Synchronized neuronal activities in neocortical explant cultures

Gutnick, Michael J.; Wolfson, B.; Baldino, Frank

doi:10.1007/bf00253630

Cited by 26 publications

(10 citation statements)

References 36 publications

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“…The nLFP peaks were indicative of population spikes (Jimbo and Robinson, 2000; Bédard et al, 2004) and occurred in bursts of approximately synchronous activity with quiescent intervals spanning several seconds (Fig. 1 B ), consistent with previous studies (Crain, 1966; Calvet, 1974; Gutnick et al, 1989; Maeda et al, 1995; Kamioka et al, 1996; Plenz and Aertsen, 1996; Corner et al, 2002; Eytan and Marom, 2006). The timing of the detected nLFP peaks is sufficient to reveal important spatiotemporal patterns of the activities obeying power scaling law, so-called neuronal avalanches (Beggs and Plenz, 2003, 2004; Stewart and Plenz, 2006; Gireesh and Plenz, 2008).…”

Section: Resultssupporting

confidence: 90%

Hierarchical Interaction Structure of Neural Activities in Cortical Slice Cultures

Santos¹,

Gireesh²,

Plenz³

et al. 2010

Journal of Neuroscience

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Recent advances in the analysis of neuronal activities suggest that the instantaneous activity patterns can be mostly explained by considering only first-order and pairwise interactions between recorded elements, i.e., action potentials or local field potentials (LFP), and do not require higher-than-pairwise-order interactions. If generally applicable, this pairwise approach greatly simplifies the description of network interactions. However, an important question remains: are the recorded elements the units of interaction that best describe neuronal activity patterns? To explore this, we recorded spontaneous LFP peak activities in cortical organotypic cultures using planar, integrated 60-microelectrode arrays. We compared predictions obtained using a pairwise approach with those using a hierarchical approach that uses two different spatial units for describing the activity interactions: single electrodes and electrode clusters. In this hierarchical model, short-range interactions within each cluster were modeled by pairwise interactions of electrode activities and longrange interactions were modeled by pairwise interactions of cluster activities. Despite the relatively low number of parameters used, the hierarchical model provided a more accurate description of the activity patterns than the pairwise model when applied to ensembles of 10 electrodes. Furthermore, the hierarchical model was successfully applied to a larger-scale data of ϳ60 electrodes. Electrode activities within clusters were highly correlated and spatially contiguous. In contrast, long-range interactions were diffuse, suggesting the presence of higher-than-pairwise-order interactions involved in the LFP peak activities. Thus, the identification of appropriate units of interaction may allow for the successful characterization of neuronal activities in large-scale networks.

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Section: Resultssupporting

confidence: 90%

Hierarchical Interaction Structure of Neural Activities in Cortical Slice Cultures

Santos¹,

Gireesh²,

Plenz³

et al. 2010

Journal of Neuroscience

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“…1 B), in agreement with previous reports of synchronized bursting in dissociated and cortical slice cultures (Crain, 1966;Calvet, 1974: Gutnick et al, 1989Maeda et al, 1995;Gopal and Gross, 1996;Kamioka et al, 1996;Plenz and Aertsen, 1996b;Plenz and Kitai, 1996). Our recent analysis revealed that these epochs are composed of neuronal avalanches, successive but distinct periods of neuronal activity with inherently complex spatiotemporal structure (Fig.…”

Section: General Description Of Cultures and Spontaneous Activitysupporting

confidence: 90%

Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures

Beggs

Plenz²

2004

J. Neurosci.

547

506

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A major goal of neuroscience is to elucidate mechanisms of cortical information processing and storage. Previous work from our laboratory (Beggs and Plenz, 2003) revealed that propagation of local field potentials (LFPs) in cortical circuits could be described by the same equations that govern avalanches. Whereas modeling studies suggested that these "neuronal avalanches" were optimal for information transmission, it was not clear what role they could play in information storage. Work from numerous other laboratories has shown that cortical structures can generate reproducible spatiotemporal patterns of activity that could be used as a substrate for memory. Here, we show that although neuronal avalanches lasted only a few milliseconds, their spatiotemporal patterns were also stable and significantly repeatable even many hours later. To investigate these issues, we cultured coronal slices of rat cortex for 4 weeks on 60-channel microelectrode arrays and recorded spontaneous extracellular LFPs continuously for 10 hr. Using correlation-based clustering and a global contrast function, we found that each cortical culture spontaneously produced 4736 Ϯ 2769 (mean Ϯ SD) neuronal avalanches per hour that clustered into 30 Ϯ 14 statistically significant families of spatiotemporal patterns. In 10 hr of recording, over 98% of the mutual information shared by these avalanche patterns were retained. Additionally, jittering analysis revealed that the correlations between avalanches were temporally precise to within Ϯ4 msec. The long-term stability, diversity, and temporal precision of these avalanches indicate that they fulfill many of the requirements expected of a substrate for memory and suggest that they play a central role in both information transmission and storage within cortical networks.

