Coding for Auditory Space in the Nucleus of the Brachium of the Inferior Colliculus in the Ferret

1997 ◽  
Vol 78 (5) ◽  
pp. 2717-2731 ◽  
Author(s):  
Jan W. H. Schnupp ◽  
Andrew J. King

Schnupp, Jan W. H. and Andrew J. King. Coding for auditory space in the nucleus of the brachium of the inferior colliculus in the ferret. J. Neurophysiol. 78: 2717–2731, 1997. The nucleus of the brachium of the inferior colliculus (BIN) projects topographically to the deeper layers of the superior colliculus (SC), which contain a two-dimensional map of auditory space. In this study, we have used broadband stimuli presented in the free field to investigate how auditory space is represented in the BIN of the ferret. Response latencies and temporal firing patterns were comparable with those in the SC, and both properties showed some variation with stimulus location. We obtained spatial response profiles at two sound levels (5–15 and 25–35 dB above unit threshold). A large proportion of azimuth profiles (41% in the suprathreshold condition, 80% in the near-threshold condition) presented a single peak, indicating that they were tuned to single regions in space. For some of these units, the preferred speaker position varied considerably with sound level. The remaining units showed predominantly either broad “hemifield” or spatially ambiguous “bilobed” response profiles. At suprathreshold sound levels, the preferred azimuths of the tuned cells were ordered topographically along the rostrocaudal axis of the BIN, although this representation is considerably more scattered than that in the SC. In contrast to the SC, we observed no systematic variation in the distribution of near-threshold best azimuths, which were instead concentrated around the interaural axis in the contralateral hemifield. The azimuth tuning of individual units in the BIN was generally broader at both sound levels than that in the SC. Many units also were tuned for the elevation of the sound source (48% for supra-, 77% for near-threshold stimulation), but there was no evidence for topographic order in the distribution of preferred elevations within the BIN. These results suggest that the BIN sends inputs to the SC that are already selective for sound azimuth and elevation and that show some degree of topographic order for sound azimuth. These inputs then presumably are sharpened and their topography refined by a mechanism that is likely to involve convergence of other inputs and activity-dependent fine tuning of terminal connections, to result in a precise two-dimensional map of auditory space in the SC.

1994 ◽  
Vol 71 (1) ◽  
pp. 182-194 ◽  
Author(s):  
A. J. King ◽  
D. R. Moore ◽  
M. E. Hutchings

1. We have investigated the role of monaural cues provided by the outer ear in the construction of a map of auditory space in the superior colliculus. Single-unit recordings were made from the superior colliculus of adult ferrets that were deprived of binaural inputs by surgically ablating the ipsilateral cochlea on postnatal day 21 or 24. 2. The spatial response properties of auditory units in the deeper layers of this nucleus were studied using white-noise bursts presented under free-field conditions in an anechoic chamber. The thresholds of the units recorded in the monaural ferrets were not significantly different from those recorded in the superior colliculus of normal adult ferrets. In both groups the unit thresholds varied by 30-50 dB in each region of the superior colliculus. 3. In normal and monaural ferrets the elevation tuning tended to be sharper than the azimuth tuning. At sound levels of approximately 10 dB above threshold the auditory units recorded in both groups of animals were tuned to a specific region of space that was restricted in azimuth and elevation. The spatial location at which the maximum response was obtained (auditory best position) varied topographically in azimuth along the rostrocaudal axis of the nucleus and in elevation along the mediolateral axis. 4. The azimuthal distribution of best positions associated with each recording location in the superior colliculus of the monaural ferrets and the alignment between this dimension of the auditory map and that of the visual map in the overlying superficial layers were no different from those found at corresponding near-threshold sound levels in normal ferrets. 5. Elevation spatial selectivity was examined in a smaller sample of units. Although elevation best positions shifted downward from the medial to the lateral side of the nucleus in both normal and monaural ferrets, we found that the topography of the auditory representation and its alignment with the visual representation were statistically different in the two groups of animals. 6. Increasing the sound level does not affect the representation of auditory space in normal ferrets. However, when the stimulus level presented to monoaural ferrets was increased, the receptive fields either expanded so that the responses were no longer tuned to any particular region of space, or the responses remained tuned but exhibited a marked shift in the value of the best position.(ABSTRACT TRUNCATED AT 400 WORDS)


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.


