Duration tuning in the auditory midbrain of echolocating and non-echolocating vertebrates

Sayegh, Riziq; Aubie, Brandon; Faure, Paul

doi:10.1007/s00359-011-0627-8

Cited by 44 publications

(69 citation statements)

References 96 publications

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“…In particular, cells tuned to stimulus duration, known as duration-tuned neurons (DTNs), are found first in the auditory midbrain of amphibians (Narins and Capranica, 1980) and mammals (Jen and Schlegel, 1982;Casseday et al, 1994;Chen, 1998;Fuzessery and Hall, 1999;Brand et al, 2000;Pérez-González et al, 2006;Wang et al, 2006). Auditory DTNs exist across vertebrate species and taxa and vary widely in their preferred range of signal durations (for review, see Sayegh et al, 2011). The existence of visual DTNs in the mammalian cortex suggests that neural mechanisms of duration selectivity may be shared across vertebrates and sensory modalities (Duysens et al, 1996).…”

Section: Introductionmentioning

confidence: 99%

Duration Tuning across Vertebrates

Aubie

Sayegh²,

Faure³

2012

J. Neurosci.

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Signal duration is important for identifying sound sources and determining signal meaning. Duration-tuned neurons (DTNs) respond preferentially to a range of stimulus durations and maximally to a best duration (BD). Duration-tuned neurons are found in the auditory midbrain of many vertebrates, although studied most extensively in bats. Studies of DTNs across vertebrates have identified cells with BDs and temporal response bandwidths that mirror the range of species-specific vocalizations. Neural tuning to stimulus duration appears to be universal among hearing vertebrates. Herein, we test the hypothesis that neural mechanisms underlying duration selectivity may be similar across vertebrates. We instantiated theoretical mechanisms of duration tuning in computational models to systematically explore the roles of excitatory and inhibitory receptor strengths, input latencies, and membrane time constant on duration tuning response profiles. We demonstrate that models of duration tuning with similar neural circuitry can be tuned with species-specific parameters to reproduce the responses of in vivo DTNs from the auditory midbrain. To relate and validate model output to in vivo responses, we collected electrophysiological data from the inferior colliculus of the awake big brown bat, Eptesicus fuscus, and present similar in vivo data from the published literature on DTNs in rats, mice, and frogs. Our results support the hypothesis that neural mechanisms of duration tuning may be shared across vertebrates despite species-specific differences in duration selectivity. Finally, we discuss how the underlying mechanisms of duration selectivity relate to other auditory feature detectors arising from the interaction of neural excitation and inhibition.

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Section: Introductionmentioning

confidence: 99%

Duration Tuning across Vertebrates

Aubie

Sayegh²,

Faure³

2012

J. Neurosci.

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“…Spiking responses of auditory DTNs have been studied in a variety of vertebrates and most extensively in echolocating bats (for review, see Sayegh et al 2011); however, until now a rigorous analysis of the efficacy of encoding stimulus duration by DTNs had not been performed. In this study, we measured information contained in the responses of individual cells and from a population of DTNs from the auditory midbrain of the big brown bat to characterize how DTNs encode stimulus duration.…”

Section: Discussionmentioning

confidence: 99%

“…Duration tuning curves of IC neurons were categorized into one of four response classes (short-pass, band-pass, long-pass, or all-pass) based on the spike count profile (Sayegh et al 2011). The spiking responses of DTNs are temporally selective and do not reflect the simple integration of stimulus energy.…”

Section: Obtaining Single Unit Responsesmentioning

confidence: 99%

“…Long-pass DTNs respond only when the stimulus exceeds some minimum duration. Unlike typical sensory neurons that integrate stimulus energy, the minimum duration for evoking a response in a long-pass DTN does not decrease with increasing stimulus amplitude/energy (Faure et al 2003;Sayegh et al 2011;Aubie et al 2012). Because long-pass DTNs do not have a BD, they were not included in this study.…”

