scholarly journals Transformation of spatial sensitivity along the ascending auditory pathway

2015 ◽  
Vol 113 (9) ◽  
pp. 3098-3111 ◽  
Author(s):  
Justin D. Yao ◽  
Peter Bremen ◽  
John C. Middlebrooks

Locations of sounds are computed in the central auditory pathway based primarily on differences in sound level and timing at the two ears. In rats, the results of that computation appear in the primary auditory cortex (A1) as exclusively contralateral hemifield spatial sensitivity, with strong responses to sounds contralateral to the recording site, sharp cutoffs across the midline, and weak, sound-level-tolerant responses to ipsilateral sounds. We surveyed the auditory pathway in anesthetized rats to identify the brain level(s) at which level-tolerant spatial sensitivity arises. Noise-burst stimuli were varied in horizontal sound location and in sound level. Neurons in the central nucleus of the inferior colliculus (ICc) displayed contralateral tuning at low sound levels, but tuning was degraded at successively higher sound levels. In contrast, neurons in the nucleus of the brachium of the inferior colliculus (BIN) showed sharp, level-tolerant spatial sensitivity. The ventral division of the medial geniculate body (MGBv) contained two discrete neural populations, one showing broad sensitivity like the ICc and one showing sharp sensitivity like A1. Dorsal, medial, and shell regions of the MGB showed fairly sharp spatial sensitivity, likely reflecting inputs from A1 and/or the BIN. The results demonstrate two parallel brainstem pathways for spatial hearing. The tectal pathway, in which sharp, level-tolerant spatial sensitivity arises between ICc and BIN, projects to the superior colliculus and could support reflexive orientation to sounds. The lemniscal pathway, in which such sensitivity arises between ICc and the MGBv, projects to the forebrain to support perception of sound location.

2016 ◽  
Vol 115 (1) ◽  
pp. 193-207 ◽  
Author(s):  
Mitchell L. Day ◽  
Bertrand Delgutte

At lower levels of sensory processing, the representation of a stimulus feature in the response of a neural population can vary in complex ways across different stimulus intensities, potentially changing the amount of feature-relevant information in the response. How higher-level neural circuits could implement feature decoding computations that compensate for these intensity-dependent variations remains unclear. Here we focused on neurons in the inferior colliculus (IC) of unanesthetized rabbits, whose firing rates are sensitive to both the azimuthal position of a sound source and its sound level. We found that the azimuth tuning curves of an IC neuron at different sound levels tend to be linear transformations of each other. These transformations could either increase or decrease the mutual information between source azimuth and spike count with increasing level for individual neurons, yet population azimuthal information remained constant across the absolute sound levels tested (35, 50, and 65 dB SPL), as inferred from the performance of a maximum-likelihood neural population decoder. We harnessed evidence of level-dependent linear transformations to reduce the number of free parameters in the creation of an accurate cross-level population decoder of azimuth. Interestingly, this decoder predicts monotonic azimuth tuning curves, broadly sensitive to contralateral azimuths, in neurons at higher levels in the auditory pathway.


2007 ◽  
Vol 97 (2) ◽  
pp. 1413-1427 ◽  
Author(s):  
Hubert H. Lim ◽  
David J. Anderson

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.


1973 ◽  
Vol 38 (3) ◽  
pp. 320-325 ◽  
Author(s):  
Ronald R. Tasker ◽  
L. W. Organ

✓ Auditory hallucinations were produced by electrical stimulation of the human upper brain stem during stereotaxic operations. The responses were confined to stimulation of the inferior colliculus, brachium of the inferior colliculus, medial geniculate body, and auditory radiations. Anatomical confirmation of an auditory site was obtained in one patient. The hallucination produced was a low-pitched nonspecific auditory “paresthesia” independent of the structure stimulated, the conditions of stimulation, or sonotopic factors. The effect was identical to that reported from stimulating the primary auditory cortex, and virtually all responses were contralateral. These observations have led to the following generalizations concerning electrical stimulation of the somesthetic, auditory, vestibular, and visual pathways within the human brain stem: the hallucination induced in each is the response to comparable conditions of stimulation, is nonspecific, independent of stimulation site, confined to the primary pathway concerned, chiefly contralateral, and identical to that induced by stimulating the corresponding primary auditory cortex. No sensory responses are found in the brain stem corresponding to those from the sensory association cortex.


