) was sectioned parallel to cortical lamina to preserve horizontal connections in layers III-V (500-m-thick, ϳ4 ϫ 6 mm 2 ). In such tangential slices, excitation waves propagated in two dimensions during cholinergic oscillations. Spiral waves occurred spontaneously and alternated with plane, ring, and irregular waves. The rotation rate of the spirals was ϳ10 turns per second, and the rotation was linked to the oscillations in a one-cycle-one-rotation manner. A small (Ͻ128 m) phase singularity occurred at the center of the spirals, about which were observed oscillations of widely distributed phases. The phase singularity drifted slowly across the tissue (ϳ1 mm/10 turns). We introduced a computational model of a cortical layer that predicted and replicated many of the features of our experimental findings. We speculate that rotating spiral waves may provide a spatial framework to organize cortical oscillations.

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Initiation of Spontaneous Epileptiform Activity in the Neocortical Slice

Cited by 66 publications

References 20 publications

Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

Thalamic-Evoked Synaptic Interactions in Barrel Cortex Revealed by Optical Imaging

Initiation, Propagation, and Termination of Epileptiform Activity in Rodent NeocortexIn VitroInvolve Distinct Mechanisms

Spiral Waves in Disinhibited Mammalian Neocortex

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