Development of Cochlear Amplification, Frequency Tuning, and Two-Tone Suppression in the Mouse

2008 ◽  
Vol 99 (1) ◽  
pp. 344-355 ◽  
Author(s):  
Lei Song ◽  
JoAnn McGee ◽  
Edward J. Walsh

It is generally believed that the micromechanics of active cochlear transduction mature later than passive elements among altricial mammals. One consequence of this developmental order is the loss of transduction linearity, because an active, physiologically vulnerable process is superimposed on the passive elements of transduction. A triad of sensory advantage is gained as a consequence of acquiring active mechanics; sensitivity and frequency selectivity (frequency tuning) are enhanced and dynamic operating range increases. Evidence supporting this view is provided in this study by tracking the development of tuning curves in BALB/c mice. Active transduction, commonly known as cochlear amplification, enhances sensitivity in a narrow frequency band associated with the “tip” of the tuning curve. Passive aspects of transduction were assessed by considering the thresholds of responses elicited from the tuning curve “tail,” a frequency region that lies below the active transduction zone. The magnitude of cochlear amplification was considered by computing tuning curve tip-to-tail ratios, a commonly used index of active transduction gain. Tuning curve tip thresholds, frequency selectivity and tip-to-tail ratios, all indices of the functional status of active biomechanics, matured between 2 and 7 days after tail thresholds achieved adultlike values. Additionally, two-tone suppression, another product of active cochlear transduction, was first observed in association with the earliest appearance of tuning curve tips and matured along an equivalent time course. These findings support a traditional view of development in which the maturation of passive transduction precedes the maturation of active mechanics in the most sensitive region of the mouse cochlea.

1995 ◽  
Vol 74 (4) ◽  
pp. 1563-1572 ◽  
Author(s):  
M. P. McCue ◽  
J. J. Guinan

1. Recordings were made from single afferent fibers in the inferior vestibular nerve. Firing rates of a substantial portion of the afferents with irregular background activity increased in response to moderately intense tone bursts. 2. Spontaneous activity from acoustically responsive vestibular afferents was statistically analyzed and compared with data from a more widespread sampling of primary afferents in the cat's vestibulocochlear nerve. Acoustically responsive vestibular afferents had interspike interval histograms with modes > 10 ms, coefficients of variation > 0.15, and skews > 0.88. On the basis of spontaneous activity, these afferents were easily distinguishable from cochlear afferents and regular vestibular afferents, but no obvious features differentiated them from other irregular vestibular afferents. 3. The distributions of spike intervals in the spontaneous activity of acoustically responsive vestibular afferents were fitted by Erlang probability density functions describing the second-order interarrival times of a Poisson process initiated after a finite delay (refractory period). 4. Acoustically responsive vestibular afferents had broad, V-shaped tuning curves with best frequencies between 500 and 1,000 Hz, thresholds of > or = 90 dB SPL, and shapes comparable with the tuning-curve “tails” of cochlear afferents. In contrast to cochlear-nerve afferents, acoustically responsive vestibular afferents did not show a strong relationship between spontaneous rate and threshold. 5. We compare the acoustic frequency selectivity of vestibular and cochlear afferents in terms of their functional and evolutionary relationships. Our data and those of others indicate that acoustically responsive vestibular afferents are likely to provide an input to the acoustic activation of the sternocleidomastoid muscle in humans, and they may provide an input to other acoustic reflexes such as the middle-ear-muscle reflexes.


1997 ◽  
Vol 77 (2) ◽  
pp. 923-943 ◽  
Author(s):  
Michael Brosch ◽  
Christoph E. Schreiner

