Patterns of Unilateral and Bilateral Projections From Layers 5 and 6 of the Auditory Cortex to the Inferior Colliculus in Mouse

The auditory cortex sends massive projections to the inferior colliculus, but the organization of this pathway is not yet well understood. Previous work has shown that the corticocollicular projection emanates from both layers 5 and 6 of the auditory cortex and that neurons in these layers have different morphological and physiological properties. It is not yet known in the mouse if both layer 5 and layer 6 project bilaterally, nor is it known if the projection patterns differ based on projection location. Using targeted injections of Fluorogold into either the lateral cortex or dorsal cortex of the inferior colliculus, we quantified retrogradely labeled neurons in both the left and right lemniscal regions of the auditory cortex, as delineated using parvalbumin immunostaining. After dorsal cortex injections, we observed that approximately 18–20% of labeled cells were in layer 6 and that this proportion was similar bilaterally. After lateral cortex injections, only ipsilateral cells were observed in the auditory cortex, and they were found in both layer 5 and layer 6. The ratio of layer 5:layer 6 cells after lateral cortex injection was similar to that seen after dorsal cortex injection. Finally, injections of different tracers were made into the two inferior colliculi, and an average of 15–17% of cells in the auditory cortex were double-labeled, and these proportions were similar in layers 5 and 6. These data suggest that (1) only the dorsal cortex of the inferior colliculus receives bilateral projections from the auditory cortex, (2) both the dorsal and lateral cortex of the inferior colliculus receive similar layer 5 and layer 6 auditory cortical input, and (3) a subpopulation of individual neurons in both layers 5 and 6 branch to innervate both dorsal cortices of the inferior colliculus.

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Iba1+ Microglia Exhibit Morphological Differences between Inferior Colliculus Sub-Regions and Their Abutments onto GAD67+ Somata Reveal Two Novel Sub-types of GABAergic Neuron

10.1101/606509 ◽

2019 ◽

Author(s):

Samuel David Webb ◽

Llwyd David Orton

Keyword(s):

Nervous System ◽

Auditory Processing ◽

Central Nucleus ◽

Significant Heterogeneity ◽

Dorsal Cortex ◽

Lateral Cortex ◽

Glia Limitans ◽

Morphological Differences ◽

Inferior Colliculi ◽

The Brain

AbstractMicroglia have classically been viewed as the endogenous phagocytes of the brain, however, emerging evidence suggests roles for microglia in the healthy, mature nervous system. We know little of the contribution microglia make to ongoing processing in sensory systems. To explore Iba1+ microglial diversity, we employed the inferior colliculi (IC) as model nuclei, as they are characterized by sub-regions specialized for differing aspects of auditory processing. We conducted fluorescent multi-channel immunohistochemistry and confocal microscopy in guinea pigs of both sexes and discovered that the density and morphology of Iba1+ labelling varied between parenchymal sub-regions of IC, while GFAP+ labelling of astrocytes was confined to the glia limitans externa and peri-vascular regions. The density of Iba1+ microglia somata was similar across sub-regions, however a greater amount of labelling was found in dorsal cortex than ventral central nucleus or lateral cortex. To further understand these differences between sub-regions in IC, Sholl and skeleton analyses of individual microglia revealed a greater number of branching ramifications in dorsal cortex. We also quantified abutments of Iba1+ microglial processes onto GAD67+ (putative GABAergic) somata. Cluster analyses revealed two novel sub-types of GAD67+ neuron, which can be distinguished solely based on the quantity of axo-somatic Iba1+ abutments they receive. These data demonstrate Iba1+ microglia exhibit different morphologies and interactions with GAD67+ neurons in distinct sub-regions of the mature, healthy IC. Taken together, these findings suggest significant heterogeneity amongst microglia in the auditory system, possibly related to the ongoing functional demands of their niche.

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Unifying the Midbrain

The Oxford Handbook of the Auditory Brainstem ◽

10.1093/oxfordhb/9780190849061.013.21 ◽

2018 ◽

pp. 548-576

Author(s):

Adrian Rees ◽

Llwyd D. Orton

Keyword(s):

Inferior Colliculus ◽

Auditory Processing ◽

Auditory Pathway ◽

Neural Representation ◽

Central Nucleus ◽

Dorsal Cortex ◽

Auditory Midbrain ◽

Inferior Colliculi ◽

Behavioral Influences

Commissural fibres interconnecting the two sides of the brain are found at several points along the auditory pathway, thus suggesting their fundamental importance for the analysis of sound. This chapter presents an overview of what is currently known about the anatomy, physiology, and behavioral influences of the commissure of the inferior colliculus (CoIC)—the most prominent brainstem auditory commissure—that reciprocally interconnects the principal nuclei of the auditory midbrain, the inferior colliculi (IC). The primary contribution to the CoIC originates from neurons projecting from one inferior colliculus to the other, with the dorsal cortex and central nucleus providing the most extensive connections. In addition, many ascending and descending auditory centers send projections to the IC via the CoIC, together with diverse sources located outside the classically defined auditory pathway. The degree of interconnection between the two ICs suggests they function as a single entity. Recent in vivo evidence has established that CoIC projections modulate the neural representation of sound frequency, level, and location in the IC, thus indicating an important role for the CoIC in auditory processing. However, there is limited evidence for the influence of the CoIC on auditory behavior. This, together with the diversity of sources projecting via the CoIC, suggest unknown roles that warrant further exploration.