2019 ◽  
Author(s):  
Björn Herrmann ◽  
Thomas Augereau ◽  
Ingrid S. Johnsrude

AbstractSensitivity to sound-level statistics is crucial for optimal perception, but research has focused mostly on neurophysiological recordings, whereas behavioral evidence is sparse. We use electroencephalography (EEG) and behavioral methods to investigate how sound-level statistics affect neural activity and the detection of near-threshold changes in sound amplitude. We presented noise bursts with sound levels drawn from distributions with either a low or a high modal sound level. One participant group listened to the stimulation while EEG was recorded (Experiment I). A second group performed a behavioral amplitude-modulation detection task (Experiment II). Neural activity depended on sound-level statistical context in two different ways. Consistent with an account positing that the sensitivity of neurons to sound intensity adapts to ambient sound level, responses for higher-intensity bursts were larger in low-mode than high-mode contexts, whereas responses for lower-intensity bursts did not differ between contexts. In contrast, a concurrent slow neural response indicated prediction-error processing: The response was larger for bursts at intensities that deviated from the predicted statistical context compared to those not deviating. Behavioral responses were consistent with prediction-error processing, but not with neural adaptation. Hence, neural activity adapts to sound-level statistics, but fine-tuning of perceptual sensitivity appears to involve neural prediction-error responses.


1991 ◽  
Vol 65 (2) ◽  
pp. 383-392 ◽  
Author(s):  
L. Aitkin

1. The responses as a function of stimulus level of 125 single units in the inferior colliculus of anesthetized cats were studied with the use of free-field acoustic stimuli. 2. The characteristic frequency (CF; frequency at which threshold was lowest) of each unit was determined, and stimuli were presented from one of three speaker positions: 45 degrees contralateral to the midline, midline, and 45 degrees ipsilateral to the midline. 3. For each unit a variety of stimulus levels was presented at CF, and the total spike count was summed for 20 stimuli at each level. If time permitted, a similar series of levels of noise was presented. 4. Four classes of rate-level (RL) functions were observed. Monotonic increases in firing rate were observed in 10% of units stimulated with CF stimuli and 57% of units studied with noise. Nonmonotonic RL functions, for which firing first increased and then declined to less than 50% of the peak level, were observed in 61% of units responding to CF tones and in 10% responding to noise. Plateau functions, with shapes lying between these, accounted for 19% of CF responses and the remaining units excited by noise. Some very complex shapes that could not be categorized into the above groups were seen in the remaining 10% of the units responding to CF stimuli. 5. The RL functions of units studied with both noise and CF tones could belong to different classes; commonly, nonmonotonic RL functions to tones were associated with monotonic RL functions to noise. The noise thresholds averaged 10 dB, some 10-20 dB less sensitive than those to CF stimuli. 6. For the vast majority of both noise and tone responses, stimuli from the contralateral location were more effective than those from the other two positions in terms of a lower threshold, higher peak discharge rate, and, for nonmonotonic units, a lower sound level at which the function became nonmonotonic (turnover point). 7. The turnover points of nonmonotonic functions at any given CF could be spread broadly but, overall, tended to be concentrated between -6 and 44 dB. 8. The dynamic ranges (range of levels over which firing rate increased) were larger for monotonic and plateau functions than for nonmonotonic functions, which had dynamic ranges less than 45 dB. The median dynamic range for units stimulated with CF tones was 20 dB and for noise stimuli, 40 dB.(ABSTRACT TRUNCATED AT 400 WORDS)