2014 ◽  
Vol 111 (5) ◽  
pp. 930-938 ◽  
Author(s):  
Michael Kyweriga ◽  
Whitney Stewart ◽  
Michael Wehr

How does the brain accomplish sound localization with invariance to total sound level? Sensitivity to interaural level differences (ILDs) is first computed at the lateral superior olive (LSO) and is observed at multiple levels of the auditory pathway, including the central nucleus of inferior colliculus (ICC) and auditory cortex. In LSO, this ILD sensitivity is level-dependent, such that ILD response functions shift toward the ipsilateral (excitatory) ear with increasing sound level. Thus early in the processing pathway changes in firing rate could indicate changes in sound location, sound level, or both. In ICC, while ILD responses can shift toward either ear in individual neurons, there is no net ILD response shift at the population level. In behavioral studies of human sound localization acuity, ILD sensitivity is invariant to increasing sound levels. Level-invariant sound localization would suggest transformation in level sensitivity between LSO and perception of sound sources. Whether this transformation is completed at the level of the ICC or continued at higher levels remains unclear. It also remains unknown whether perceptual sound localization is level-invariant in rats, as it is in humans. We asked whether ILD sensitivity is level-invariant in rat auditory cortex. We performed single-unit and whole cell recordings in rat auditory cortex under ketamine anesthesia and measured responses to white noise bursts presented through sealed earphones at a range of ILDs. Surprisingly, we found that with increasing sound levels ILD responses shifted toward the ipsilateral ear (which is typically inhibitory), regardless of whether cells preferred ipsilateral, contralateral, or binaural stimuli. Voltage-clamp recordings suggest that synaptic inhibition does not contribute substantially to this transformation in level sensitivity. We conclude that the level invariance of ILD sensitivity seen in behavioral studies is not present in rat auditory cortex.


2019 ◽  
Author(s):  
Yaqing Su ◽  
Bertrand Delgutte

AbstractHarmonic complex tones (HCT) commonly occurring in speech and music evoke a strong pitch at their fundamental frequency (F0), especially when they contain harmonics individually resolved by the cochlea. When all frequency components of an HCT are shifted by the same amount, the pitch of the resulting inharmonic tone (IHCT) also shifts although the envelope repetition rate is unchanged. A rate-place code whereby resolved harmonics are represented by local maxima in firing rates along the tonotopic axis has been characterized in the auditory nerve and primary auditory cortex, but little is known about intermediate processing stages. We recorded single neuron responses to HCT and IHCT with varying F0 and sound level in the inferior colliculus (IC) of unanesthetized rabbits. Many neurons showed peaks in firing rates when a low-numbered harmonic aligned with the neuron’s characteristic frequency, demonstrating “rate-place” coding. The IC rate-place code was most prevalent for F0>800 Hz, was only moderately dependent on sound level over a 40 dB range, and was not sensitive to stimulus harmonicity. A spectral receptive-field model incorporating broadband inhibition better predicted the neural responses than a purely excitatory model, suggesting an enhancement of the rate-place representation by inhibition. Some IC neurons showed facilitation in response to HCT, similar to cortical “harmonic template neurons” (Feng and Wang 2017), but to a lesser degree. Our findings shed light on the transformation of rate-place coding of resolved harmonics along the auditory pathway, and suggest a gradual emergence of harmonic templates from low to high processing centers.Significance statementHarmonic complex tones are ubiquitous in speech and music and produce strong pitch percepts in human listeners when they contain frequency components that are individually resolved by the cochlea. Here, we characterize a “rate-place” code for resolved harmonics in the auditory midbrain that is more robust across sound levels than the peripheral rate-place code and insensitive to the harmonic relationships among frequency components. We use a computational model to show that inhibition may play an important role in shaping the rate-place code. We also show that midbrain auditory neurons can demonstrate similar properties as cortical harmonic template neurons. Our study fills a gap in understanding the transformation in neural representations of resolved harmonics along the auditory pathway.


