Immediate Changes in Tuning of Inferior Colliculus Neurons Following Acute Lesions of Cat Spiral Ganglion

2002 ◽  
Vol 87 (1) ◽  
pp. 434-452 ◽  
Author(s):  
Russell L. Snyder ◽  
Donal G. Sinex
Keyword(s):  
Inferior Colliculus ◽  
Spiral Ganglion ◽  
Primary Auditory Cortex ◽  
Compound Action Potential ◽  
Central Nucleus ◽  
Auditory Information ◽  
Cells Of Origin ◽  
Wide Range ◽  
Before And After ◽  
Evoked Compound Action Potential

In previous studies, we demonstrated that acute lesions the spiral ganglion (SG), the cells of origin of the auditory nerve (AN), change the frequency organization of the inferior colliculus central nucleus (ICC) and primary auditory cortex (AI). In those studies, we used a map/re-map approach and recorded the tonotopic organization of neurons before and after restricted SG lesions. In the present study, response areas (RAs) of ICC multi-neuronal clusters were recorded to contralateral and ipsilateral tones after inserting and fixing-in-place tungsten microelectrodes. RAs were recorded from most electrodes before, immediately (within 33–78 min) after, and long(several hours) after restricted mechanical lesions of the ganglion. Each SG lesion produced a “notch” in the tone-evoked compound action potential (CAP) audiogram corresponding to a narrow range of lesion frequencies with elevated thresholds. Responses of contralateral IC neurons, which responded to these lesion frequencies, underwent an elevation in threshold to the lesion frequencies with either no change in sensitivity to other frequencies or with dramatic decreases in threshold to lesion-edge frequencies. These changes in sensitivity produced shifts in characteristic frequency (CF) that could be more than an octave. Thresholds at these new CFs matched the prelesion thresholds of neurons tuned to the lesion-edge frequencies. Responses evoked by ipsilateral tones delivered to the intact ear often underwent complementary changes, i.e., decreased thresholds to lesion frequency tones with little or no change in sensitivity to other frequencies. These results indicate that responses of IC neurons are produced by convergence of auditory information across a wide range of AN fibers and that the acute “plastic” changes reported in our previous studies occur within 1 h of an SG lesion.

Intracellular Recording Reveals Temporal Integration in Inferior Colliculus Neurons of Awake Bats

2007 ◽  
Vol 97 (2) ◽  
pp. 1368-1378 ◽  
Author(s):  
S. V. Voytenko ◽  
A. V. Galazyuk
Keyword(s):  
Inferior Colliculus ◽  
Temporal Integration ◽  
Myotis Lucifugus ◽  
Central Nucleus ◽  
Intracellular Recordings ◽  
Auditory Pathways ◽  
Postsynaptic Potentials ◽  
Sound Levels ◽  
Wide Range ◽  
Little Brown Bats

The central nucleus of the inferior colliculus (IC) is a major integrative center in the central auditory system. It receives information from both the ascending and descending auditory pathways. To determine how single IC neurons integrate information over a wide range of sound frequencies and sound levels, we examined their intracellular responses to frequency-modulated (FM) sounds in awake little brown bats ( Myotis lucifugus). Postsynaptic potentials were recorded in response to downward FM sweeps of the range typical for little brown bats (80–20 kHz) and to three FM subcomponents (80–60, 60–40, and 40–20 kHz). The majority of recorded neurons responded to the 80- to 20-kHz downward FM sweep with a complex response. In this response an initial hyperpolarization was followed by depolarization with or without spike followed by hyperpolarization. Intracellular recordings in response to three FM subcomponents revealed that these neurons receive excitatory and inhibitory inputs from a wide range of sound frequencies. One third of IC neurons performed nearly linear temporal summation across a wide range of sound frequencies, whereas two thirds of IC neurons exhibited nonlinear summation with different degrees of nonlinearity. Some IC neurons showed different latencies of postsynaptic potentials in response to different FM subcomponents. Often responses to the later FM subcomponent occurred before responses to the earlier ones. This phenomenon may be responsible for response selectivity of IC neurons to FM sweeps.

