Precisely timed spatiotemporal patterns of neural activity in dissociated cortical cultures

doi:10.1016/j.neuroscience.2007.05.025

Neuroscience

Volume 148, Issue 1, 10 August 2007, Pages 294-303

https://doi.org/10.1016/j.neuroscience.2007.05.025 Get rights and content

Abstract

Recurring patterns of neural activity, a potential substrate of both information transfer and transformation in cortical networks, have been observed in the intact brain and in brain slices. Do these patterns require the inherent cortical microcircuitry of such preparations or are they a general property of self-organizing neuronal networks? In networks of dissociated cortical neurons from rats—which lack evidence of the intact brain’s intrinsic cortical architecture—we have observed a robust set of spontaneously repeating spatiotemporal patterns of neural activity, using a template-matching algorithm that has been successful both in vivo and in brain slices. The observed patterns in cultured monolayer networks are stable over minutes of extracellular recording, occur throughout the culture’s development, and are temporally precise within milliseconds. The identification of these patterns in dissociated cultures opens a powerful methodological avenue for the study of such patterns, and their persistence despite the topological and morphological rearrangements of cellular dissociation is further evidence that precisely timed patterns are a universal emergent feature of self-organizing neuronal networks.

Section snippets

Cell culture

The data analyzed in this paper are from Wagenaar et al. (2006b), which is accompanied by a large publicly available dataset of recordings from dissociated embryonic day 18 (E18) rat cortical cultures. No additional experiments using animal cells were conducted for the present study.

Extracellular recording

Approximately 50,000 cells were plated in a 5 mm diameter droplet on top of an MEA containing 59 electrodes arranged in a rectangular grid with 200 μm spacing. The MEA’s signals were amplified and sent to a data

Results

Thirty minutes of spontaneous activity was recorded from each of 12 cultures, aged 21 days in vitro (DIV), derived from four separate platings (Wagenaar et al., 2006b). From these datasets, 1 min (arbitrarily the 16th minute of recording time) was examined with a template-matching algorithm (see Experimental Procedures) to determine the number of repeating sequences. The algorithm used a precision of 1 ms and a window size T=200 ms, following Nadasdy et al. (1999). On average, 2993±1077 unique

Discussion

We have shown the presence of persistently recurring, precisely timed sequences of action potentials in dissociated networks of cortical neurons, using an algorithm with noted success both in vivo in the rat hippocampus (Nadasdy et al., 1999) and in vitro in neocortical slices (Ikegaya et al., 2004). Examination of the persistence of these patterns suggests that the most frequently recurring sequences are maintained for at least several minutes following their initial observation. The patterns

Acknowledgments

We wish to thank Dieter Jaeger and Radhika Madhavan for helpful discussion, Sheri McKinney for technical assistance with cell culture, and our anonymous reviewers for suggesting significant improvements to the manuscript. This work was supported by the Emory University Graduate Division of Biological and Biomedical Sciences, the Whitaker Foundation, the Wallace H. Coulter Foundation, the NSF Center for Behavioral Neuroscience, NINDS grant NS38628, and NINDS/NIBIB grant EB00786.

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Systems neurosciencePrecisely timed spatiotemporal patterns of neural activity in dissociated cortical cultures

Abstract

Section snippets

Cell culture

Extracellular recording

Results

Discussion

Acknowledgments

Corticonics: neural circuits of the cerebral cortex

Spatiotemporal firing patterns in the frontal-cortex of behaving monkeys

J Neurophysiol

Detecting spatiotemporal firing patterns among simultaneously recorded single neurons

J Neurophysiol

Propagation of synchronous spiking activity in feedforward neural networks

J Physiol Paris

How nature works: the science of self-organized criticality

Self-organized criticality: an explanation of the 1/f noise

Phys Rev Lett

Precise spatiotemporal repeating patterns in monkey primary and supplementary motor areas occur at chance levels

J Neurophysiol

Culturing nerve cells

Does the 1/f frequency scaling of brain signals reflect self-organized critical states?

Phys Rev Lett

Neuronal avalanches in neocortical circuits

J Neurosci

Neuronal avalanches are diverse and precise activity patterns that are stable for many hours in cortical slice cultures

J Neurosci

On the dimensionality of cortical graphs

J Physiol Paris

Multiple significance tests: the Bonferroni method

BMJ

Spike timing-dependent plasticity: from synapse to perception

Physiol Rev

Rat cortical neurons in cell culture: culture methods, cell morphology, electrophysiology, and synapse formation

Brain Res

Multielectrode analysis of coordinated, multisite, rhythmic bursting in cultured CNS monolayer networks

J Neurosci

Dynamics and effective topology underlying synchronization in networks of cortical neurons

J Neurosci

Information trainsThe technique and its uses in spike train and network analysis, with examples taken from the nucleus parabrachialis medialis during sleep-waking states

Brain Res

Simultaneous single unit recording in vitro with a photoetched laser deinsulated gold multimicroelectrode surface

IEEE Trans Biomed Eng

The tempotron: a neuron that learns spike timing–based decisions

Nat Neurosci

The organization of behavior: a neuropsychological theory

Analysis of synfire chains

Network

Synfire chains and cortical songs: temporal modules of cortical activity

Science

Polychronization: computation with spikes

Neural Comput

Systems neuroscience
Precisely timed spatiotemporal patterns of neural activity in dissociated cortical cultures