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The Inferior Colliculus in Alcoholism and Beyond

Frontiers in Systems Neuroscience ◽

10.3389/fnsys.2020.606345 ◽

2020 ◽

Vol 14 ◽

Author(s):

Tanuja Bordia ◽

Natalie M. Zahr

Keyword(s):

Inferior Colliculus ◽

Ethanol Exposure ◽

Ethanol Withdrawal ◽

Hypoxic Injury ◽

Auditory Gating ◽

Korsakoff Syndrome ◽

Altered Metabolism ◽

Magnetic Resonance Imaging Mri ◽

Inferior Colliculi

Post-mortem neuropathological and in vivo neuroimaging methods have demonstrated the vulnerability of the inferior colliculus to the sequelae of thiamine deficiency as occurs in Wernicke-Korsakoff Syndrome (WKS). A rich literature in animal models ranging from mice to monkeys—including our neuroimaging studies in rats—has shown involvement of the inferior colliculi in the neural response to thiamine depletion, frequently accomplished with pyrithiamine, an inhibitor of thiamine metabolism. In uncomplicated alcoholism (i.e., absent diagnosable neurological concomitants), the literature citing involvement of the inferior colliculus is scarce, has nearly all been accomplished in preclinical models, and is predominately discussed in the context of ethanol withdrawal. Our recent work using novel, voxel-based analysis of structural Magnetic Resonance Imaging (MRI) has demonstrated significant, persistent shrinkage of the inferior colliculus using acute and chronic ethanol exposure paradigms in two strains of rats. We speculate that these consistent findings should be considered from the perspective of the inferior colliculi having a relatively high CNS metabolic rate. As such, they are especially vulnerable to hypoxic injury and may be provide a common anatomical link among a variety of disparate insults. An argument will be made that the inferior colliculi have functions, possibly related to auditory gating, necessary for awareness of the external environment. Multimodal imaging including diffusion methods to provide more accurate in vivo visualization and quantification of the inferior colliculi may clarify the roles of brain stem nuclei such as the inferior colliculi in alcoholism and other neuropathologies marked by altered metabolism.

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Phase-Locked Responses to Pure Tones in the Inferior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.00497.2005 ◽

2006 ◽

Vol 95 (3) ◽

pp. 1926-1935 ◽

Cited By ~ 70

Author(s):

Liang-Fa Liu ◽

Alan R. Palmer ◽

Mark N. Wallace

Keyword(s):

Guinea Pig ◽

Inferior Colliculus ◽

Phase Locking ◽

Single Units ◽

Central Nucleus ◽

Dorsal Cortex ◽

Upper Limits ◽

Ascending Pathways ◽

Pure Tones ◽

The Brain

In the auditory system, some ascending pathways preserve the precise timing information present in a temporal code of frequency. This can be measured by studying responses that are phase-locked to the stimulus waveform. At each stage along a pathway, there is a reduction in the upper frequency limit of the phase-locking and an increase in the steady-state latency. In the guinea pig, phase-locked responses to pure tones have been described at various levels from auditory nerve to neocortex but not in the inferior colliculus (IC). Therefore we made recordings from 161 single units in guinea pig IC. Of these single units, 68% (110/161) showed phase-locked responses. Cells that phase-locked were mainly located in the central nucleus but also occurred in the dorsal cortex and external nucleus. The upper limiting frequency of phase-locking varied greatly between units (80−1,034 Hz) and between anatomical divisions. The upper limits in the three divisions were central nucleus, >1,000 Hz; dorsal cortex, 700 Hz; external nucleus, 320 Hz. The mean latencies also varied and were central nucleus, 8.2 ± 2.8 (SD) ms; dorsal cortex, 17.2 ms; external nucleus, 13.3 ms. We conclude that many cells in the central nucleus receive direct inputs from the brain stem, whereas cells in the external and dorsal divisions receive input from other structures that may include the forebrain.