Brosch, Michael and Christoph E. Schreiner. Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 77: 923–943, 1997. Nonsimultaneous two-tone interactions were studied in the primary auditory cortex of anesthetized cats. Poststimulatory effects of pure tone bursts (masker) on the evoked activity of a fixed tone burst (probe) were investigated. The temporal interval from masker onset to probe onset (stimulus onset asynchrony), masker frequency, and intensity were parametrically varied. For all of the 53 single units and 58 multiple-unit clusters, the neural activity of the probe signal was either inhibited, facilitated, and/or delayed by a limited set of masker stimuli. The stimulus range from which forward inhibition of the probe was induced typically was centered at and had approximately the size of the neuron's excitatory receptive field. This “masking tuning curve” was usually V shaped, i.e., the frequency range of inhibiting masker stimuli increased with the masker intensity. Forward inhibition was induced at the shortest stimulus onset asynchrony between masker and probe. With longer stimulus onset asynchronies, the frequency range of inhibiting maskers gradually became smaller. Recovery from forward inhibition occurred first at the lower- and higher-frequency borders of the masking tuning curve and lasted the longest for frequencies close to the neuron's characteristic frequency. The maximal duration of forward inhibition was measured as the longest period over which reduction of probe responses was observed. It was in the range of 53–430 ms, with an average of 143 ± 71 (SD) ms. Amount, duration and type of forward inhibition were weakly but significantly correlated with “static” neural receptive field properties like characteristic frequency, bandwidth, and latency. For the majority of neurons, the minimal inhibitory masker intensity increased when the stimulus onset asynchrony became longer. In most cases the highest masker intensities induced the longest forward inhibition. A significant number of neurons, however, exhibited longest periods of inhibition after maskers of intermediate intensity. The results show that the ability of cortical cells to respond with an excitatory activity depends on the temporal stimulus context. Neurons can follow higher repetition rates of stimulus sequences when successive stimuli differ in their spectral content. The differential sensitivity to temporal sound sequences within the receptive field of cortical cells as well as across different cells could contribute to the neural processing of temporally structured stimuli like speech and animal vocalizations.


2007 ◽  
Vol 98 (6) ◽  
pp. 3461-3472 ◽  
Author(s):  
Lars Holmstrom ◽  
Patrick D. Roberts ◽  
Christine V. Portfors

Neurons in the inferior colliculus (IC) of the mustached bat integrate input from multiple frequency bands in a complex fashion. These neurons are important for encoding the bat's echolocation and social vocalizations. The purpose of this study was to quantify the contribution of complex frequency interactions on the responses of IC neurons to social vocalizations. Neural responses to single tones, two-tone pairs, and social vocalizations were recorded in the IC of the mustached bat. Three types of data driven stimulus-response models were designed for each neuron from single tone and tone pair stimuli to predict the responses of individual neurons to social vocalizations. The first model was generated only using the neuron's primary frequency tuning curve, whereas the second model incorporated the entire hearing range of the animal. The extended model often predicted responses to many social vocalizations more accurately for multiply tuned neurons. One class of multiply tuned neuron that likely encodes echolocation information also responded to many of the social vocalizations, suggesting that some neurons in the mustached bat IC have dual functions. The third model included two-tone frequency tunings of the neurons. The responses to vocalizations were better predicted by the two-tone models when the neuron had inhibitory frequency tuning curves that were not near the neuron's primary tuning curve. Our results suggest that complex frequency interactions in the IC determine neural responses to social vocalizations and some neurons in IC have dual functions that encode both echolocation and social vocalization signals.


1978 ◽  
Vol 74 (1) ◽  
pp. 83-100 ◽  
Author(s):  
R. R. Fay ◽  
W. A. Ahroon ◽  
A. A. Orawski

The masking effects of tones on the detection auditory signals were studied in goldfish using the psychophysical tuning-curve paradigm. For signals below 350 Hz, masking is an inverse function of the frequency separation between masker and signal; a finding consistent with previous masking studies on fishes, birds and mammals. For signals above 350 Hz, masking peaks occur both in the 350 Hz region and at the frequency of the signal. Quantitative comparisons with recent neural tuning curves for goldfish saccular neurones suggest that the filtering observed may be determined by mechanical frequency selectivity below 350 Hz, but by a neural analysis of temporal patterns above this range.


2001 ◽  
Vol 85 (5) ◽  
pp. 2245-2266 ◽  
Author(s):  
A. Takemura ◽  
Y. Inoue ◽  
K. Kawano ◽  
C. Quaia ◽  
F. A. Miles

