Synchronized excitation and inhibition driven by intrinsically bursting neurons in neocortex

Y. Chagnac-Amitai, B. W. Connors

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289 Scopus citations


The cellular mechanisms of synchronous synaptic activity were studied in isolated slices of rat SmI neocortex in which γ-aminobutyric acid (GABA)-mediated inhibition was slightly suppressed. Intracellular measurements were made from single neurons, and extracellular recordings monitored the timing and intensity of population events. Neurons in cortical layers II-VI were classified by the attributes of their single action potentials and repetitive firing patterns during injection of intracellular current pulses. Regular-spiking (RS) cells occurred in all layers and had relatively long-duration spikes and strong frequency adaptation. Intrinsically bursting (IB) cells occurred only in layers IV and V and generated bursts of ≥3 spikes; some IB cells of lower-layer V produced repetitive bursts during long depolarizing pulses. Fast-spiking (FS) cells had brief spikes and little or no adaptation and fired at high frequencies. When GABA(A)-mediated inhibition was slightly reduced with low doses of bicuculline methiodide (BMI, 0.8-1.0 μM), synchronous events were evoked by stimulating layer VI with single shocks. Synchronous events were characterized by prominent, often all-or-none extracellular field potentials that propagated horizontally for variable distances up to several millimeters. Large field potentials were invariably correlated with excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) in single neurons. Both PSPs and field potentials often had long (up to 250 ms) and variable latencies, and sometimes two or more events were generated by single stimuli. In all cases the PSPs and field potentials were synchronous. Both field potentials and single cells sometimes generated short epochs (3-7 peaks) of rhythmic events at 20-50 Hz. The psychological class of single neurons was correlated with the relative dominance of excitation and inhibition during each synchronous event. In phase with each synchronous event, most RS cells were very strongly inhibited with only small amounts of concurrent excitation. By contrast, IB cells were strongly and consistently excited, with relatively little inhibition. FS cells were also phasically excited. Anatomic studies have identified RS and IB cells as pyramidal cells and FS cells as GABAergic nonpyramidal cells. This implies that, during the synchronous events of the present study, the majority of pyramidal cells were dominated by IPSPs. Synchronous excitation of FS cells, the presumed inhibitory interneurons, is consistent with this. Only a subset of the pyramidal neurons, almost all of them IB cells of the middle layers, displayed strong, synchronous excitation and clusters of action potentials. The data imply that the intrinsic membrane properties of neocortical neurons are correlated with their local synaptic connections. We suggest that a network of IB cells in middle cortical layers, because of the unique membrane characteristics and excitatory interconnections of its neurons, can initiate and coordinate synchronous EPSPs and IPSPs within the entire local population of neurons.

Original languageEnglish
Pages (from-to)1149-1162
Number of pages14
JournalJournal of Neurophysiology
Issue number5
StatePublished - 1 Jan 1989
Externally publishedYes

ASJC Scopus subject areas

  • Neuroscience (all)
  • Physiology


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