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Transient down-regulation of sound-induced c-Fos protein expression in the inferior colliculus after ablation of the auditory cortex

Frontiers in Neuroanatomy ◽

10.3389/fnana.2010.00141 ◽

2010 ◽

Vol 4 ◽

Cited By ~ 6

Author(s):

Cheryl Clarkson

Keyword(s):

Protein Expression ◽

Auditory Cortex ◽

Inferior Colliculus ◽

Down Regulation ◽

Fos Protein

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Disparity in interaural time difference improves the accuracy of neural representations of individual concurrent narrowband sounds in rat inferior colliculus and auditory cortex

Journal of Neurophysiology ◽

10.1152/jn.00284.2019 ◽

2020 ◽

Vol 123 (2) ◽

pp. 695-706

Author(s):

Lu Luo ◽

Na Xu ◽

Qian Wang ◽

Liang Li

Keyword(s):

Auditory Cortex ◽

Inferior Colliculus ◽

Interaural Time Difference ◽

Critical Role ◽

Low Frequency ◽

Time Difference ◽

Neural Representation ◽

Frequency Bands ◽

Neural Segregation ◽

Peripheral Auditory System

The central mechanisms underlying binaural unmasking for spectrally overlapping concurrent sounds, which are unresolved in the peripheral auditory system, remain largely unknown. In this study, frequency-following responses (FFRs) to two binaurally presented independent narrowband noises (NBNs) with overlapping spectra were recorded simultaneously in the inferior colliculus (IC) and auditory cortex (AC) in anesthetized rats. The results showed that for both IC FFRs and AC FFRs, introducing an interaural time difference (ITD) disparity between the two concurrent NBNs enhanced the representation fidelity, reflected by the increased coherence between the responses evoked by double-NBN stimulation and the responses evoked by single NBNs. The ITD disparity effect varied across frequency bands, being more marked for higher frequency bands in the IC and lower frequency bands in the AC. Moreover, the coherence between IC responses and AC responses was also enhanced by the ITD disparity, and the enhancement was most prominent for low-frequency bands and the IC and the AC on the same side. These results suggest a critical role of the ITD cue in the neural segregation of spectrotemporally overlapping sounds. NEW & NOTEWORTHY When two spectrally overlapped narrowband noises are presented at the same time with the same sound-pressure level, they mask each other. Introducing a disparity in interaural time difference between these two narrowband noises improves the accuracy of the neural representation of individual sounds in both the inferior colliculus and the auditory cortex. The lower frequency signal transformation from the inferior colliculus to the auditory cortex on the same side is also enhanced, showing the effect of binaural unmasking.

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Asymmetric sampling in human auditory cortex reveals spectral processing hierarchy

10.1101/581520 ◽

2019 ◽

Author(s):

Jérémy Giroud ◽

Agnès Trébuchon ◽

Daniele Schön ◽

Patrick Marquis ◽

Catherine Liegeois-Chauvel ◽

...

Keyword(s):

Auditory Cortex ◽

Auditory System ◽

Speech Processing ◽

Auditory Processing ◽

Differential Sensitivity ◽

Processing Mode ◽

Cortical Hierarchy ◽

Processing Modes ◽

Left And Right ◽

Cortical Auditory Processing

AbstractSpeech perception is mediated by both left and right auditory cortices, but with differential sensitivity to specific acoustic information contained in the speech signal. A detailed description of this functional asymmetry is missing, and the underlying models are widely debated. We analyzed cortical responses from 96 epilepsy patients with electrode implantation in left or right primary, secondary, and/or association auditory cortex. We presented short acoustic transients to reveal the stereotyped spectro-spatial oscillatory response profile of the auditory cortical hierarchy. We show remarkably similar bimodal spectral response profiles in left and right primary and secondary regions, with preferred processing modes in the theta (∼4-8 Hz) and low gamma (∼25-50 Hz) ranges. These results highlight that the human auditory system employs a two-timescale processing mode. Beyond these first cortical levels of auditory processing, a hemispheric asymmetry emerged, with delta and beta band (∼3/15 Hz) responsivity prevailing in the right hemisphere and theta and gamma band (∼6/40 Hz) activity in the left. These intracranial data provide a more fine-grained and nuanced characterization of cortical auditory processing in the two hemispheres, shedding light on the neural dynamics that potentially shape auditory and speech processing at different levels of the cortical hierarchy.Author summarySpeech processing is now known to be distributed across the two hemispheres, but the origin and function of lateralization continues to be vigorously debated. The asymmetric sampling in time (AST) hypothesis predicts that (1) the auditory system employs a two-timescales processing mode, (2) present in both hemispheres but with a different ratio of fast and slow timescales, (3) that emerges outside of primary cortical regions. Capitalizing on intracranial data from 96 epileptic patients we sensitively validated each of these predictions and provide a precise estimate of the processing timescales. In particular, we reveal that asymmetric sampling in associative areas is subtended by distinct two-timescales processing modes. Overall, our results shed light on the neurofunctional architecture of cortical auditory processing.

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