Single-unit discharges were recorded in the medial superior temporal area (MST) of five behaving monkeys. Brief (230-ms) horizontal disparity steps were applied to large correlated or anticorrelated random-dot patterns (in which the dots had the same or opposite contrast, respectively, at the two eyes), eliciting vergence eye movements at short latencies [65.8 ± 4.5 (SD) ms]. Disparity tuning curves, describing the dependence of the initial vergence responses (measured over the period 50–110 ms after the step) on the magnitude of the steps, resembled the derivative of a Gaussian, the curves obtained with correlated and anticorrelated patterns having opposite sign. Cells with disparity-related activity were isolated using correlated stimuli, and disparity tuning curves describing the dependence of these initial neuronal responses (measured over the period of 40–100 ms) on the magnitude of the disparity step were constructed ( n = 102 cells). Using objective criteria and the fuzzy c-means clustering algorithm, disparity tuning curves were sorted into four groups based on their shapes. A post hoc comparison indicated that these four groups had features in common with four of the classes of disparity-selective neurons in striate cortex, but three of the four groups appeared to be part of a continuum. Most of the data were obtained from two monkeys, and when the disparity tuning curves of all the individual neurons recorded from either monkey were summed together, they fitted the disparity tuning curve for that same animal's vergence responses remarkably well ( r 2: 0.93, 0.98). Fifty-six of the neurons recorded from these two monkeys were also tested with anticorrelated patterns, and all showed significant modulation of their activity ( P < 0.005, 1-way ANOVA). Further, when all of the disparity tuning curves obtained with these patterns from either monkey were summed together, they too fitted the disparity tuning curve for that same animal's vergence responses very well ( r 2: 0.95, 0.96). Indeed, the summed activity even reproduced idiosyncratic differences in the vergence responses of the two monkeys. Based on these and other observations on the temporal coding of events, we hypothesize that the magnitude, direction, and time course of the initial vergence velocity responses associated with disparity steps applied to large patterns are all encoded in the summed activity of the disparity-sensitive cells in MST. Latency data suggest that this activity in MST occurs early enough to play an active role in the generation of vergence eye movements at short latencies.


2005 ◽  
Vol 93 (1) ◽  
pp. 71-83 ◽  
Author(s):  
Jun Yan ◽  
Yunfeng Zhang ◽  
Günter Ehret

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.


2020 ◽  
Author(s):  
Shawn M. Willett ◽  
Jennifer M. Groh

AbstractHow we distinguish multiple simultaneous stimuli is uncertain, particularly given that such stimuli sometimes recruit largely overlapping populations of neurons. One hypothesis is that tuning curves might change to limit the number of stimuli driving any given neuron when multiple stimuli are present. To test this hypothesis, we recorded the activity of neurons in the inferior colliculus while monkeys localized either one or two simultaneous sounds differing in frequency. Although monkeys easily distinguished simultaneous sounds (∼90% correct performance), the frequency tuning of inferior colliculus neurons on dual sound trials did not improve in any obvious way. Frequency selectivity was degraded on dual sound trials compared to single sound trials: tuning curves broadened, and frequency accounted for less of the variance in firing rate. These tuning curve changes led a maximum-likelihood decoder to perform worse on dual sound trials than on single sound trials. These results fail to support the hypothesis that changes in frequency response functions serve to reduce the overlap in the representation of simultaneous sounds. Instead these results suggest alternative theories, such as recent evidence of alternations in firing rate between the rates corresponding to each of the two stimuli, offer a more promising approach.


1991 ◽  
Vol 65 (3) ◽  
pp. 693-701 ◽  
Author(s):  
G. M. Koschorke ◽  
R. A. Meyer ◽  
D. B. Tillman ◽  
J. N. Campbell

1. The responses to mechanical stimulation of myelinated fibers that originate from an acutely cut nerve or a neuroma were studied in the anesthetized monkey. The superficial radial or sural nerve was tightly ligated and cut. Either immediately (acute experiment) or 2-6 wk later (chronic experiment), single-unit recording techniques were used to record the evoked neural activity after vibratory mechanical stimulation (5-100 Hz; 50-800 microns) near the injury site. 2. The 30 myelinated afferents studied in the chronic experiments displayed an entrained response (1 action potential for each stimulus cycle) to vibratory stimuli applied at or near the nerve injury site. For 19 fibers, the minimum amplitude for entrainment was determined as a function of frequency (tuning curve). For 11 others, complete tuning curves were not obtained, although the frequency range over which they were most sensitive could be estimated. The afferents could be classified into three groups on the basis of the frequency range over which they were most sensitive: 1) a low-frequency group that was most sensitive to frequencies less than or equal to 5 Hz (n = 7), 2) a mid-frequency group that was most sensitive to a broad range of frequencies (i.e., 20-75 Hz, n = 13), and 3) a high-frequency group that was most sensitive to frequencies greater than or equal to 100 Hz (n = 10). These three response classes are similar to the three classes of response associated with the different low-threshold mechanoreceptors (i.e., slowly and rapidly adapting and Pacinian-like mechanoreceptors).(ABSTRACT TRUNCATED AT 250 WORDS)


