Spectral summation and facilitation in on‐ and off‐responses for optimized representation of communication calls in mouse inferior colliculus

Akimov, A. G.; Егорова, М. А.; Ehret, Günter

doi:10.1111/ejn.13488

Cited by 24 publications

(49 citation statements)

References 74 publications

(131 reference statements)

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“…One difference may arise from different injection areas within the shell. Considerable ascending inputs were observed when the HRP injection covered both the ICC and ICX (Aitkin et al, 1981). However, a portion of the injection area assigned to the ICC in the above study was actually the ventrolateral nucleus in the cat, which corresponds to layer 3 of the ICX in the rat (Loftus et al, 2008).…”

Section: Dominant Ascending Pathway In the Ic Shellmentioning

confidence: 85%

Neuronal Organization in the Inferior Colliculus Revisited with Cell-Type-Dependent Monosynaptic Tracing

et al. 2018

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The inferior colliculus (IC) is a critical integration center in the auditory pathway. However, because the inputs to the IC have typically been studied by the use of conventional anterograde and retrograde tracers, the neuronal organization and cell-type-specific connections in the IC are poorly understood. Here, we used monosynaptic rabies tracing and hybridization combined with excitatory and inhibitory Cre transgenic mouse lines of both sexes to characterize the brainwide and cell-type-specific inputs to specific neuron types within the lemniscal IC core and nonlemniscal IC shell. We observed that both excitatory and inhibitory neurons of the IC shell predominantly received ascending inputs rather than descending or core inputs. Correlation and clustering analyses revealed two groups of excitatory neurons in the shell: one received inputs from a combination of ascending nuclei, and the other received inputs from a combination of descending nuclei, neuromodulatory nuclei, and the contralateral IC. In contrast, inhibitory neurons in the core received inputs from the same combination of all nuclei. After normalizing the extrinsic inputs, we found that core inhibitory neurons received a higher proportion of inhibitory inputs from the ventral nucleus of the lateral lemniscus than excitatory neurons. Furthermore, the inhibitory neurons preferentially received inhibitory inputs from the contralateral IC shell. Because IC inhibitory neurons innervate the thalamus and contralateral IC, the inhibitory inputs we uncovered here suggest two long-range disinhibitory circuits. In summary, we found: (1) dominant ascending inputs to the shell, (2) two subpopulations of shell excitatory neurons, and (3) two disinhibitory circuits. Sound undergoes extensive processing in the brainstem. The inferior colliculus (IC) core is classically viewed as the integration center for ascending auditory information, whereas the IC shell integrates descending feedback information. Here, we demonstrate that ascending inputs predominated in the IC shell but appeared to be separated from the descending inputs. The presence of inhibitory projection neurons is a unique feature of the auditory ascending pathways, but the connections of these neurons are poorly understood. Interestingly, we also found that inhibitory neurons in the IC core and shell preferentially received inhibitory inputs from ascending nuclei and contralateral IC, respectively. Therefore, our results suggest a bipartite domain in the IC shell and disinhibitory circuits in the IC.

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Section: Dominant Ascending Pathway In the Ic Shellmentioning

confidence: 85%

Neuronal Organization in the Inferior Colliculus Revisited with Cell-Type-Dependent Monosynaptic Tracing

et al. 2018

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“…Inhibition from SPON may also contribute to facilitation of IC responses to harmonically related frequencies (Akimov et al, 2017), which is a mechanism that presumably enhances the perception of natural mouse calls (Ehret and Riecke, 2002). Strong inhibition from the SPON and VNLL that marks the onset of a broadband natural sound via octopus cell activation could deactivate local interneurons, providing inhibitory side fields to IC neurons and, thereby, achieve spectral facilitation within the same neural critical band (Ehret and Merzenich, 1988; Schreiner and Langner, 1997; Akimov et al, 2017). Simultaneously, slightly temporally dispersed inhibition from SPON and VNLL may sharpen the time window of integration of the spectral peaks (Nayagam et al, 2006; Mayko et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus