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“…Average multiunit firing rates were variable between cultures (median 5.1 Hz, interquartile range 1.4–8.6 Hz), in all likelihood due to the variable number of neurons recorded from per electrode. Overall, activity patterns combined features typical of networks hyperexcited by nominally zero extracellular magnesium (Gutnick et al, 1989; Kawaguchi, 2001) and features reported in previous studies on rat neocortical slice cultures in less activity-fostering conditions (Plenz and Kitai, 1996; Klostermann and Wahle, 1999; Hentschke et al, 2005; Johnson and Buonomano, 2007; Czarnecki et al, 2012). …”

Section: Resultssupporting

confidence: 58%

“…In order to assess the contribution of GABA A versus GABA B receptors to the inhibitory effects of NO-711, we performed experiments in which blockers of either receptor type were applied prior to NO-711. GABA A receptor blockade by 100 μM bicuculline transformed activity into a regular pattern of stereotyped bursts characterized by intense firing activity, strong oscillatory (~10 Hz) components and prolonged silent periods between bursts, typical of disinhibited cortical networks (Gutnick et al, 1989; Castro-Alamancos et al, 2007; Sanchez-Vives et al, 2010; Figures 4A,C ). By contrast, GABA B receptor blockade by CGP 55845 (5 or 10 μM) altered activity in a moderate and selective manner, primarily by prolonging bursts ( Figures 4B,D ).…”

Section: Resultsmentioning

confidence: 99%

Impairment of GABA transporter GAT-1 terminates cortical recurrent network activity via enhanced phasic inhibition

Razik¹,

Hawellek²,

Antkowiak³

et al. 2013

Front. Neural Circuits

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In the central nervous system, GABA transporters (GATs) very efficiently clear synaptically released GABA from the extracellular space, and thus exert a tight control on GABAergic inhibition. In neocortex, GABAergic inhibition is heavily recruited during recurrent phases of spontaneous action potential activity which alternate with neuronally quiet periods. Therefore, such activity should be quite sensitive to minute alterations of GAT function. Here, we explored the effects of a gradual impairment of GAT-1 and GAT-2/3 on spontaneous recurrent network activity – termed network bursts and silent periods – in organotypic slice cultures of rat neocortex. The GAT-1 specific antagonist NO-711 depressed activity already at nanomolar concentrations (IC50 for depression of spontaneous multiunit firing rate of 42 nM), reaching a level of 80% at 500–1000 nM. By contrast, the GAT-2/3 preferring antagonist SNAP-5114 had weaker and less consistent effects. Several lines of evidence pointed toward an enhancement of phasic GABAergic inhibition as the dominant activity-depressing mechanism: network bursts were drastically shortened, phasic GABAergic currents decayed slower, and neuronal excitability during ongoing activity was diminished. In silent periods, NO-711 had little effect on neuronal excitability or membrane resistance, quite in contrast to the effects of muscimol, a GABA mimetic which activates GABAA receptors tonically. Our results suggest that an enhancement of phasic GABAergic inhibition efficiently curtails cortical recurrent activity and may mediate antiepileptic effects of therapeutically relevant concentrations of GAT-1 antagonists.

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Synchronized neuronal activities in neocortical explant cultures

Cited by 26 publications

References 36 publications

Hierarchical Interaction Structure of Neural Activities in Cortical Slice Cultures

Hierarchical Interaction Structure of Neural Activities in Cortical Slice Cultures

Neuronal Avalanches Are Diverse and Precise Activity Patterns That Are Stable for Many Hours in Cortical Slice Cultures

Impairment of GABA transporter GAT-1 terminates cortical recurrent network activity via enhanced phasic inhibition

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