Neural Tuning for Sound Duration: Role of Inhibitory Mechanisms in the Inferior Colliculus

Casseday, John H.; Ehrlich, Daphna; Covey, Ellen

doi:10.1126/science.8171341

Cited by 372 publications

(308 citation statements)

References 24 publications

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“…Neurons tuned for the duration of a stimulus have been found in the central auditory systems of a number of vertebrates, including frogs (Potter, 1965;Narins and Capranica, 1980;Hall and Feng, 1986;Gooler and Feng, 1992), mice (Brand et al, 2000), chinchillas (Chen, 1998), cats , and various species of echolocating bats (Jen and Schlegel, 1982;Pinheiro et al, 1991;Casseday et al, 1994;Condon et al, 1996;Galazyuk and Feng, 1997;Fuzessery and Hall, 1999). Neurons tuned to the duration of a stationary bar of light have also been found in areas 17 and 18 of the cat visual cortex (Duysens et al, 1996).…”

Section: Discussionmentioning

confidence: 95%

Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

et al. 2003

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The inferior colliculus (IC) is the first place in the central auditory pathway where duration-selective neurons are found. Previous neuropharmacological and electrophysiological studies have shown that they are created there and have led to a conceptual model in which excitatory and inhibitory inputs are offset in time so that the cell fires only when sound duration is such that onset-and offsetevoked excitation coincide; the response is suppressed by inhibition at other durations. We tested predictions from the model using paired tone stimulation and extracellular recording in the IC of the big brown bat, Eptesicus fuscus. Responses to a best duration (BD) tone were used as a probe to examine the strength and time course of inhibition activated by a nonexcitatory (NE) tone of the same frequency but differing in duration. As the relative time between the BD and NE tones was varied, the activity evoked by the BD tone was affected in ways comparable with backward, simultaneous, and forward masking. Responses to the BD tone were completely suppressed at short interstimulus intervals when the BD tone preceded the NE tone. Suppression was also seen when the stimuli temporally overlapped and summed and at intervals when the BD tone followed the NE tone. The results show that duration-selective neurons receive an onsetevoked, inhibitory input that precedes their excitatory input. The period of leading inhibition was correlated with BD and first spike latency. The results suggest how inhibition in the CNS could explain temporal masking phenomena, including backward masking.

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Section: Discussionmentioning

confidence: 95%

Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

et al. 2003

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“…LG cells are shown to send long‐range projection to thalamus to elicit inhibitory response faster than excitation (Peruzzi, Bartlett, Smith, & Oliver, 1997). The long‐range connection inside the IC may also cause fast inhibition, which is important for coding complex information such as duration (Casseday et al., 1994). To understand the roles of local neurons on the synaptic‐domain‐based information coding, cell‐type specific manipulation of local circuit is required.…”

Section: Discussionmentioning

confidence: 99%

“…Lower brainstem nuclei, namely, cochlear nuclei (CN), SOC, and nuclei of the lateral lemniscus (NLL), analyze specific features of sound and send the analyzed information to the inferior colliculus (IC), which is the largest nuclei in entire subcortical auditory system (Ito, Bishop, & Oliver, 2016). Since all the sound information is converged, the IC is considered to integrate sound information and create coding of complex sound information: In bats, analyses related to echolocation such as tunings of sound duration (Casseday, Ehrlich, & Covey, 1994), and delay coding (Portfors & Wenstrup, 1999) are found in the IC.…”

Section: Introductionmentioning

confidence: 99%

Organization of projection from brainstem auditory nuclei to the inferior colliculus of Japanese house bat (Pipistrellus abramus)

et al. 2018

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ObjectivesEcholocating bats show remarkable specialization which is related to analysis of echoes of biosonars in subcortical auditory brainstem pathways. The inferior colliculus (IC) receives inputs from all lower brainstem auditory nuclei, i.e., cochlear nuclei, nuclei of the lateral lemniscus, and superior olivary complex, and create de novo responses to sound, which is considered crucial for echolocation. Inside the central nucleus of the IC (ICC), small domains which receive specific combination of extrinsic inputs are the basis of integration of sound information. In addition to extrinsic inputs, each domain is interconnected by local IC neurons but the cell types related to the interconnection are not well‐understood. The primary objective of the current study is to examine whether the ascending inputs are reorganized and terminate in microdomains inside the ICC.MethodsWe made injection of a retrograde tracer into different parts of the ICC, and analyzed distribution of retrogradely labeled cells in the auditory brainstem of Japanese house bat (Pipistrellus abramus).ResultsPattern of ascending projections from brainstem nuclei was similar to other bat species. Percentages of labeled cells in several nuclei were correlated each other. Furthermore, within the IC, we identified that large GABAergic (LG) and glutamatergic neurons made long‐range connection.ConclusionsSynaptic organization of IC of Japanese house bat shows specialization which is likely to relate for echolocation. Input nuclei to the IC make clusters which terminate in specific part of the ICC, implying the presence of microdomains. LG neurons have roles for binding IC microdomains.

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“…It has been proposed that duration-selective neurons are present in early sensory areas for both auditory and visual information (Heron et al, 2012). Evidence for this claim comes from single cell recording studies in different mammals that have reported duration-selective neurons in both early auditory processing areas such as inferior colliculus and the auditory midbrain (Brand, Urban, & Grothe, 2000;Casseday, Ehrlich, & Covey, 1994;Ehrlich, Casseday, & Covey, 1997;He, Hashikawa, Ojima, & Kinouchi, 1997), as well as early visual areas such as area 17 & 18 (Duysens, Schaafsma, & Orban, 1996;Eriksson, Tompa, & Roland, 2008). One can argue that an early locus for duration processing can be beneficial given that the temporal integration window of neurons is known to increase along the visual processing hierarchy (Hasson, Yang, Vallines, Heeger, & Rubin, 2008).…”

Section: Introductionmentioning

confidence: 98%

An investigation of the spatial selectivity of the duration after-effect

et al. 2017

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a b s t r a c tAdaptation to the duration of a visual stimulus causes the perceived duration of a subsequently presented stimulus with a slightly different duration to be skewed away from the adapted duration. This pattern of repulsion following adaptation is similar to that observed for other visual properties, such as orientation, and is considered evidence for the involvement of duration-selective mechanisms in duration encoding. Here, we investigated whether the encoding of duration -by duration-selective mechanisms -occurs early on in the visual processing hierarchy. To this end, we investigated the spatial specificity of the duration after-effect in two experiments. We measured the duration after-effect at adapter-test distances ranging between 0 and 15°of visual angle and for within-and between-hemifield presentations. We replicated the duration after-effect: the test stimulus was perceived to have a longer duration following adaptation to a shorter duration, and a shorter duration following adaptation to a longer duration. Importantly, this duration after-effect occurred at all measured distances, with no evidence for a decrease in the magnitude of the after-effect at larger distances or across hemifields. This shows that adaptation to duration does not result from adaptation occurring early on in the visual processing hierarchy. Instead, it seems likely that duration information is a high-level stimulus property that is encoded later on in the visual processing hierarchy.

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Neural Tuning for Sound Duration: Role of Inhibitory Mechanisms in the Inferior Colliculus

Cited by 372 publications

References 24 publications

Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

Temporal Masking Reveals Properties of Sound-Evoked Inhibition in Duration-Tuned Neurons of the Inferior Colliculus

Organization of projection from brainstem auditory nuclei to the inferior colliculus of Japanese house bat (Pipistrellus abramus)

An investigation of the spatial selectivity of the duration after-effect

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