scholarly journals Unifying the Midbrain

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.

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

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.

Duration Selective Neurons in the Inferior Colliculus of the Rat: Topographic Distribution and Relation of Duration Sensitivity to Other Response Properties

2006 ◽  
Vol 95 (2) ◽  
pp. 823-836 ◽  
Author(s):  
D. Pérez-González ◽  
M. S. Malmierca ◽  
J. M. Moore ◽  
O. Hernández ◽  
E. Covey
Keyword(s):  
Inferior Colliculus ◽  
Excitatory Input ◽  
Central Nucleus ◽  
Response Patterns ◽  
Dorsal Cortex ◽  
Auditory Midbrain ◽  
Duration Threshold ◽  
Band Pass ◽  
Species Specific ◽  
Sound Duration

Many animals use duration to help them identify the source and meaning of a sound. Duration-sensitive neurons have been found in the auditory midbrain of mammals and amphibians, where their selectivity seems to correspond to the lengths of species-specific vocalizations. In this study, single neurons in the rat inferior colliculus (IC) were tested for sensitivity to sound duration. About one-half (54%) of the units sampled showed some form of duration selectivity. The majority of these (76%) were long-pass neurons that responded to sounds exceeding some duration threshold (range: 5–60 ms). Band-pass neurons, which only responded to a restricted range of durations, made up 13% of duration-sensitive neurons (best durations: 15–120 ms). Other units displayed short-pass (2%) or mixed (9%) response patterns. The majority of duration-sensitive neurons were localized outside the central nucleus of the IC, especially in the dorsal cortex, where more than one-half of the neurons sampled had long-pass selectivity for duration. Band-pass duration tuned neurons were only found outside the central nucleus. Characteristics of duration-sensitive neurons in the rat support the idea that this filtering arises through an interaction of excitatory and inhibitory inputs that converge in the IC. Band-pass neurons typically responded at sound offset, suggesting that their tuning is created through the same mechanisms that have been described in echolocating bats. The finding that the first-spike latencies of all long-pass neurons were longer than the shortest duration to which they responded supports the idea that they receive transient inhibition before, or simultaneously with, a sustained excitatory input. The ranges of selectivity in rat IC neurons are within the range of durations of rat vocalizations. These data suggest that a population of neurons in the rat IC have evolved to transmit information about behaviorally relevant sound durations using mechanisms that are common to all mammals, with an emphasis on long-pass tuning characteristics.

scholarly journals The Inferior Colliculus in Alcoholism and Beyond

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.

Phase-Locked Responses to Pure Tones in the Inferior Colliculus

2006 ◽  
Vol 95 (3) ◽  
pp. 1926-1935 ◽  
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.

Neural Transformation of Dissonant Intervals in the Auditory Brainstem

2015 ◽  
Vol 32 (5) ◽  
pp. 445-459 ◽  
Author(s):  
Kyung Myun Lee ◽  
Erika Skoe ◽  
Nina Kraus ◽  
Richard Ashley
Keyword(s):  
Auditory System ◽  
Auditory Processing ◽  
Response Spectrum ◽  
Phase Locking ◽  
Auditory Pathway ◽  
Auditory Brainstem ◽  
Neural Representation ◽  
Auditory Brainstem Responses ◽  
Distortion Products ◽  
Stimulus Waveform

Acoustic periodicity is an important factor for discriminating consonant and dissonant intervals. While previous studies have found that the periodicity of musical intervals is temporally encoded by neural phase locking throughout the auditory system, how the nonlinearities of the auditory pathway influence the encoding of periodicity and how this effect is related to sensory consonance has been underexplored. By measuring human auditory brainstem responses (ABRs) to four diotically presented musical intervals with increasing degrees of dissonance, this study seeks to explicate how the subcortical auditory system transforms the neural representation of acoustic periodicity for consonant versus dissonant intervals. ABRs faithfully reflect neural activity in the brainstem synchronized to the stimulus while also capturing nonlinear aspects of auditory processing. Results show that for the most dissonant interval, which has a less periodic stimulus waveform than the most consonant interval, the aperiodicity of the stimulus is intensified in the subcortical response. The decreased periodicity of dissonant intervals is related to a larger number of nonlinearities (i.e., distortion products) in the response spectrum. Our findings suggest that the auditory system transforms the periodicity of dissonant intervals resulting in consonant and dissonant intervals becoming more distinct in the neural code than if they were to be processed by a linear auditory system.

