Relationship between individual neuron and network spontaneous activity in developing mouse cortex

Barnett, Heather; Gjorgjieva, Julijana; Weir, Keiko; Comfort, Cara; Fairhall, Adrienne L.; Moody, William J.

doi:10.1152/jn.00349.2014

Cited by 13 publications

(11 citation statements)

References 19 publications

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“…However, it remains to be tested whether sensory-modality thalamic nuclei might have a specific connexins expression patterns or stronger gap junction connectivity than adjacent thalamic regions, preventing the Ca 2+ waves from surpassing their borders. Our results with TTX and Carbenoxolone that block thalamic calcium waves, suggest similar mechanisms of generation and propagation of thalamic and neocortical spontaneous synchronous activity 33 34 .…”

Section: Discussionsupporting

confidence: 61%

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Prenatal thalamic waves regulate cortical area size prior to sensory processing

et al. 2017

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The cerebral cortex is organized into specialized sensory areas, whose initial territory is determined by intracortical molecular determinants. Yet, sensory cortical area size appears to be fine tuned during development to respond to functional adaptations. Here we demonstrate the existence of a prenatal sub-cortical mechanism that regulates the cortical areas size in mice. This mechanism is mediated by spontaneous thalamic calcium waves that propagate among sensory-modality thalamic nuclei up to the cortex and that provide a means of communication among sensory systems. Wave pattern alterations in one nucleus lead to changes in the pattern of the remaining ones, triggering changes in thalamic gene expression and cortical area size. Thus, silencing calcium waves in the auditory thalamus induces Rorβ upregulation in a neighbouring somatosensory nucleus preluding the enlargement of the barrel-field. These findings reveal that embryonic thalamic calcium waves coordinate cortical sensory area patterning and plasticity prior to sensory information processing.

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Section: Discussionsupporting

confidence: 61%

“…The function of gap-junctions has been implicated in the propagation of cortical waves in the developing neocortex 33 34 35 . Thus, we wondered whether gap-junctions might also participate in the mechanism of thalamic waves propagation.…”

Section: Resultsmentioning

confidence: 99%

Prenatal thalamic waves regulate cortical area size prior to sensory processing

et al. 2017

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“…This argues that the emergence of synchrony plays a fundamental role in achieving reliable propagation of a range of DC inputs (and correspondingly population firing rates) in the NGS networks. Although experimental measurements of the connectivity probability in developing cortical networks are lacking, calcium imaging of single neurons demonstrates that activity across many neurons during wave propagation is synchronous [34] . Intracellular recordings of adult cultured cortical networks also demonstrate that synchronous neuronal firing activity is transmitted in multiple layers [32] .…”

Section: Resultsmentioning

confidence: 99%

Intrinsic Neuronal Properties Switch the Mode of Information Transmission in Networks

et al. 2014

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Diverse ion channels and their dynamics endow single neurons with complex biophysical properties. These properties determine the heterogeneity of cell types that make up the brain, as constituents of neural circuits tuned to perform highly specific computations. How do biophysical properties of single neurons impact network function? We study a set of biophysical properties that emerge in cortical neurons during the first week of development, eventually allowing these neurons to adaptively scale the gain of their response to the amplitude of the fluctuations they encounter. During the same time period, these same neurons participate in large-scale waves of spontaneously generated electrical activity. We investigate the potential role of experimentally observed changes in intrinsic neuronal properties in determining the ability of cortical networks to propagate waves of activity. We show that such changes can strongly affect the ability of multi-layered feedforward networks to represent and transmit information on multiple timescales. With properties modeled on those observed at early stages of development, neurons are relatively insensitive to rapid fluctuations and tend to fire synchronously in response to wave-like events of large amplitude. Following developmental changes in voltage-dependent conductances, these same neurons become efficient encoders of fast input fluctuations over few layers, but lose the ability to transmit slower, population-wide input variations across many layers. Depending on the neurons' intrinsic properties, noise plays different roles in modulating neuronal input-output curves, which can dramatically impact network transmission. The developmental change in intrinsic properties supports a transformation of a networks function from the propagation of network-wide information to one in which computations are scaled to local activity. This work underscores the significance of simple changes in conductance parameters in governing how neurons represent and propagate information, and suggests a role for background synaptic noise in switching the mode of information transmission.

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“…Events were detected at a threshold 3 SDs above mean baseline, and the frequency of events was tabulated for each ROI. For high‐magnification Ca 2+ imaging experiments in Figures and , additional custom MATLAB routines were used to quantify Ca 2+ activity in individual cells as in Barnett et al (). Briefly, after detection of events in all RFP positive cells in the field of view, the average number of interneurons active during each frame was determined, and the occurrence of synchronous events was defined as those time points during which the number of cells active in a single frame exceeded the mean plus twice the standard deviation.…”

Section: Methodsmentioning

confidence: 99%

Distinct calcium signals in developing cortical interneurons persist despite disorganization of cortex by Tbr1 KO

Easton

Dickey

Moen

et al. 2015

Developmental Neurobiology

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Cortical development involves the structuring of network features by genetically programmed molecular signaling pathways. Additionally, spontaneous ion channel activity refines neuronal connections. We examine Ca(2+) fluctuations in the first postnatal week of normal mouse neocortex and that expressing knockout of the transcription factor T-brain-1 (Tbr1): a signaling molecule in cortical patterning and differentiation of excitatory neurons. In cortex, glutamatergic neurons express Tbr1 just before the onset of population electrical activity that is accompanied by intracellular Ca(2+) increases. It is known that glutamatergic cells are disordered with Tbr1 KO such that normal laying of the cortex, with newer born cells residing in superficial layers, does not occur. However, the fate of cortical interneurons is not well studied, nor is the ability of Tbr1 deficient cortex to express normal physiological activity. Using fluorescent proteins targeted to interneurons, we find that cortical interneurons are also disordered in the Tbr1 knockout. Using Ca(2+) imaging we find that population activity in mutant cortex occurs at normal frequencies with similar sensitivity to GABAA receptor blockade as in nonmutant cortex. Finally, using multichannel fluorescence imaging of Ca(2+) indicator dye and interneurons labeled with red fluorescent protein, we identify an additional Ca(2+) signal in interneurons distinct from population activity and with different pharmacological sensitivities. Our results show the population activity described here is a robust property of the developing network that continues in the absence of an important signaling molecule, Tbr1, and that cortical interneurons generate distinct forms of activity that may serve different developmental functions. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 705-720, 2016.

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Relationship between individual neuron and network spontaneous activity in developing mouse cortex

Abstract: Barnett HM, Gjorgjieva J, Weir K, Comfort C, Fairhall AL, Moody WJ. Relationship between individual neuron and network spontaneous activity in developing mouse cortex.

Cited by 13 publications

References 19 publications

Prenatal thalamic waves regulate cortical area size prior to sensory processing

Prenatal thalamic waves regulate cortical area size prior to sensory processing

Intrinsic Neuronal Properties Switch the Mode of Information Transmission in Networks

Distinct calcium signals in developing cortical interneurons persist despite disorganization of cortex by Tbr1 KO

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