1975 ◽  
Vol 38 (5) ◽  
pp. 1208-1216 ◽  
Author(s):  
L. M. Aitkin ◽  
D. R. Moore

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.


2013 ◽  
Vol 110 (9) ◽  
pp. 2140-2151 ◽  
Author(s):  
Justin D. Yao ◽  
Peter Bremen ◽  
John C. Middlebrooks

The rat is a widely used species for study of the auditory system. Psychophysical results from rats have shown an inability to discriminate sound source locations within a lateral hemifield, despite showing fairly sharp near-midline acuity. We tested the hypothesis that those characteristics of the rat's sound localization psychophysics are evident in the characteristics of spatial sensitivity of its cortical neurons. In addition, we sought quantitative descriptions of in vivo spatial sensitivity of cortical neurons that would support development of an in vitro experimental model to study cortical mechanisms of spatial hearing. We assessed the spatial sensitivity of single- and multiple-neuron responses in the primary auditory cortex (A1) of urethane-anesthetized rats. Free-field noise bursts were varied throughout 360° of azimuth in the horizontal plane at sound levels from 10 to 40 dB above neural thresholds. All neurons encountered in A1 displayed contralateral-hemifield spatial tuning in that they responded strongly to contralateral sound source locations, their responses cut off sharply for locations near the frontal midline, and they showed weak or no responses to ipsilateral sources. Spatial tuning was quite stable across a 30-dB range of sound levels. Consistent with rat psychophysical results, a linear discriminator analysis of spike counts exhibited high spatial acuity for near-midline sounds and poor discrimination for off-midline locations. Hemifield spatial tuning is the most common pattern across all mammals tested previously. The homogeneous population of neurons in rat area A1 will make an excellent system for study of the mechanisms underlying that pattern.


2007 ◽  
Vol 97 (2) ◽  
pp. 1368-1378 ◽  
Author(s):  
S. V. Voytenko ◽  
A. V. Galazyuk

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.


1995 ◽  
Vol 74 (1) ◽  
pp. 1-11 ◽  
Author(s):  
I. Saitoh ◽  
N. Suga

1. The central auditory system of the mustached bat has arrays of delay-tuned (FM-FM combination-sensitive) neurons in the inferior colliculus, the medial geniculate body, and the auditory cortex. These neurons are tuned to particular echo delays, i.e., target distances. The neural mechanisms for creating the delay-tuned neurons involve delay lines, coincidence detection, and amplification. We have hypothesized that delay lines longer than 4 ms are created by inhibition occurring in the anterolateral division (ALD) of the central nucleus of the inferior colliculus. If this hypothesis is correct, suppression of inhibition occurring in the ALD must shorten the best delays of the collicular, thalamic, and cortical delay-tuned neurons. The aim of the present study is to test this hypothesis. Responses of single delay-tuned neurons in the FM-FM area of the auditory cortex were recorded with a tungsten-wire microelectrode, and the effects of iontophoretic microinjections of strychnine (STR) and/or bicuculline methiodide (BMI) into the ALD were examined on the responses of these neurons. 2. STR (glycine receptor antagonist) and/or BMI [gamma-aminobutyric acid-A (GABAA) receptor antagonist] injections into the ALD shortened the best delays of delay-tuned neurons in the FM-FM area with little change in their response patterns. The longer the best delay of a delay-tuned neuron, the larger the amount of shortening. 3. Inhibition mediated by glycine receptors plays a larger role in creating delay lines than that mediated by GABAA receptors, because STR and BMI, respectively, shortened the best delay of 91 and 74% of the neurons with best delays longer than 4.5 ms. 4. BMI has no effect on the best delays of delay-tuned neurons that were tuned to echo delays shorter than 4.5 ms. 5. The present data support the hypothesis that long delay lines utilized by delay-tuned neurons are created by inhibition occurring in the ALD of the inferior colliculus. However, the amount of shortening in delay lines by STR and/or BMI was generally smaller than that predicted by a neural network model. Therefore the present study partially answers the questions of where and how long delay lines were created.


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