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J Neurophysiol 91: 2551-2567, 2004. First published January 28, 2004; doi:10.1152/jn.01121.2003
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Intracortical Pathways Determine Breadth of Subthreshold Frequency Receptive Fields in Primary Auditory Cortex

Simranjit Kaur, Ronit Lazar and Raju Metherate

Department of Neurobiology and Behavior, University of California, Irvine, California 92697

Submitted 20 November 2003; accepted in final form 20 January 2004

To examine the basis of frequency receptive fields in auditory cortex (ACx), we have recorded intracellular (whole cell) and extracellular (local field potential, LFP) responses to tones in anesthetized rats. Frequency receptive fields derived from excitatory postsynaptic potentials (EPSPs) and LFPs from the same location resembled each other in terms of characteristic frequency (CF) and breadth of tuning, suggesting that LFPs reflect local synaptic (including subthreshold) activity. Subthreshold EPSP and LFP receptive fields were remarkably broad, often spanning five octaves (the maximum tested) at moderate intensities (40–50 dB above threshold). To identify receptive-field features that are generated intracortically, we microinjected the GABAA receptor agonist muscimol (0.2–5.1 mM, 1–5 µl) into ACx. Muscimol dramatically reduced LFP amplitude and reduced receptive-field bandwidth, implicating intracortical contributions to these features but had lesser effects on CF response threshold or onset latency, suggesting minimal loss of thalamocortical input. Reversal of muscimol's inhibition preferentially at the recording site by diffusion from the recording pipette of the GABAA receptor antagonist picrotoxin (0.01–100 µM) disinhibited responses to CF stimuli more than responses to spectrally distant, non-CF stimuli. We propose that thalamocortical and intracortical pathways preferentially contribute to responses evoked by CF and non-CF stimuli, respectively, and that intracortical projections linking frequency representations determine the breadth of receptive fields in primary ACx. Broad, subthreshold receptive fields may distinguish ACx from subcortical auditory relay nuclei, promote integrated responses to spectrotemporally complex stimuli, and provide a substrate for plasticity of cortical receptive fields and maps.


Address for reprint requests and other correspondence: R. Metherate, Dept. of Neurobiology and Behavior, University of California, 2205 McGaugh Hall, Irvine, CA 92697–4550. (E-mail: rmethera{at}uci.edu).




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