Temporal Features of Spectral Integration in the Inferior Colliculus: Effects of Stimulus Duration and Rise Time

Gans, Donald; Sheykholeslami, Kianoush; Peterson, Diana C.; Wenstrup, Jeffrey J.

doi:10.1152/jn.91300.2008

Cited by 11 publications

(17 citation statements)

References 68 publications

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“…In the mustached bat, however, the combination-sensitive inhibition displayed by INLL neurons is closely linked to similar responses in IC neurons (Portfors and Wenstrup, 1999; Nataraj and Wenstrup, 2005, 2006; Gans et al, 2009; Peterson et al, 2009). There is strong evidence that the inhibitory interaction does not originate in the IC (Nataraj and Wenstrup, 2005, 2006; Peterson et al, 2008).…”

Section: Discussionmentioning

confidence: 96%

Substrates of auditory frequency integration in a nucleus of the lateral lemniscus

2010

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In the intermediate nucleus of the lateral lemniscus (INLL), some neurons display a form of spectral integration in which excitatory responses to sounds at their best frequency are inhibited by sounds within a frequency band at least one octave lower. Previous work showed that this response property depends on low-frequency-tuned glycinergic input. To identify all sources of inputs to these INLL neurons, and in particular the low-frequency glycinergic input, we combined retrograde tracing with immunohistochemistry for the neurotransmitter glycine. We deposited a retrograde tracer at recording sites displaying either high best frequencies (>75 kHz) in conjunction with combination-sensitive inhibition, or at sites displaying low best frequencies (23)(24)(25)(26)(27)(28)(29)(30). Most retrogradely labeled cells were located in the ipsilateral medial nucleus of the trapezoid body (MNTB) and contralateral anteroventral cochlear nucleus. Consistent labeling, but in fewer numbers, was observed in the ipsilateral lateral nucleus of the trapezoid body (LNTB), contralateral posteroventral cochlear nucleus, and a few other brainstem nuclei. When tracer deposits were combined with glycine immunohistochemistry, most double-labeled cells were observed in the ipsilateral MNTB (84%), with fewer in LNTB (13%). After tracer deposits at combination-sensitive recording sites, a striking result was that MNTB labeling occurred in both medial and lateral regions. This labeling appeared to overlap the MNTB labeling that resulted from tracer deposits in low-frequency recording sites of INLL. These findings suggest that MNTB is the most likely source of low-frequency glycinergic input to INLL neurons with high best frequencies and combination-sensitive inhibition. This work establishes an anatomical basis for frequency integration in the auditory brainstem. Keywords combination sensitivity; spectral integration; glycine; mustached bat; INLL; Pteronotus parnelliiAlthough the initial stages of the auditory system create and maintain a spectral decomposition of sounds, acoustically guided behavior and perception are based on integration of information across spectral elements. Whether the task is localization of sounds (Hebrank and Wright, 1974, Knudsen andKonishi 1979;Middlebrooks, 1992;Populin and Yin, 1998), the analysis of sonar echoes (Simmons et al., 2004; Genzel and © 2010 IBRO. Published by Elsevier Ltd. All rights reserved.Corresponding author: Jeffrey Wenstrup, Ph.D., Department of Anatomy and Neurobiology, Northeastern Ohio Universities Colleges of Medicine and Pharmacy, 4209 State Route 44, PO Box 95, Rootstown, Ohio 44272, Telephone: (330) Fax: (330) 325-5916, jjw@neoucom.edu. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please n...

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Section: Discussionmentioning

confidence: 96%

Substrates of auditory frequency integration in a nucleus of the lateral lemniscus

2010

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“…General methods used for acoustic stimulation and physiological recording were described previously (Gans et al 2009). Physiological experiments were conducted in a single-walled acoustic chamber.…”

Section: Acoustic Stimulation and Physiological Recordingmentioning

confidence: 99%

A novel coding mechanism for social vocalizations in the lateral amygdala

Gadziola

Grimsley

Shanbhag

et al. 2012

Journal of Neurophysiology

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The amygdala plays a central role in evaluating the significance of acoustic signals and coordinating the appropriate behavioral responses. To understand how amygdalar responses modulate auditory processing and drive emotional expression, we assessed how neurons respond to and encode information that is carried within complex acoustic stimuli. We characterized responses of single neurons in the lateral nucleus of the amygdala to social vocalizations and synthetic acoustic stimuli in awake big brown bats. Neurons typically responded to most of the social vocalizations presented (mean = nine of 11 vocalizations) but differentially modulated both firing rate and response duration. Surprisingly, response duration provided substantially more information about vocalizations than did spike rate. In most neurons, variation in response duration depended, in part, on persistent excitatory discharge that extended beyond stimulus duration. Information in persistent firing duration was significantly greater than in spike rate, and the majority of neurons displayed more information in persistent firing, which was more likely to be observed in response to aggressive vocalizations (64%) than appeasement vocalizations (25%), suggesting that persistent firing may relate to the behavioral context of vocalizations. These findings suggest that the amygdala uses a novel coding strategy for discriminating among vocalizations and underscore the importance of persistent firing in the general functioning of the amygdala.

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“…For example, the <23 kHz suppressive interactions almost always extend for the duration of the suppressing signal, rather than for a brief period following signal onset (Gans et al, 2009). Further, when the <23 kHz signal evokes an excitatory response, this response suppresses spiking responses to the high-frequency signal.…”

Section: Combination-sensitive Response Properties In the Inferior Comentioning

confidence: 99%

Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus

Wenstrup¹,

Nataraj²,

Sanchez³

2012

Front. Neural Circuits

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This review describes mechanisms and circuitry underlying combination-sensitive response properties in the auditory brainstem and midbrain. Combination-sensitive neurons, performing a type of auditory spectro-temporal integration, respond to specific, properly timed combinations of spectral elements in vocal signals and other acoustic stimuli. While these neurons are known to occur in the auditory forebrain of many vertebrate species, the work described here establishes their origin in the auditory brainstem and midbrain. Focusing on the mustached bat, we review several major findings: (1) Combination-sensitive responses involve facilitatory interactions, inhibitory interactions, or both when activated by distinct spectral elements in complex sounds. (2) Combination-sensitive responses are created in distinct stages: inhibition arises mainly in lateral lemniscal nuclei of the auditory brainstem, while facilitation arises in the inferior colliculus (IC) of the midbrain. (3) Spectral integration underlying combination-sensitive responses requires a low-frequency input tuned well below a neuron's characteristic frequency (ChF). Low-ChF neurons in the auditory brainstem project to high-ChF regions in brainstem or IC to create combination sensitivity. (4) At their sites of origin, both facilitatory and inhibitory combination-sensitive interactions depend on glycinergic inputs and are eliminated by glycine receptor blockade. Surprisingly, facilitatory interactions in IC depend almost exclusively on glycinergic inputs and are largely independent of glutamatergic and GABAergic inputs. (5) The medial nucleus of the trapezoid body (MNTB), the lateral lemniscal nuclei, and the IC play critical roles in creating combination-sensitive responses. We propose that these mechanisms, based on work in the mustached bat, apply to a broad range of mammals and other vertebrates that depend on temporally sensitive integration of information across the audible spectrum.

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Temporal Features of Spectral Integration in the Inferior Colliculus: Effects of Stimulus Duration and Rise Time

Cited by 11 publications

References 68 publications

Substrates of auditory frequency integration in a nucleus of the lateral lemniscus

Substrates of auditory frequency integration in a nucleus of the lateral lemniscus

A novel coding mechanism for social vocalizations in the lateral amygdala

Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus

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