Cooling of the auditory cortex modifies neuronal activity in the inferior colliculus in rats

Popelář, Jiří; Šuta, Daniel; Lindovský, Jiří; Bureš, Zbyněk; Pysanenko, Kateryna; Chumak, Tetyana; Syka, Josef

doi:10.1016/j.heares.2015.10.021

Cited by 23 publications

(16 citation statements)

References 44 publications

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“…The current data, combined with previous findings of a combined excitatory/inhibitory set of projections from the IC to the MGB (Winer et al, ; Peruzzi et al, ; Venkataraman and Bartlett, ; Llano et al, ), and known inputs from the IC to the nucleus of the BIC (Kudo and Niimi, ) suggest that the IC and the nucleus of the BIC contain reciprocal mixed excitatory and inhibitory inputs. Given the strong projection from the AC to the nucleus of the BIC (Andersen et al, ; Saldaña et al, ; Mellott et al, ), and the finding that inactivation of the AC leads to disinhibition of some IC neurons (Jen et al, ; Anderson and Malmierca, ; Popeláø et al, ), the presence of an inhibitory projection from the BIC to the IC suggests that long‐range corticocollicular inhibition may be mediated via GABAergic neurons in the BIC. The significance of the relative absence of GABAergic projections from the PP compared to BIC is not yet clear.…”

Section: Discussionmentioning

confidence: 99%

Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse

Patel

Sons

Yudintsev

et al. 2016

J of Comparative Neurology

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Descending projections from the thalamus and related structures to the midbrain are evolutionarily highly conserved. However, the basic organization of this auditory thalamotectal pathway has not yet been characterized. The purpose of this study is to obtain a better understanding of the anatomical and neurochemical features of this pathway. Analysis of the distributions of retrogradely labeled cells after focal injections of retrograde tracer into the inferior colliculus of the mouse revealed that most of the subcortical descending projections originated in the brachium of the inferior colliculus and the paralaminar portions of the auditory thalamus. In addition, the vast majority of thalamotectal cells were found to be negative for the calcium-binding proteins calbindin, parvalbumin or calretinin. Using two different strains of GAD-GFP mice, as well as immunostaining for GABA, we found that a subset of neurons in the brachium of the inferior colliculus is GABAergic, suggesting that part of this descending pathway is inhibitory. Finally, dual retrograde injections into the inferior colliculus and amygdala plus corpus striatum as well into the inferior colliculus and auditory cortex did not reveal any double labeling. These data suggest that the thalamocollicular pathway comprises a unique population of thalamic neurons that do not contain typical calcium binding proteins and do not project to other paralaminar thalamic forebrain targets, and that a previously undescribed descending GABAergic pathway emanates from the brachium of the inferior colliculus.

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Section: Discussionmentioning

confidence: 99%

Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse

Patel

Sons

Yudintsev

et al. 2016

J of Comparative Neurology

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“…Existing methodologies to study corticofugal functions, including our previous study, have limitations. Specifically, most studies have employed non-specific cortical modulation, such as electrical stimulation 26 – 29 or chemical/cryogenic deactivation 30 – 32 . These cortical manipulations affect all cortical neuron types in the stimulation region, even though descending projections arise primarily from pyramidal neurons 17 , 18 .…”

Section: Introductionmentioning

confidence: 99%

Optogenetic auditory fMRI reveals the effects of visual cortical inputs on auditory midbrain response

Leong

Dong

Gao

et al. 2018

Sci Rep

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Sensory cortices contain extensive descending (corticofugal) pathways, yet their impact on brainstem processing – particularly across sensory systems – remains poorly understood. In the auditory system, the inferior colliculus (IC) in the midbrain receives cross-modal inputs from the visual cortex (VC). However, the influences from VC on auditory midbrain processing are unclear. To investigate whether and how visual cortical inputs affect IC auditory responses, the present study combines auditory blood-oxygenation-level-dependent (BOLD) functional MRI (fMRI) with cell-type specific optogenetic manipulation of visual cortex. The results show that predominant optogenetic excitation of the excitatory pyramidal neurons in the infragranular layers of the primary VC enhances the noise-evoked BOLD fMRI responses within the IC. This finding reveals that inputs from VC influence and facilitate basic sound processing in the auditory midbrain. Such combined optogenetic and auditory fMRI approach can shed light on the large-scale modulatory effects of corticofugal pathways and guide detailed electrophysiological studies in the future.