Inferior colliculus. II. Development of tuning characteristics and tonotopic organization in central nucleus of the neonatal cat

1975 ◽  
Vol 38 (5) ◽  
pp. 1208-1216 ◽  
Author(s):  
L. M. Aitkin ◽  
D. R. Moore
Keyword(s):  
Inferior Colliculus ◽  
Tuning Curve ◽  
External Auditory Meatus ◽  
Auditory Pathway ◽  
Central Nucleus ◽  
Synaptic Density ◽  
Tonotopic Organization ◽  
Tuning Curves ◽  
Sharp Form ◽  
Cochlear Development

Tuning curves were measured for 65 units in the inferior colliculus of seven anesthetized kittens aged from 6 to 28 days. At 2 days of age the inferior colliculus was divisible into central, pericentral, and external nuclei. Evidence was found for broader tuning curves to occur in the pericentral nucleus compared with the central nucleus, as has been observed in the adult. The middle ear was filled with serous fluid to 6 days, while the external auditory meatus remained collapsed until 10 days. Central nucleus tuning curves in kittens were relatively flat with high thresholds. Best-frequency thresholds diminished from a mean of near 100 dB SPL at 6-11 days to near 50 dB in the adult. The marked drop in thresholds between days 22 and 21 led to the adoption of the sharp form of tuning curve common for adults. Tonotopic organization of the central nucleus was clear at day 11. Speculations were advanced about the dependence of central auditory maturations on cochlear development, axon myelination in the auditory pathway, and changes in synaptic density as a function of age.

scholarly journals Serotonin 1B Receptor Modulates Frequency Response Curves and Spectral Integration in the Inferior Colliculus by Reducing GABAergic Inhibition

2008 ◽  
Vol 100 (3) ◽  
pp. 1656-1667 ◽  
Author(s):  
Laura M. Hurley ◽  
Jo Anne Tracy ◽  
Alexander Bohorquez
Keyword(s):  
Frequency Response ◽  
Inferior Colliculus ◽  
Extracellular Recording ◽  
Evoked Responses ◽  
Auditory Midbrain ◽  
Response Curves ◽  
Response Characteristics ◽  
Spectral Integration ◽  
Serotonin 1B Receptor

The selectivity of sensory neurons for stimuli is often shaped by a balance between excitatory and inhibitory inputs, making this balance an effective target for regulation. In the inferior colliculus (IC), an auditory midbrain nucleus, the amplitude and selectivity of frequency response curves are altered by the neuromodulator serotonin, but the changes in excitatory-inhibitory balance that mediate this plasticity are not well understood. Previous findings suggest that the presynaptic 5-HT1B receptor may act to decrease the release of GABA onto IC neurons. Here, in vivo extracellular recording and iontophoresis of the selective 5-HT1B agonist CP93129 were used to characterize inhibition within and surrounding frequency response curves using two-tone protocols to indirectly measure inhibition as a decrease in spikes relative to an excitatory tone alone. The 5-HT1B agonist attenuated such two-tone spike reduction in a varied pattern among neurons, suggesting that the function of 5-HT1B modulation also varies. The hypothesis that the 5-HT1B receptor reduces inhibition was tested by comparing the effects of CP93129 and the GABAA antagonists bicuculline and gabazine in the same neurons. The effects of GABAA antagonists on spike count, tuning bandwidth, two-tone ratio, and temporal response characteristics mimicked those of CP93129 across the neuron population. GABAA antagonists also blocked or reduced the facilitation of evoked responses by CP93129. These results are all consistent with the reduction of GABAA-mediated inhibition by 5-HT1B receptors in the IC, resulting in an increase in the level of evoked responses in some neurons, and a decrease in spectral selectivity in others.

scholarly journals Inverse Density of Iba1 and Glutamine Synthetase Expressing Glia in Rat Inferior Colliculus

2021 ◽  
Author(s):  
Llwyd David Orton
Keyword(s):  
Glial Cell ◽  
Calcium Binding ◽  
Cell Types ◽  
Central Nucleus ◽  
Gradual Transition ◽  
Relative Distribution ◽  
Dorsal Cortex ◽  
Auditory Midbrain ◽  
Cellular Density ◽  
Male Wistar Rats

Microglia and astrocytes undertake numerous essential roles in nervous systems but we know little of their anatomical distribution within numerous nuclei. In the principal nuclei of the mammalian auditory midbrain, the inferior colliculi (IC), the cellular density and relative distribution of glutamate synthetase (GS) expressing astrocytes and ionized calcium-binding adapter molecule 1 (Iba1) expressing microglia is unknown. To address this, the IC of young adult, male Wistar rats were immunohistochemically labelled for GS and Iba1, using chromogenic methods. Sub-regions of imaged IC sections were demarked and soma density of both cell types determined. GS labelled somata were twice more densely packed as Iba1 labelled somata throughout IC parenchyma and peri-vascular regions. Furthermore, GS labelled somata density was significantly lower in dorsal cortex than external cortex or central nucleus. Iba1 labelled somata density exhibited the opposite trend, revealing an inverse density of these glial cell types between IC sub-regions. GS labelled neuropil was strongest in the cortices with and a gradual transition of lighter labelling towards central nucleus. These data provide the first detailed descriptions of GS labelling in IC and demonstrate sub-regional differences in IC glial cell density. Taken together, these findings suggest neurochemical specialization of glia in IC sub-regions, likely related to local physiological and metabolic demands, with implications for IC function.

scholarly journals Nitric oxide signalling underlies salicylate-induced increases in neuronal firing in the inferior colliculus: a central mechanism of tinnitus?

