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The Journal of Neuroscience, May 26, 2004, 24(21):5031-5043; doi:10.1523/JNEUROSCI.0357-04.2004

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Behavioral/Systems/Cognitive
GABA_A Synapses Shape Neuronal Responses to Sound Intensity in the Inferior Colliculus

Shobhana Sivaramakrishnan, Susanne J. Sterbing-D'Angelo, Blagoje Filipovic, William R. D'Angelo, Douglas L. Oliver, and Shigeyuki Kuwada

Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030

Neurons in the inferior colliculus (IC) change their firing rates with sound pressure level. Some neurons maintain monotonic increases in firing rate over a wide range of sound intensities, whereas other neurons are monotonic over limited intensity ranges. We examined the conditions necessary for monotonicity in this nucleus in vitro in rat brain slices and in vivo in the unanesthetized rabbit. Our in vitro recordings indicate that concurrent activation of GABA_A synapses with excitatory inputs facilitates monotonic increases in firing rate with increases in stimulus strength. In the absence of synaptic inhibition, excitatory input to IC neurons causes large depolarizations that result in firing block and nonmonotonicity. In vivo, although GABA_A synapses decrease the firing rate in all IC neurons, they can have opposing effects on rate-level functions. GABAergic inputs activated by all sound intensities maintain monotonicity by keeping the postsynaptic potential below the level at which depolarization block occurs. When these inputs are blocked, firing block can occur and rate-level functions become nonmonotonic. High-threshold GABAergic inputs, in contrast, cause nonmonotonic responses by decreasing the firing rate at high intensities. Our results suggest that a dynamic regulation of the postsynaptic membrane potential by synaptic inhibition is necessary to allow neurons to respond monotonically to a wide range of sound intensities.

Key words: inferior colliculus; rate coding; depolarization block; synaptic inhibition; GABA; sensory coding; synaptic depression

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Received Feb 1, 2004; revised April 21, 2004; accepted April 22, 2004.

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