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“…Inactivation studies have shown mixed effects on sound-evoked responses in IC, but consistently demonstrated no effect on frequency selectivity. Specifically, suppression of AC increased or decreased IC sound responses in distinct subsets of cells (Popelář et al, 2003(Popelář et al, , 2016 while suppression of direct cortico-collicular feedback terminals in IC decreased sound-evoked responses (Xiong et al, 2015). However, our results show that suppression of direct cortico-collicular feedback has inconsistent effects on frequency selectivity and no effect on any other sound response properties in IC.…”

Section: Discussionmentioning

confidence: 46%

“…AC inactivation studies, on the other hand, found less consistent effects on IC responses. Whereas pharmacological inactivation of AC caused a shift in best frequency in IC neurons (Zhang et al, 1997), several studies show inactivation of AC had no effect on frequency selectivity in IC (Jen et al, 1998), but rather modulated soundevoked and spontaneous activity (Gao and Suga, 1998;Popelář et al, 2003Popelář et al, , 2016. Cortico-collicular feedback is critical to auditory learning, specifically learning to adapt to a unilateral earplug during sound localization (Bajo et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Auditory cortex shapes sound responses in the inferior colliculus

Blackwell

Lesicko

Rao

et al. 2019

Preprint

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The extensive feedback from the auditory cortex (AC) to the inferior colliculus (IC) supports critical aspects of auditory learning, but has not been extensively characterized. Furthermore, it remains unknown whether and how intra-cortical processing of auditory information propagates to earlier stages in the auditory pathway. Previous studies demonstrated that responses of neurons in IC are altered by focal electrical stimulation and pharmacological inactivation of auditory cortex, but these methods lack the ability to selectively manipulate the activity of projection neurons. Combining viral technology with electrophysiological recordings, we measured the effects of selective optogenetic activation or suppression of cortico-collicular feedback projections on IC responses to sounds. Activation of cortico-collicular feedback generally increased spontaneous activity and decreased stimulus selectivity in IC, whereas suppression of the feedback did not affect collicular activity. To further understand how microcircuits in the auditory cortex may control collicular activity, we tested the effects of optogenetically modulating different cortical neuronal subtypes, specifically parvalbumin-positive (PV) and somatostatin-positive (SOM) inhibitory interneurons. We found that, despite strong effects on sound-evoked responses across the layers of AC, activating either type of interneuron did not affect IC sound-evoked activity. However, suppression of SOMs, but not PVs, weakly increased spontaneous activity in IC. These findings suggest that shaping of sound responses mediated by cortical inhibition does not affect sound processing in IC. Combined, our results identify that activation of excitatory projections, but not inhibitory-driven increases in cortical activity, affects collicular sound responses. Significance StatementDescending projections from the auditory cortex to the auditory midbrain, the inferior colliculus, have been shown to play a critical role in auditory learning and behavior. However, little is known about the details of how this direct feedback shapes neuronal responses to sounds in the inferior colliculus. We found that direct activation of cortico-collicular feedback increased spontaneous and modulated sound-evoked activity in the inferior colliculus. Interestingly, modulation of inhibitory interneuron activity, thereby increasing or decreasing excitatory neuronal activity in the auditory cortex, did not affect sound responses in the inferior colliculus. This work offers evidence that auditory cortex shapes sound responses in the inferior colliculus via direct feedback independently of the activity of cortical inhibitory interneurons.

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Cooling of the auditory cortex modifies neuronal activity in the inferior colliculus in rats

Cited by 23 publications

References 44 publications

Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse

Anatomical characterization of subcortical descending projections to the inferior colliculus in mouse

Optogenetic auditory fMRI reveals the effects of visual cortical inputs on auditory midbrain response

Auditory cortex shapes sound responses in the inferior colliculus

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