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Integration of Synaptic Responses to Neighboring Whiskers in Rat Barrel Cortex In Vivo

Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania

Submitted 2 September 2004; accepted in final form 15 November 2004

Characterizing input integration at the single-cell level is a critical step to understanding cortical function, particularly when sensory stimuli are represented over wide cortical areas and single cells exhibit large receptive fields. To study synaptic integration of sensory inputs, we made intracellular recordings from the barrel cortex of anesthetized rats in vivo. For each cell, we deflected the principal whisker (PW) either alone or preceded by the deflection of a single adjacent whisker (AW) at an interval of 20 or 3 ms. At the 20-ms interval in all cases, prior AW deflection significantly suppressed the PW-evoked spike output and caused the underlying synaptic response to reach a peak Vm less depolarized than that arising from PW deflection alone. The decrease in peak Vm was not attributed to hyperpolarizing inhibition but to a divisive reduction in PW-evoked PSP amplitude. The reduction in amplitude was not a result of shunting inhibition but was mostly a result of removal of the synaptic drive, or disfacilitation. When the AW–PW interval was shortened to 3 ms, spike suppression was observed in a subset of the cells studied. In most cases, a divisive reduction in synaptic response amplitude was offset by summation with the preceding AW-evoked depolarization. To determine whether suppression is a general feature of synaptic integration by barrel cortex neurons, we also characterized the interaction of responses evoked by local electrical stimulation. In contrast to the whisker data, we found that responses to paired stimulation at the same intervals produced more spikes and reached a peak Vm more depolarized than the individual responses alone, suggesting that whisker-evoked suppression is not a result of postsynaptic mechanisms. Instead, we propose that cross-whisker response suppression depends on sensory-specific mechanisms at cortical and subcortical levels.

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