scholarly journals Antidromic Activation Reveals Tonotopically Organized Projections From Primary Auditory Cortex to the Central Nucleus of the Inferior Colliculus in Guinea Pig

2007 ◽  
Vol 97 (2) ◽  
pp. 1413-1427 ◽  
Author(s):  
Hubert H. Lim ◽  
David J. Anderson
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Spatial Organization ◽  
Medial Geniculate Body ◽  
Primary Auditory Cortex ◽  
Central Nucleus ◽  
Antidromic Activation ◽  
Antidromic Stimulation ◽  
Medial Geniculate ◽  
Layer V

The inferior colliculus (IC) is highly modulated by descending projections from higher auditory and nonauditory centers. Traditionally, corticofugal fibers were believed to project mainly to the extralemniscal IC regions. However, there is some anatomical evidence suggesting that a substantial number of fibers from the primary auditory cortex (A1) project into the IC central nucleus (ICC) and appear to be tonotopically organized. In this study, we used antidromic stimulation combined with other electrophysiological techniques to further investigate the spatial organization of descending fibers from A1 to the ICC in ketamine-anesthetized guinea pigs. Based on our findings, corticofugal fibers originate predominantly from layer V of A1, are amply scattered throughout the ICC and only project to ICC neurons with a similar best frequency (BF). This strict tonotopic pattern suggests that these corticofugal projections are involved with modulating spectral features of sound. Along the isofrequency dimension of the ICC, there appears to be some differences in projection patterns that depend on BF region and possibly isofrequency location within A1 and may be indicative of different descending coding strategies. Furthermore, the success of the antidromic stimulation method in our study demonstrates that it can be used to investigate some of the functional properties associated with corticofugal projections to the ICC as well as to other regions (e.g., medial geniculate body, cochlear nucleus). Such a method can address some of the limitations with current anatomical techniques for studying the auditory corticofugal system.

scholarly journals Hair cells use active zones with different voltage dependence of Ca2+ influx to decompose sounds into complementary neural codes

2016 ◽  
Vol 113 (32) ◽  
pp. E4716-E4725 ◽  
Author(s):  
Tzu-Lun Ohn ◽  
Mark A. Rutherford ◽  
Zhizi Jing ◽  
Sangyong Jung ◽  
Carlos J. Duque-Afonso ◽  
...  
Keyword(s):  
Hair Cells ◽  
Dynamic Range ◽  
Spiral Ganglion ◽  
Spatial Gradient ◽  
Auditory Information ◽  
Neural Codes ◽  
Deafness Gene ◽  
Wide Range ◽  
Ganglion Neurons ◽  
Channel Properties

For sounds of a given frequency, spiral ganglion neurons (SGNs) with different thresholds and dynamic ranges collectively encode the wide range of audible sound pressures. Heterogeneity of synapses between inner hair cells (IHCs) and SGNs is an attractive candidate mechanism for generating complementary neural codes covering the entire dynamic range. Here, we quantified active zone (AZ) properties as a function of AZ position within mouse IHCs by combining patch clamp and imaging of presynaptic Ca2+ influx and by immunohistochemistry. We report substantial AZ heterogeneity whereby the voltage of half-maximal activation of Ca2+ influx ranged over ∼20 mV. Ca2+ influx at AZs facing away from the ganglion activated at weaker depolarizations. Estimates of AZ size and Ca2+ channel number were correlated and larger when AZs faced the ganglion. Disruption of the deafness gene GIPC3 in mice shifted the activation of presynaptic Ca2+ influx to more hyperpolarized potentials and increased the spontaneous SGN discharge. Moreover, Gipc3 disruption enhanced Ca2+ influx and exocytosis in IHCs, reversed the spatial gradient of maximal Ca2+ influx in IHCs, and increased the maximal firing rate of SGNs at sound onset. We propose that IHCs diversify Ca2+ channel properties among AZs and thereby contribute to decomposing auditory information into complementary representations in SGNs.