Felix

Gourévitch

Gómez-Álvarez

et al. 2017

Front. Neural Circuits

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Auditory streaming enables perception and interpretation of complex acoustic environments that contain competing sound sources. At early stages of central processing, sounds are segregated into separate streams representing attributes that later merge into acoustic objects. Streaming of temporal cues is critical for perceiving vocal communication, such as human speech, but our understanding of circuits that underlie this process is lacking, particularly at subcortical levels. The superior paraolivary nucleus (SPON), a prominent group of inhibitory neurons in the mammalian brainstem, has been implicated in processing temporal information needed for the segmentation of ongoing complex sounds into discrete events. The SPON requires temporally precise and robust excitatory input(s) to convey information about the steep rise in sound amplitude that marks the onset of voiced sound elements. Unfortunately, the sources of excitation to the SPON and the impact of these inputs on the behavior of SPON neurons have yet to be resolved. Using anatomical tract tracing and immunohistochemistry, we identified octopus cells in the contralateral cochlear nucleus (CN) as the primary source of excitatory input to the SPON. Cluster analysis of miniature excitatory events also indicated that the majority of SPON neurons receive one type of excitatory input. Precise octopus cell-driven onset spiking coupled with transient offset spiking make SPON responses well-suited to signal transitions in sound energy contained in vocalizations. Targets of octopus cell projections, including the SPON, are strongly implicated in the processing of temporal sound features, which suggests a common pathway that conveys information critical for perception of complex natural sounds.

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“…Higher thresholds for between-channel than within-channel gap detection suggest that the mechanisms of temporal correlation across sound frequencies differ from those of discontinuity detection. Studies in both humans and mice have already indicated that sound offsets play an important role in temporal correlation across sound frequencies [36][37][38]. Thus sound-offset responses seem likely to be crucial for between-channel gap detection.…”

Section: Perceptual Roles Of Sound Offsetsmentioning

confidence: 99%

When Sound Stops: Offset Responses in the Auditory System

Kopp‐Scheinpflug

Sinclair

Linden

2018

Trends in Neurosciences

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The auditory modality is fundamentally a temporal sense, requiring analysis of changes in sound signals on timescales ranging from microseconds to minutes. To generate a faithful representation of changes in sound intensity and frequency over time, sound offsets (disappearances) as well as sound onsets (appearances) must be encoded by the auditory system. Here we review the computational significance, perceptual roles, anatomical locations, and cellular and network origins of sound-offset responses in the mammalian auditory brain. We show that sound-offset responses arise from mechanisms and pathways distinct from those producing sound-onset responses, and are likely to be essential for auditory processing of temporally discontinuous sounds such as speech. 1 Sound-Offset Responses in the Auditory System Mechanoelectrical transduction mechanisms in the ear encode transient changes in sound pressure with sub-millisecond precision. The auditory nerve then provides to the brain a high-fidelity representation of sound frequency, intensity, and timing, usually including sharp increases in nerve activity following sound onsets and decreases following sound offsets [1]. Many neurons in the auditory brain also represent sound onsets and offsets in this way; however, others produce bursts of activity following sound offsets (e.g., [2]), or following both onsets and offsets (e.g., [3]). Historically, most studies of the central auditory system have ignored sound-offset responses, or dismissed them on neurobiological, acoustical, or perceptual grounds. Neurobiologically, sound-onset responses are much more prevalent in the auditory system than sound-offset responses [4], especially in anaesthetized animals [5], in which the majority of in vivo studies have been performed. Acoustically, offsets of natural sounds tend to be less abrupt than onsets [6], and sound offsets are often obscured by reverberation, especially in enclosed environments. Lastly, perceptually, sound offsets are less salient than sound onsets [4,7,8].

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Spectral summation and facilitation in on‐ and off‐responses for optimized representation of communication calls in mouse inferior colliculus

Cited by 24 publications

References 74 publications

Neuronal Organization in the Inferior Colliculus Revisited with Cell-Type-Dependent Monosynaptic Tracing

Neuronal Organization in the Inferior Colliculus Revisited with Cell-Type-Dependent Monosynaptic Tracing

Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus

When Sound Stops: Offset Responses in the Auditory System

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