2021 ◽  
Author(s):  
Bas MJ Olthof ◽  
Dominika Lyzwa ◽  
Sarah E Gartside ◽  
Adrian Rees
Keyword(s):  
Nitric Oxide ◽  
Inferior Colliculus ◽  
Auditory Pathway ◽  
Excitatory Input ◽  
Neuronal Firing ◽  
Auditory Midbrain ◽  
Nitric Oxide Synthase Inhibitor ◽  
Electrode Recording ◽  
Reverse Microdialysis ◽  
Synthase Inhibitor

The tinnitus-inducing agent salicylate reduces cochlear output but causes hyperactivity in higher auditory centres, including the inferior colliculus (the auditory midbrain). Using multi-electrode recording in anaesthetised guinea pigs (Cavia porcellus), we addressed the hypothesis that salicylate-induced hyperactivity in the inferior colliculus involves nitric oxide signalling secondary to increased ascending excitatory input. In the inferior colliculus, systemic salicylate (200 mg/kg i.p., 0 h) markedly increased spontaneous and sound-driven neuronal firing (3-6 h post drug) with both onset and sustained responses to pure tones being massively increased. Reverse microdialysis of increasing concentrations of salicylate directly into the inferior colliculus (100 μM-10 mM, from 0 h) failed to mimic systemic salicylate. In contrast, it caused a small, transient, increase in sound-driven firing (1 h), followed by a larger sustained decrease in both spontaneous and sound-driven firing (2-5 h). When salicylate was given systemically, reverse microdialysis of the neuronal nitric oxide synthase inhibitor L-methyl arginine into the inferior colliculus (500 mM, 2-6 h) completely blocked the salicylate-induced increase in spontaneous and sound-driven neuronal firing. Our data indicate that systemic salicylate induces neuronal hyperactivity in the auditory midbrain via a mechanism outside the inferior colliculus, presumably upstream in the auditory pathway; and that the mechanism is ultimately dependent on nitric oxide signalling within the inferior colliculus. Given that nitric oxide is known to mediate NMDA receptor signalling in the inferior colliculus, we propose that salicylate activates an ascending glutamatergic input to the inferior colliculus and that this is an important mechanism underlying salicylate-induced tinnitus.

scholarly journals α3β4* Nicotinic acetylcholine receptors strongly modulate the excitability of VIP neurons in the mouse inferior colliculus

2021 ◽  
Author(s):  
Luis M. Rivera-Perez ◽  
Julia T. Kwapiszewski ◽  
Michael T. Roberts
Keyword(s):  
Inferior Colliculus ◽  
Auditory System ◽  
Nicotinic Acetylcholine Receptors ◽  
Auditory Processing ◽  
Acetylcholine Receptors ◽  
Central Auditory System ◽  
Nicotinic Acetylcholine ◽  
The Brain ◽  
Cholinergic Terminals

AbstractThe inferior colliculus (IC), the midbrain hub of the central auditory system, receives extensive cholinergic input from the pontomesencephalic tegmentum. Activation of nicotinic acetylcholine receptors (nAChRs) in the IC can alter acoustic processing and enhance auditory task performance. However, how nAChRs affect the excitability of specific classes of IC neurons remains unknown. Recently, we identified vasoactive intestinal peptide (VIP) neurons as a distinct class of glutamatergic principal neurons in the IC. Here, in experiments using male and female mice, we show that cholinergic terminals are routinely located adjacent to the somas and dendrites of VIP neurons. Using whole-cell electrophysiology in brain slices, we found that acetylcholine drives surprisingly strong and long-lasting excitation and inward currents in VIP neurons. This excitation was unaffected by the muscarinic receptor antagonist atropine. Application of nAChR antagonists revealed that acetylcholine excites VIP neurons mainly via activation of α3β4* nAChRs, a nAChR subtype that is rare in the brain. Furthermore, we show that cholinergic excitation is intrinsic to VIP neurons and does not require activation of presynaptic inputs. Lastly, we found that low frequency trains of acetylcholine puffs elicited temporal summation in VIP neurons, suggesting that in vivo-like patterns of cholinergic input can reshape activity for prolonged periods. These results reveal the first cellular mechanisms of nAChR regulation in the IC, identify a functional role for α3β4* nAChRs in the auditory system, and suggest that cholinergic input can potently influence auditory processing by increasing excitability in VIP neurons and their postsynaptic targets.Key points summaryThe inferior colliculus (IC), the midbrain hub of the central auditory system, receives extensive cholinergic input and expresses a variety of nicotinic acetylcholine receptor (nAChR) subunits.In vivo activation of nAChRs alters the input-output functions of IC neurons and influences performance in auditory tasks. However, how nAChR activation affects the excitability of specific IC neuron classes remains unknown.Here we show in mice that cholinergic terminals are located adjacent to the somas and dendrites of VIP neurons, a class of IC principal neurons.We find that acetylcholine elicits surprisingly strong, long-lasting excitation of VIP neurons and this is mediated mainly through activation of α3β4* nAChRs, a subtype that is rare in the brain.Our data identify a role for α3β4* nAChRs in the central auditory pathway and reveal a mechanism by which cholinergic input can influence auditory processing in the IC and the postsynaptic targets of VIP neurons.

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