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.

scholarly journals Neural integration and enhancement from the inferior colliculus up to different layers of auditory cortex

2013 ◽  
Vol 110 (4) ◽  
pp. 1009-1020 ◽  
Author(s):  
Malgorzata M. Straka ◽  
Dillon Schendel ◽  
Hubert H. Lim
Keyword(s):  
Auditory Cortex ◽  
Inferior Colliculus ◽  
Primary Auditory Cortex ◽  
Neural Mechanism ◽  
Cortical Activation ◽  
Enhancement Effect ◽  
Auditory Midbrain ◽  
Temporal Cues ◽  
Neural Integration ◽  
The Individual

While the cochlear implant has successfully restored hearing to many deaf patients, it cannot benefit those without a functional auditory nerve or an implantable cochlea. As an alternative, the auditory midbrain implant (AMI) has been developed and implanted into deaf patients. Consisting of a single-shank array, the AMI is designed for stimulation along the tonotopic gradient of the inferior colliculus (ICC). Although the AMI can provide frequency cues, it appears to insufficiently transmit temporal cues for speech understanding because repeated stimulation of a single site causes strong suppressive and refractory effects. Applying the electrical stimulation to at least two sites within an isofrequency lamina can circumvent these refractory processes. Moreover, coactivation with short intersite delays (<5 ms) can elicit cortical activation which is enhanced beyond the summation of activity induced by the individual sites. The goal of our study was to further investigate the role of the auditory cortex in this enhancement effect. In guinea pigs, we electrically stimulated two locations within an ICC lamina or along different laminae with varying interpulse intervals (0–10 ms) and recorded activity in different locations and layers of primary auditory cortex (A1). Our findings reveal a neural mechanism that integrates activity only from neurons located within the same ICC lamina for short spiking intervals (<6 ms). This mechanism leads to enhanced activity into layers III–V of A1 that is further magnified in supragranular layers. This integration mechanism may contribute to perceptual coding of different sound features that are relevant for improving AMI performance.

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.

Auditory Cortical Responses to Electrical Stimulation of the Inferior Colliculus: Implications for an Auditory Midbrain Implant

2006 ◽  
Vol 96 (3) ◽  
pp. 975-988 ◽  
Author(s):  
Hubert H. Lim ◽  
David J. Anderson
Keyword(s):  
Electrical Stimulation ◽  
Inferior Colliculus ◽  
Dynamic Range ◽  
Primary Auditory Cortex ◽  
Single Pulse ◽  
Central Nucleus ◽  
Published Data ◽  
Auditory Prosthesis ◽  
Auditory Midbrain ◽  
Stimulation Of

The success and limitations of cochlear implants (CIs) along with recent advances in deep brain stimulation and neural engineering have motivated the development of a central auditory prosthesis. In this study, we investigated the effects of electrical stimulation of the inferior colliculus central nucleus (ICC) on primary auditory cortex (A1) activity to determine the potential benefits of an auditory midbrain implant (AMI). We recorded multiunit activity in A1 of ketamine-anesthetized guinea pigs in response to single-pulse (200 μs/phase) monopolar stimulation of the ICC using multisite silicon-substrate probes. We then compared measures of threshold, dynamic range, and tonotopic spread of activation for ICC stimulation with that of published data for CI stimulation. Our results showed that compared with cochlear stimulation, ICC stimulation achieved: 1) thresholds about 8 dB lower; 2) dynamic ranges ≥4 dB greater; and 3) more localized, frequency-specific activation, even though frequency specificity was partially lost at higher stimulus levels for low-frequency ICC regions. Our results also showed that stimulation of rostral ICC regions elicited lower thresholds but with greater activation spread along the tonotopic gradient of A1 than did stimulation of more caudal regions. These results suggest that an AMI may improve frequency and level coding with lower energy requirements compared with CIs. However, a trade-off between lower perceptual thresholds and better frequency discrimination may exist that depends on location of stimulation along the caudorostral dimension of the ICC. Overall, this study provides the foundation for future AMI research and development.

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.

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.

scholarly journals Spectral and Temporal Modulation Tradeoff in the Inferior Colliculus

2010 ◽  
Vol 103 (2) ◽  
pp. 887-903 ◽  
Author(s):  
Francisco A. Rodríguez ◽  
Heather L. Read ◽  
Monty A. Escabí
Keyword(s):  
Inferior Colliculus ◽  
Spectral Characteristics ◽  
Receptive Fields ◽  
Nerve Fibers ◽  
Central Nucleus ◽  
Natural Sounds ◽  
Auditory Midbrain ◽  
Spectrotemporal Receptive Fields ◽  
Low Pass ◽  
Frequency Selective Channels

The cochlea encodes sounds through frequency-selective channels that exhibit low-pass modulation sensitivity. Unlike the cochlea, neurons in the auditory midbrain are tuned for spectral and temporal modulations found in natural sounds, yet the role of this transformation is not known. We report a distinct tradeoff in modulation sensitivity and tuning that is topographically ordered within the central nucleus of the inferior colliculus (CNIC). Spectrotemporal receptive fields (STRFs) were obtained with 16-channel electrodes inserted orthogonal to the isofrequency lamina. Surprisingly, temporal and spectral characteristics exhibited an opposing relationship along the tonotopic axis. For low best frequencies (BFs), units were selective for fast temporal and broad spectral modulations. A systematic progression was observed toward slower temporal and finer spectral modulation sensitivity at high BF. This tradeoff was strongly reflected in the arrangement of excitation and inhibition and, consequently, in the modulation tuning characteristics. Comparisons with auditory nerve fibers show that these trends oppose the pattern imposed by the peripheral filters. These results suggest that spectrotemporal preferences are reordered within the tonotopic axis of the CNIC. This topographic organization has profound implications for the coding of spectrotemporal features in natural sounds and could underlie a number of perceptual phenomena.

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.

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