Neurosteroids Involved in Regulating Inhibition in the Inferior Colliculus

2006 ◽  
Vol 96 (6) ◽  
pp. 3064-3073 ◽  
Author(s):  
Yuri B. Saalmann ◽  
Ian G. Morgan ◽  
Mike B. Calford
Keyword(s):  
Inferior Colliculus ◽  
Physiological Role ◽  
Pharmacological Action ◽  
Central Nucleus ◽  
Neural Population ◽  
Neuron Activity ◽  
Auditory Midbrain ◽  
Inhibitory Circuits ◽  
Acid Type ◽  
The Brain

Fast inhibitory neurotransmission in the brain is largely mediated by the γ-aminobutyric acid-type A (GABAA) receptor. The 3α,5α-reduced neurosteroids (e.g., allopregnanolone) are the most potent endogenous modulators of the GABAA receptor. Although it is known that 3α,5α-reduced neurosteroid levels change during stress or depression and over the estrus cycle, a basic physiological role consistent with their pharmacological action remains elusive. We used the unique architecture of the auditory midbrain to reveal a role for 3α,5α-reduced neurosteroids in regulating inhibitory efficacy. After blocking the massive GABAergic projection from the dorsal nucleus of the lateral lemniscus (DNLL) to the contralateral central nucleus of the inferior colliculus (ICC) in anesthetized rats, a reactive increase in the efficacy of other inhibitory circuits in the ICC (separable because of the dominant ear that drives each circuit) was demonstrated with physiological measures—single-neuron activity and a neural-population-evoked response. This effect was prevented by blocking 3α,5α-reduced neurosteroid synthesis with a 5α-reductase inhibitor: finasteride. Immunohistochemistry confirmed that the DNLL blockade induced an increase in 3α,5α-reduced neurosteroids in the contralateral ICC. This study shows that when GABAergic inhibition is reduced, the brain compensates within minutes by locally increasing synthesis of neurosteroids, thereby balancing excitatory and inhibitory inputs in complex neural circuits.

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.

Binaural masking and sensitivity to interaural delay in the inferior colliculus

1992 ◽  
Vol 336 (1278) ◽  
pp. 415-422 ◽  
Keyword(s):  
Inferior Colliculus ◽  
Physiological Mechanism ◽  
Central Nucleus ◽  
Neural Population ◽  
Physiological Basis ◽  
Low Frequencies ◽  
Delay Sensitive ◽  
Masking Level Difference ◽  
The Mean ◽  
Number Of Discharges

The binaural masking level difference (BMLD) is a psychophysical effect whereby signals masked by a noise at one ear become unmasked by sounds reaching the other, BMLD effects are largest at low frequencies where they depend on signal phase, suggesting that part of the physiological mechanism responsible for the BMLD resides in cells that are sensitive to interaural time disparities. We have investigated a physiological basis for unmasking in the responses of delay-sensitive cells in the central nucleus of the inferior colliculus in anaesthetized guinea pigs. The masking effects of a binaurally presented noise, as a function of the masker delay, were quantified by measuring the number of discharges synchronized to the signal, and by measuring the masked threshold. The noise level for masking was lowest at the best delay for the noise. The mean magnitude of the unmasking across our neural population was similar to the human psychophysical BMLD under the same signal and masker conditions.

scholarly journals Preservation of Spectrotemporal Tuning Between the Nucleus Laminaris and the Inferior Colliculus of the Barn Owl

2007 ◽  
Vol 97 (5) ◽  
pp. 3544-3553 ◽  
Author(s):  
G. Björn Christianson ◽  
José Luis Peña
Keyword(s):  
Inferior Colliculus ◽  
Phase Locking ◽  
Interaural Time Difference ◽  
Barn Owl ◽  
Central Nucleus ◽  
Sound Recognition ◽  
Spectral Structure ◽  
Two Stages ◽  
The Brain ◽  
Ongoing Phase

Performing sound recognition is a task that requires an encoding of the time-varying spectral structure of the auditory stimulus. Similarly, computation of the interaural time difference (ITD) requires knowledge of the precise timing of the stimulus. Consistent with this, low-level nuclei of birds and mammals implicated in ITD processing encode the ongoing phase of a stimulus. However, the brain areas that follow the binaural convergence for the computation of ITD show a reduced capacity for phase locking. In addition, we have shown that in the barn owl there is a pooling of ITD-responsive neurons to improve the reliability of ITD coding. Here we demonstrate that despite two stages of convergence and an effective loss of phase information, the auditory system of the anesthetized barn owl displays a graceful transition to an envelope coding that preserves the spectrotemporal information throughout the ITD pathway to the neurons of the core of the central nucleus of the inferior colliculus.

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 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 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.

scholarly journals Response features across the auditory midbrain reveal an organization consistent with a dual lemniscal pathway

2014 ◽  
Vol 112 (4) ◽  
pp. 981-998 ◽  
Author(s):  
Małgorzata M. Straka ◽  
Samuel Schmitz ◽  
Hubert H. Lim
Keyword(s):  
Spatial Distribution ◽  
Auditory System ◽  
Local Field ◽  
Guinea Pigs ◽  
Pure Tone ◽  
Three Dimensional ◽  
Central Nucleus ◽  
Field Potentials ◽  
Auditory Midbrain ◽  
The Brain

The central auditory system has traditionally been divided into lemniscal and nonlemniscal pathways leading from the midbrain through the thalamus to the cortex. This view has served as an organizing principle for studying, modeling, and understanding the encoding of sound within the brain. However, there is evidence that the lemniscal pathway could be further divided into at least two subpathways, each potentially coding for sound in different ways. We investigated whether such an interpretation is supported by the spatial distribution of response features in the central nucleus of the inferior colliculus (ICC), the part of the auditory midbrain assigned to the lemniscal pathway. We recorded responses to pure tone stimuli in the ICC of ketamine-xylazine-anesthetized guinea pigs and used three-dimensional brain reconstruction techniques to map the location of the recording sites. Compared with neurons in caudal-and-medial regions within an isofrequency lamina of the ICC, neurons in rostral-and-lateral regions responded with shorter first-spike latencies with less spiking jitter, shorter durations of spiking responses, a higher proportion of spikes occurring near the onset of the stimulus, lower thresholds, and larger local field potentials with shorter latencies. Further analysis revealed two distinct clusters of response features located in either the caudal-and-medial or the rostral-and-lateral parts of the isofrequency laminae of the ICC. Thus we report substantial differences in coding properties in two regions of the ICC that are consistent with the hypothesis that the lemniscal pathway is made up of at least two distinct subpathways from the midbrain up to the cortex.

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.

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