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J Neurosci. 2014 Nov 5;34(45):14984-94. doi: 10.1523/JNEUROSCI.1091-14.2014.

Millisecond timescale synchrony among hippocampal neurons.

Author information

1
Department of Psychology, University of Wisconsin-Milwaukee, Milwaukee, Wisconsin 53201, Center for Molecular and Behavioral Neuroscience, Rutgers University-Newark, Newark, New Jersey 07102, diba@uwm.edu.
2
Department of Mathematics, City College, City University of New York, New York, New York 10031, Center for Molecular and Behavioral Neuroscience, Rutgers University-Newark, Newark, New Jersey 07102, Departments of Biology and Psychology, Graduate Center, City University of New York, New York, New York 10031, and.
3
Allen Institute for Brain Science, Seattle, Washington 98103, Center for Molecular and Behavioral Neuroscience, Rutgers University-Newark, Newark, New Jersey 07102, Neuroscience Institute, New York University, New York, New York 10016.
4
Center for Molecular and Behavioral Neuroscience, Rutgers University-Newark, Newark, New Jersey 07102, Neuroscience Institute, New York University, New York, New York 10016.

Abstract

Inhibitory neurons in cortical circuits play critical roles in composing spike timing and oscillatory patterns in neuronal activity. These roles in turn require coherent activation of interneurons at different timescales. To investigate how the local circuitry provides for these activities, we applied resampled cross-correlation analyses to large-scale recordings of neuronal populations in the cornu ammonis 1 (CA1) and CA3 regions of the hippocampus of freely moving rats. Significant counts in the cross-correlation of cell pairs, relative to jittered surrogate spike-trains, allowed us to identify the effective couplings between neurons in CA1 and CA3 hippocampal regions on the timescale of milliseconds. In addition to putative excitatory and inhibitory monosynaptic connections, we uncovered prominent millisecond timescale synchrony between cell pairs, observed as peaks in the central 0 ms bin of cross-correlograms. This millisecond timescale synchrony appeared to be independent of network state, excitatory input, and γ oscillations. Moreover, it was frequently observed between cells of differing putative interneuronal type, arguing against gap junctions as the sole underlying source. Our observations corroborate recent in vitro findings suggesting that inhibition alone is sufficient to synchronize interneurons at such fast timescales. Moreover, we show that this synchronous spiking may cause stronger inhibition and rebound spiking in target neurons, pointing toward a potential function for millisecond synchrony of interneurons in shaping and affecting timing in pyramidal populations within and downstream from the circuit.

KEYWORDS:

fast oscillations; gap junctions; hippocampus; interneurons; networks; synchrony

PMID:
25378164
PMCID:
PMC4220030
DOI:
10.1523/JNEUROSCI.1091-14.2014
[Indexed for MEDLINE]
Free PMC Article

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