Section: Obtaining Single Unit Responsesmentioning

confidence: 99%

“…We measured spike counts and latencies from auditory DTNs in the mammalian IC to characterize the information content of duration-selective neural responses. Previous studies, including those by the authors, have characterized the spiking profile of DTNs by the shape of the duration tuning curve (i.e., short-pass, band-pass, or long-pass) and defined the neuronal best duration (BD) to be the stimulus duration that evoked the peak spike count (Casseday et al 1994(Casseday et al , 2000Ehrlich et al 1997;Faure et al 2003;Aubie et al 2009Aubie et al , 2012Sayegh et al 2011). To test this hypothesis, we measured information content of DTN spiking responses by calculating the stimulus-specific information (SSI) and estimated observed Fisher information (FI).…”

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confidence: 99%

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Decoding stimulus duration from neural responses in the auditory midbrain

Aubie

Sayegh

Fremouw

et al. 2014

Journal of Neurophysiology

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(DTNs). Temporal specificity in their spiking suggests that one function of DTNs is to encode stimulus duration; however, the efficacy of duration encoding by DTNs has yet to be investigated. Herein, we characterize the information content of individual cells and a population of DTNs from the mammalian inferior colliculus (IC) by measuring the stimulus-specific information (SSI) and estimated Fisher information (FI) of spike count responses. We found that SSI was typically greatest for those stimulus durations that evoked maximum spike counts, defined as best duration (BD) stimuli, and that FI was maximal for stimulus durations off BD where sensitivity to a change in duration was greatest. Using population data, we demonstrate that a maximum likelihood estimator (MLE) can accurately decode stimulus duration from evoked spike counts. We also simulated a two-alternative forced choice task by having MLE models decide whether two durations were the same or different. With this task we measured the just-noticeable difference threshold for stimulus duration and calculated the corresponding Weber fractions across the stimulus domain. Altogether, these results demonstrate that the spiking responses of DTNs from the mammalian IC contain sufficient information for the CNS to encode, decode, and discriminate behaviorally relevant auditory signal durations. big brown bat; Eptesicus fuscus; Fisher information, inferior colliculus; just-noticeable difference; stimulus-specific information, temporal processing; Weber fraction DURATION-TUNED NEURONS (DTNs) are ideal candidates for encoding spectral, intensity, and temporal information about an auditory stimulus because they respond selectively to the frequency, amplitude, and duration of acoustic signals. First reported in the torus semicircularis of frogs and subsequently the inferior colliculus (IC) of bats, DTNs have now been recorded from the auditory midbrain, thalamus, and cortex in a variety of vertebrates, and from the mammalian visual cortex (see Sayegh et al. 2011, for review). To date, the electrophysiological properties and underlying synaptic inputs responsible for creating the temporally selective responses of DTNs have been a major research focus, but a quantitative analysis of the information content and encoding efficiency of any neural system is important for linking neurophysiology to behavior and perception because it can suggest limits on the efficacy of information representation. Information theoretic measurements have previously been used to characterize the spiking responses of visual (Strong et al. 1998;Tolhurst et al. 2009 Sensory neurons in general, and auditory neurons in particular, are often viewed as feature detectors that have a preferred value in stimulus domains such as frequency or amplitude, and they encode the domain with spike counts (or rates) and latencies that vary as a function of the stimulus. We measured spike counts and latencies from auditory DTNs in the mammalian IC to characterize the information content of duration-selective ne...

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Neural Coding of Signal Duration and Complex Acoustic Objects

Faure

Firzlaff

2016

Bat Bioacoustics

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Duration tuning in the auditory midbrain of echolocating and non-echolocating vertebrates

Cited by 44 publications

References 96 publications

Duration Tuning across Vertebrates

Duration Tuning across Vertebrates

Decoding stimulus duration from neural responses in the auditory midbrain

Neural Coding of Signal Duration and Complex Acoustic Objects

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