Coactivation of different neurons within an isofrequency lamina of the inferior colliculus elicits enhanced auditory cortical activation

2012 ◽  
Vol 108 (4) ◽  
pp. 1199-1210 ◽  
Author(s):  
Roger Calixto ◽  
Minoo Lenarz ◽  
Anke Neuheiser ◽  
Verena Scheper ◽  
Thomas Lenarz ◽  
...  
Keyword(s):  
Inferior Colliculus ◽  
Temporal Integration ◽  
Three Dimensional ◽  
Primary Auditory Cortex ◽  
Cortical Activation ◽  
Central Nucleus ◽  
Speech Understanding ◽  
Auditory Midbrain ◽  
Temporal Cues ◽  
Multiple Regions

The phenomenal success of the cochlear implant (CI) is attributed to its ability to provide sufficient temporal and spectral cues for speech understanding. Unfortunately, the CI is ineffective for those without a functional auditory nerve or an implantable cochlea required for CI implementation. As an alternative, our group developed and implanted in deaf patients a new auditory midbrain implant (AMI) to stimulate the central nucleus of the inferior colliculus (ICC). Although the AMI can provide frequency cues, it appears to insufficiently transmit temporal cues for speech understanding. The three-dimensional ICC consists of two-dimensional isofrequency laminae. The single-shank AMI only stimulates one site in any given ICC lamina and does not exhibit enhanced activity (i.e., louder percepts or lower thresholds) for repeated pulses on the same site with intervals <2–5 ms, as occurs for CI pulse or acoustic click stimulation. This enhanced activation, related to short-term temporal integration, is important for tracking the rapid temporal fluctuations of a speech signal. Therefore, we investigated the effects of coactivation of different regions within an ICC lamina on primary auditory cortex activity in ketamine-anesthetized guinea pigs. Interestingly, our findings reveal an enhancement mechanism for integrating converging inputs from an ICC lamina on a fast scale (<6-ms window) that is compromised when stimulating just a single ICC location. Coactivation of two ICC regions also reduces the strong and long-term (>100 ms) suppressive effects induced by repeated stimulation of just a single location. Improving AMI performance may require at least two shanks implanted along the tonotopic gradient of the ICC that enables coactivation of multiple regions along an ICC lamina with the appropriate interstimulus delays.

Corticofugal Shaping of Frequency Tuning Curves in the Central Nucleus of the Inferior Colliculus of Mice

2005 ◽  
Vol 93 (1) ◽  
pp. 71-83 ◽  
Author(s):  
Jun Yan ◽  
Yunfeng Zhang ◽  
Günter Ehret
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Cortical Neurons ◽  
Frequency Tuning ◽  
Tuning Curve ◽  
Primary Auditory Cortex ◽  
Nerve Fibers ◽  
Cortical Activation ◽  
Central Nucleus ◽  
Tuning Curves

Plasticity of the auditory cortex can be induced by conditioning or focal cortical stimulation. The latter was used here to measure how stimulation in the tonotopy of the mouse primary auditory cortex influences frequency tuning in the midbrain central nucleus of the inferior colliculus (ICC). Shapes of collicular frequency tuning curves (FTCs) were quantified before and after cortical activation by measuring best frequencies, FTC bandwidths at various sound levels, level tolerance, Q-values, steepness of low- and high-frequency slopes, and asymmetries. We show here that all of these measures were significantly changed by focal cortical activation. The changes were dependent not only on the relationship of physiological properties between the stimulated cortical neurons and recorded collicular neurons but also on the tuning curve class of the collicular neuron. Cortical activation assimilated collicular FTC shapes; sharp and broad FTCs were changed to the shapes comparable to those of auditory nerve fibers. Plasticity in the ICC was organized in a center (excitatory)-surround (inhibitory) way with regard to the stimulated location (i.e., the frequency) of cortical tonotopy. This ensures, together with the spatial gradients of distribution of collicular FTC shapes, a sharp spectral filtering at the core of collicular frequency-band laminae and an increase in frequency selectivity at the periphery of the laminae. Mechanisms of FTC plasticity were suggested to comprise both corticofugal and local ICC components of excitatory and inhibitory modulation leading to a temporary change of the balance between excitation and inhibition in the ICC.

scholarly journals Passive stimulation and behavioral training differentially transform temporal processing in the inferior colliculus and primary auditory cortex

