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Edited by Eric I. Knudsen, Stanford University School of Medicine, Stanford, CA, and approved January 29, 2016 (received for review October 23, 2015)
Significance
Understanding how excitatory and inhibitory inputs are integrated to achieve sensory selectivity is an important, but elusive, goal in neuroscience. Whole-cell recordings in vivo have revealed excitation and inhibition, but the computational mechanisms are generally unclear. In the inferior colliculus, neurons exist that respond selectively to short-duration sounds; the mechanistic basis of this selectivity has long been debated. We combined whole-cell recordings, in vivo, with conductance extraction algorithms and focal pharmacological manipulations to show that duration selectivity results from an anticoincidence of suprathreshold excitation and inhibition. These results challenge the widely held view that postinhibitory rebound depolarization must coincide with subthreshold excitation to generate duration selectivity.
Abstract
Sound duration is important in acoustic communication, including speech recognition in humans. Although duration-selective auditory neurons have been found, the underlying mechanisms are unclear. To investigate these mechanisms we combined in vivo whole-cell patch recordings from midbrain neurons, extraction of excitatory and inhibitory conductances, and focal pharmacological manipulations. We show that selectivity for short-duration stimuli results from integration of short-latency, sustained inhibition with delayed, phasic excitation; active membrane properties appeared to amplify responses to effective stimuli. Blocking GABAA receptors attenuated stimulus-related inhibition, revealed suprathreshold excitation at all stimulus durations, and decreased short-pass selectivity without changing resting potentials. Blocking AMPA and NMDA receptors to attenuate excitation confirmed that inhibition tracks stimulus duration and revealed no evidence of postinhibitory rebound depolarization inherent to coincidence models of duration selectivity. These results strongly support an anticoincidence mechanism of short-pass selectivity, wherein inhibition and suprathreshold excitation show greatest temporal overlap for long duration stimuli.
Footnotes
- ↵1To whom correspondence should be addressed. Email: rose{at}bioscience.utah.edu.
Author contributions: R.K.A., G.J.R., and C.J.L. designed research; R.K.A., G.J.R., J.L.H., C.J.L., G.A.V.-O., J.A.G., and J.W. performed research; R.K.A., G.J.R., C.J.L., and J.W. contributed new reagents/analytic tools; R.K.A., G.J.R., J.L.H., C.J.L., G.A.V.-O., and J.W. analyzed data; and R.K.A., G.J.R., J.L.H., C.J.L., and G.A.V.-O. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Mechanism for short-duration selectivity
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