2022 ◽  
Author(s):  
Julien Besle ◽  
Rosa-Maria Sánchez-Panchuelo ◽  
Susan Francis ◽  
Katrin Krumbholz

Frequency selectivity is a ubiquitous property of auditory neurons. Measuring it in human auditory cortex may be crucial for understanding common auditory deficits, but current non-invasive neuroimaging techniques can only measure the aggregate response of large populations of cells, thereby overestimating tuning width. Here we attempted to estimate neuronal frequency tuning in human auditory cortex using a combination of fMRI-adaptation paradigm at 7T and computational modelling. We measured the BOLD response in the auditory cortex of eleven participants to a high frequency (3.8 kHz) probe presented alone or preceded by adaptors at different frequencies (0.5 to 3.8 kHz). From these data, we derived both the response tuning curves (the BOLD response to adaptors alone as a function of adaptor frequency) and adaptation tuning curves (the degree of response suppression to the probe as a function of adaptor frequency, assumed to reflect neuronal tuning) in primary and secondary auditory cortical areas, delineated in each participant. Results suggested the existence of both frequency-independent and frequency-specific adaptation components, with the latter being more frequency-tuned than response tuning curves. Using a computational model of neuronal adaptation and BOLD non-linearity in topographically-organized cortex, we demonstrate both that the frequency-specific adaptation component overestimates the underlying neuronal frequency tuning and that frequency-specific and frequency-independent adaptation component cannot easily be disentangled from the adaptation tuning curve. By fitting our model directly to the response and adaptation tuning curves, we derive a range of plausible values for neuronal frequency tuning. Our results suggest that fMRI adaptation is suitable for measuring neuronal frequency tuning properties in human auditory cortex, provided population effects and the non-linearity of BOLD response are taken into account.


1997 ◽  
Vol 77 (4) ◽  
pp. 2098-2114 ◽  
Author(s):  
Nobuo Suga ◽  
Yunfeng Zhang ◽  
Jun Yan

Suga, N., Y. Zhang, and J. Yan. Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. J. Neurophysiol. 77: 2098–2114, 1997. Unlike the quasitriangular frequency-tuning curves of peripheral neurons, pencil- or spindle-shaped frequency-tuning curves (excitatory areas) have been found in the central auditory systems of many species of animals belonging to different classes. Inhibitory tuning curves (areas) are commonly found on both sides of such “level-tolerant” sharp frequency-tuning curves. However, it has not yet been examined whether sharpening of frequency tuning takes place in the medial geniculate body (MGB). We injected an inhibitory transmitter antagonist, bicuculline methiodide (BMI), into the MGB of the mustached bat to examine whether frequency tuning is sharpened by inhibition in the MGB and whether this sharpening, if any, occurs in addition to that performed in prethalamic auditory nuclei. Thirty-seven percent of thalamic Doppler-shifted constant frequency (DSCF) neurons mostly showing a level-tolerant frequency-tuning curve had an inhibitory area or areas. BMI changed the inhibitory areas of these neurons into excitatory areas, so that their excitatory frequency-tuning curves became broader. However, the BMI-broadened excitatory frequency-tuning curves were still much narrower than those of peripheral neurons. Our results indicate that level-tolerant frequency tuning of thalamic DSCF neurons is mostly created by prethalamic auditory nuclei and that it is further sharpened in 37% of thalamic DSCF neurons by lateral inhibition occurring in the MGB. The comparisons in sharpness (quality factors) of frequency-tuning curves between peripheral, thalamic, and cortical DSCF neurons indicate that the skirt portion of tuning curves is sharper in the above order, and that their tip portion is not significantly different between the peripheral and thalamic DSCF neurons, but significantly sharper in the cortical DSCF neurons than in the thalamic DSCF neurons. Therefore the central auditory system has inhibitory mechanisms for the progressive sharpening of frequency tuning. DSCF neurons in the primary auditory cortex were recently found to show facilitative responses to paired sounds. That is, they are combination sensitive. In the present studies, we found that thalamic DSCF neurons also showed facilitative responses to paired sounds. The responses of thalamic DSCF neurons to acoustic stimuli consisted of a slow and a fast component. BMI mainly increased the slow component and an excitatory transmitter antagonist, d-2-amino-5-phosphonovalerate mainly suppressed the slow component. Therefore the response pattern of these thalamic neurons is shaped by both γ-aminobutyric acid-mediated inhibition and N-methyl-d-aspartate-mediated facilitation.


Sign in / Sign up

Export Citation Format

Share Document