2017 ◽  
Vol 117 (1) ◽  
pp. 47-64 ◽  
Author(s):  
Maike Vollmer ◽  
Ralph E. Beitel ◽  
Christoph E. Schreiner ◽  
Patricia A. Leake
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Temporal Processing ◽  
Electric Stimulation ◽  
Primary Auditory Cortex ◽  
Central Nucleus ◽  
Electrophysiological Recording ◽  
Response Patterns ◽  
Behavioral Training ◽  
Auditory Midbrain

In profoundly deaf cats, behavioral training with intracochlear electric stimulation (ICES) can improve temporal processing in the primary auditory cortex (AI). To investigate whether similar effects are manifest in the auditory midbrain, ICES was initiated in neonatally deafened cats either during development after short durations of deafness (8 wk of age) or in adulthood after long durations of deafness (≥3.5 yr). All of these animals received behaviorally meaningless, “passive” ICES. Some animals also received behavioral training with ICES. Two long-deaf cats received no ICES prior to acute electrophysiological recording. After several months of passive ICES and behavioral training, animals were anesthetized, and neuronal responses to pulse trains of increasing rates were recorded in the central (ICC) and external (ICX) nuclei of the inferior colliculus. Neuronal temporal response patterns (repetition rate coding, minimum latencies, response precision) were compared with results from recordings made in the AI of the same animals (Beitel RE, Vollmer M, Raggio MW, Schreiner CE. J Neurophysiol 106: 944–959, 2011; Vollmer M, Beitel RE. J Neurophysiol 106: 2423–2436, 2011). Passive ICES in long-deaf cats remediated severely degraded temporal processing in the ICC and had no effects in the ICX. In contrast to observations in the AI, behaviorally relevant ICES had no effects on temporal processing in the ICC or ICX, with the single exception of shorter latencies in the ICC in short-deaf cats. The results suggest that independent of deafness duration passive stimulation and behavioral training differentially transform temporal processing in auditory midbrain and cortex, and primary auditory cortex emerges as a pivotal site for behaviorally driven neuronal temporal plasticity in the deaf cat. NEW & NOTEWORTHY Behaviorally relevant vs. passive electric stimulation of the auditory nerve differentially affects neuronal temporal processing in the central nucleus of the inferior colliculus (ICC) and the primary auditory cortex (AI) in profoundly short-deaf and long-deaf cats. Temporal plasticity in the ICC depends on a critical amount of electric stimulation, independent of its behavioral relevance. In contrast, the AI emerges as a pivotal site for behaviorally driven neuronal temporal plasticity in the deaf auditory system.

scholarly journals Potential implications of slim modiolar electrodes for severely malformed cochlea: A comparison with the straight array with circumferential electrodes

2021 ◽  
Author(s):  
Sang-Yeon Lee ◽  
Byung Yoon Choi
Keyword(s):  
Spiral Ganglion ◽  
Compound Action Potential ◽  
Lateral Wall ◽  
Electrode Position ◽  
Type I ◽  
Evoked Compound Action Potential ◽  
Incomplete Partition ◽  
Auditory Performance ◽  
Ganglion Neurons ◽  
Selection Of

Objectives: Malformations of the inner ear account for approximately 20% of congenital deafness. In current practice, the straight arrays with circumferential electrodes (i.e., full-banded electrodes) are widely used in severely malformed cochlea. However, the unpredictability of the location of residual spiral ganglion neurons in such malformations argues against obligatorily pursuing the full-banded electrode in all cases. Here, we present an experience of electrically evoked compound action potential (ECAP) and radiography-based selection of an appropriate electrode for severely malformed cochlea. Methods: Three patients with the severely malformed cochlea, showing cochlear hypoplasia type II (CH-II), incomplete partition type I (IP-I), and cochlear aplasia with a dilated vestibule (CADV), were included, and the cochlear nerve deficiency (CND) was evaluated. Full-banded electrode (CI24RE(ST)) and slim modiolar electrode (CI632) were alternately inserted to compare ECAP responses and electrode position. Results: In patient 1 (CH-II with CND) who had initially undergone cochlear implantation (CI) using the lateral wall electrode (CI422), a revision CI was performed due to incomplete insertion of CI422 and resultant unsatisfactory performance, thus explanting the CI422 and re-inserting the CI24RE(ST) and CI632 sequentially. Although both electrodes elicited reliable ECAP responses with correct positioning, CI24RE(ST) showed overall lower ECAP thresholds compared to CI632; thus, CI24RE(ST) was selected. In patient 2 (IP-I with CND), CI632 elicited superior ECAP responses relative to CI24RE(ST), with correct positioning of the electrode; CI632 was chosen. In patient 3 (CADV), CI632 did not elicit an ECAP response while meaningful ECAP responses were obtained with the CI24RE(ST) array once correct positioning was achieved. All patients markedly improved auditory performance postoperatively. Conclusion: ECAP and radiography-based strategy for an appropriate electrode may be useful for severely malformed cochlea, leading to enhanced functional outcomes. Additionally, the practice of sticking to the full-banded straight electrode may not always be the best for IP-I and CH-II.

