Development in the absence of spontaneous bioelectric activity results in increased stereotyped burst firing in cultures of dissociated cerebral cortex

Ramakers, G.J.A.; Corner, M.A.; Habets, A.M.M.C.

doi:10.1007/bf00228885

Cited by 95 publications

(71 citation statements)

References 28 publications

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“…Previous studies of homeostatic plasticity have primarily followed the consequences of experimentally imposed disruptions of neuronal function. For example, genetic manipulation (Davis et al, 1997;Sandrock et al, 1997;Davis and Goodman, 1998;Guan et al, 2005), physical isolation of parts of the nervous system (Turrigiano et al, 1995;Thoby-Brisson and Simmers, 1998), pharmacological treatments (Berg and Hall, 1975;Ramakers et al, 1990;Turrigiano et al, 1998), or sensory deprivation during development (Desai et al, 2002). Only the scaling of synaptic inputs over the course of normal postnatal development shows a similar naturally occurring homeostatic plasticity (Desai et al, 2002).…”

Section: Discussionmentioning

confidence: 99%

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

Rogers¹,

Krapp²,

Burrows³

et al. 2007

J. Neurosci.

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We characterized homeostatic plasticity at an identified sensory-motor synapse in an insect, which maintains constant levels of motor drive as locusts transform from their solitarious phase to their gregarious swarming phase. The same mechanism produces behaviorally relevant changes in response timing that can be understood in the context of an animal's altered behavioral state. For individual animals of either phase, different looming objects elicited different spiking responses in a visual looming detector interneuron, descending contralateral movement detector (DCMD), yet its synaptic drive to a leg motoneuron, fast extensor tibiae (FETi), always had the same maximum amplitude. Gregarious locust DCMDs produced more action potentials and had higher firing frequencies, but individual postsynaptic potentials (PSPs) elicited in FETi were half the amplitude of those in solitarious locusts. A model suggested that this alone could not explain the similarity in overall amplitude, and we show that facilitation increased the maximum compound PSP amplitude in gregarious animals. There was the same linear relationship between times of peak DCMD firing before collision and the size/velocity of looming objects in both phases. The DCMD-FETi synapse transformed this relationship nonlinearly, such that peak amplitudes of compound PSPs occurred disproportionately earlier for smaller/faster objects. Furthermore, the peak PSP amplitude occurred earlier in gregarious than in solitarious locusts, indicating a differential tuning. Homeostatic modulation of the amplitude, together with a nonlinear synaptic transformation of timing, acted together to tune the DCMD-FETi system so that swarming gregarious locusts respond earlier to small moving objects, such as conspecifics, than solitarious locusts.

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Section: Discussionmentioning

confidence: 99%

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

Rogers¹,

Krapp²,

Burrows³

et al. 2007

J. Neurosci.

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“…Consistent with this hypothesis, studies have shown spontaneous activity rates to be modifiable in response to chronic application of pharmacological agents (Ramakers et al, 1990;Turrigiano et al, 1998) or sensory deprivation (Maffei et al, 2004). However, it has not yet been established whether spontaneous activity can be regulated in vitro by altering levels of external activity presented in a physiological manner.…”

Section: Plasticity Of Spontaneous Activitymentioning

confidence: 97%

“…As mentioned above, plasticity in the levels of spontaneous activity in response to global pharmacological manipulations has been established (Ramakers et al, 1990;Rutherford et al, 1997;Turrigiano et al, 1998). However, it was not known whether levels of spontaneous activity are sensitive to manipulations that would mimic the synaptically driven activity observed in vivo.…”

Section: Plasticity Of Spontaneous Dynamicsmentioning

confidence: 99%

Development and Plasticity of Spontaneous Activity and Up States in Cortical Organotypic Slices

Johnson

Buonomano²

2007

J. Neurosci.

111

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Cortical computations are an emergent property of neural dynamics. To understand how neural dynamics emerges within local cortical networks, we characterized the development and underlying mechanisms of spontaneous dynamics in cortical organotypic slices. We observed not only a quantitative increase in the levels of spontaneous dynamics, but a qualitative transition from brief bursts of activity to well defined Up states during the first 4 weeks in vitro. Analysis of cellular and synaptic properties indicates that these changes are driven by increasing excitatory drive accompanied by changes in the balance of excitation and inhibition. Examination of the structure of spontaneous dynamics revealed no evidence of precisely repeating patterns. Slices exposed to chronic patterned stimulation exhibited decreased levels of spontaneous activity, suggesting homeostatic control of the levels of network activity. Together, these results suggest that Up states reflect a fundamental mode of network dynamics that emerges through the orchestrated regulation of multiple cellular and synaptic properties in parallel.

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“…Over the past 20 years, physiologists repeatedly demonstrated that, like in vivo neurons (Kenet et al, 2003), cortical networks in vitro spontaneously synchronize once every 1-20 s (Fig. 1b,c), generating assembly activity events (Habets et al, 1987;Ramakers et al, 1990;Ramakers, 1991, 1992;Muramoto et al, 1993;Maeda et al, 1995Maeda et al, , 1998Kamioka et al, 1996;Nakanishi and Kukita, 1998;Ben-Ari, 2001;Corner et al, 2002;Marom and Shahaf, 2002;Plenz, 2003, 2004;Wagenaar et al, 2005Wagenaar et al, , 2006. Synchronizations with similar kinetics may also be evoked by site-specific electrical stimuli (Jimbo et al, 1999;Eytan et al, 2003).…”

Section: Dynamicsmentioning

confidence: 99%

Dynamics and Effective Topology Underlying Synchronization in Networks of Cortical Neurons

2006

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Cognitive processes depend on synchronization and propagation of electrical activity within and between neuronal assemblies. In vivo measurements show that the size of individual assemblies depends on their function and varies considerably, but the timescale of assembly activation is in the range of 0.1-0.2 s and is primarily independent of assembly size. Here we use an in vitro experimental model of cortical assemblies to characterize the process underlying the timescale of synchronization, its relationship to the effective topology of connectivity within an assembly, and its impact on propagation of activity within and between assemblies. We show that the basic mode of assembly activation, "network spike," is a threshold-governed, synchronized population event of 0.1-0.2 s duration and follows the logistics of neuronal recruitment in an effectively scale-free connected network. Accordingly, the sequence of neuronal activation within a network spike is nonrandom and hierarchical; a small subset of neurons is consistently recruited tens of milliseconds before others. Theory predicts that scale-free topology allows for synchronization time that does not increase markedly with network size; our experiments with networks of different densities support this prediction. The activity of early-to-fire neurons reliably forecasts an upcoming network spike and provides means for expedited propagation between assemblies. We demonstrate this capacity by observing the dynamics of two artificially coupled assemblies in vitro, using neuronal activity of one as a trigger for electrical stimulation of the other.

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Development in the absence of spontaneous bioelectric activity results in increased stereotyped burst firing in cultures of dissociated cerebral cortex

Cited by 95 publications

References 28 publications

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

Compensatory Plasticity at an Identified Synapse Tunes a Visuomotor Pathway

Development and Plasticity of Spontaneous Activity and Up States in Cortical Organotypic Slices

Dynamics and Effective Topology Underlying Synchronization in Networks of Cortical Neurons

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