Neuron Types, Intrinsic Circuits, and Plasticity in the Inferior Colliculus

2018 ◽  
pp. 502-526
Author(s):  
Tetsufumi Ito ◽  
Munenori Ono ◽  
Douglas L. Oliver
Keyword(s):  
Inferior Colliculus ◽  
De Novo ◽  
Future Research ◽  
Auditory Information ◽  
Wide Range ◽  
Neuronal Types ◽  
Key Issues ◽  
Complex Features ◽  
Local Circuits ◽  
Local Connection

The inferior colliculus is a critical auditory center in the midbrain which virtually acts as a hub of all ascending and descending auditory information flows. Wide variety of neuronal responses to sound is found in the IC, and this variety emerges not only from the wide range of extrinsic afferent inputs, but also from the complex features of the local circuits in the IC, for example, the mosaic pattern of extrinsic fiber termination, the various neuronal types each of which compose different patterns of local connection, and the unique forms of synaptic plasticity de novo. This chapter reviews the recent progress in understanding these features, and identifies the key issues for future research.

AMPA and NMDA Receptors Regulate Responses of Neurons in the Rat's Inferior Colliculus

2001 ◽  
Vol 86 (2) ◽  
pp. 871-880 ◽  
Author(s):  
Huiming Zhang ◽  
Jack B. Kelly
Keyword(s):  
Nmda Receptors ◽  
Inferior Colliculus ◽  
Ampa Receptors ◽  
Action Potentials ◽  
Drug Application ◽  
Pronounced Effect ◽  
Central Nucleus ◽  
Wide Range ◽  
Ampa And Nmda Receptors ◽  
Excitatory Responses

The contribution of N-methyl-d-aspartate (NMDA) and AMPA receptors to auditory responses in the rat's inferior colliculus was examined by recording single-unit activity before, during, and after local iontophoretic application of receptor-specific antagonists. Tone bursts and sinusoidal amplitude modulated sounds were presented to one ear, and recordings were made from the contralateral central nucleus of inferior colliculus (ICC). The receptor specific antagonists, (±)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP) for NMDA receptors and 1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide (NBQX) for AMPA receptors, were released at the recording site through a multi-barreled pipette. For most neurons, either CPP or NBQX alone resulted in a reversible reduction in the number of action potentials evoked by tonal stimulation. For neurons with an onset response pattern, NBQX either completely eliminated or greatly reduced the number of action potentials. CPP also reduced the number of action potentials but had a less pronounced effect than NBQX. For neurons with a sustained firing pattern, NBQX reduced the total number of action potentials, but had a preferential effect on the early part (first 10–20 ms) of the response. CPP also resulted in a reduction in the total number of action potentials, but had a more pronounced effect on the later part (>20 ms) of the response. These results indicate that both AMPA and NMDA receptors contribute to sound evoked excitatory responses in the ICC. They have a selective influence on early and late components of tone-evoked responses. Both receptor types are involved in generating excitatory responses across a wide range of sound pressure levels as indicated by rate level functions obtained before and during drug application. In addition, both CPP and NBQX reduced responses to sinusoidal amplitude modulated sounds. The synchrony of firing to the modulation envelope as measured by vector strength at different rates of modulation was not greatly affected by either CPP or NBQX in spite of the decrease in firing rate.

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