1994 ◽  
Vol 71 (2) ◽  
pp. 785-801 ◽  
Author(s):  
S. Carlile ◽  
A. J. King

1. The role of the structures of the outer ear in producing monaural and binaural spectral cues to sound location was examined acoustically in the ferret. A probe microphone was introduced across the wall of the external auditory canal and its responses to digitally constructed wideband signals were recorded for a large number of free field locations. 2. In the intact animal the patterns of both monaural and binaural cues were asymmetrical for horizontal locations about the interaural axis. For anterior sound locations the monaural transformations demonstrated relative gains at middle and high frequencies and a location-dependent frequency notch. Changing elevation resulted in variations in the corner frequencies of these spectral features. Additionally, there was greater front-back asymmetry in the binaural spectral cues for locations in lateral space when compared with locations near the midline. 3. Surgical removal of the pinna and concha (pinnectomy) eliminated all the major front-back asymmetrical features in the horizon monaural and binaural spectral transformations as well as the elevation-dependent variations in the monaural spectra. Thus the residual transformations were ambiguous for sound locations in lateral space, resulting in "cones of confusion" centered on the interaural axis. 4. These cues were reflected in the topographic representation of auditory space in the deeper layers of the superior colliculus (SC). Previous studies have shown that spatial tuning at near-threshold sound levels is based on monaural pinna cues, whereas binaural inputs are utilized at higher levels that stimulate both ears. In the intact ferret we examined statistically the topography of the representation of sound azimuth for near-threshold and suprathreshold stimuli and the alignment of the auditory and visual representations in the SC. The distributions of auditory best positions within the SC for near- and suprathreshold stimulus levels were statistically indistinguishable, suggesting that both monaural and binaural cues are integrated in this neural representation of space. 5. Pinnectomy resulted in a large increase in the number of auditory units that responded best to two distinct locations in space. One lobe of the response was tuned appropriately in terms of the position of the unit within the SC, demonstrating that the residual acoustical cues are sufficient for the construction of a topographic representation of auditory space. However, the second region of space, thereby producing an ambiguous representation.(ABSTRACT TRUNCATED AT 400 WORDS)


1998 ◽  
Vol 79 (2) ◽  
pp. 1053-1069 ◽  
Author(s):  
Jan W. H. Schnupp ◽  
Andrew J. King ◽  
Simon Carlile

Schnupp, Jan W. H., Andrew J. King, and Simon Carlile. Altered spectral localization cues disrupt the development of the auditory space map in the superior colliculus of the ferret. J. Neurophysiol. 79: 1053–1069, 1998. Spectral localization cues provided by the outer ear are utilized in the construction of the auditory space map in the superior colliculus (SC). The role of the outer ear in the development of this map was examined by recording from the SC of anesthetized, adult ferrets in which the pinna and concha had been removed in infancy. The acoustical consequences of this procedure were assessed by recording outer ear impulse responses via a probe-tube microphone implanted in the wall of the ear canal. Both monaural and binaural spectral cues normally show a number of asymmetric features within the horizontal plane, which allow azimuthal locations on either side of the interaural axis to be discriminated. These features were eliminated or altered by chronic pinnectomy. The responses of auditory units in the SC to noise bursts presented in the free field were examined at sound levels of ∼10 and 25 dB above unit threshold. After bilateral pinnectomy, the representation of auditory space was severely degraded at both sound levels. In contrast to normal ferrets, many units had bilobed azimuthal response profiles, indicating that they were unable to resolve sound locations on either side of the interaural axis. There was also much less order in the distribution of best azimuths or elevations of those units that were tuned to a single direction. Some units were tuned to locations that extended much further into the hemifield ipsilateral to the recording side than the normal range of best azimuths. Unilateral removal of the outer ear, which disrupts the monaural spectral cues for one side only, had a much smaller effect on the development of the auditory representation. At supra- and near-threshold sound levels, the representation of sound azimuth in the SC on both sides of the brain was less scattered than that found after bilateral pinna removal. Nevertheless, units with bilobed responses, broader tuning, and inappropriate best azimuths were observed in both the left and right SC of ferrets in which the left pinna and concha had been removed in infancy. These data illustrate that the localization cues provided by the outer ear play a critical role in the development of the auditory space map in the SC. In contrast to other manipulations of either auditory or visual inputs, the map does not appear to adapt to the changes in spectral cues brought about by pinna removal, suggesting that residual binaural cues are, by themselves, insufficient for its normal maturation.


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.


1999 ◽  
Vol 82 (1) ◽  
pp. 164-175 ◽  
Author(s):  
Kevin A. Davis ◽  
Ramnarayan Ramachandran ◽  
Bradford J. May

Single units in the central nucleus of the inferior colliculus (ICC) of unanesthetized decerebrate cats can be grouped into three distinct types (V, I, and O) according to the patterns of excitation and inhibition revealed in contralateral frequency response maps. This study extends the description of these response types by assessing their ipsilateral and binaural response map properties. Here the nature of ipsilateral inputs is evaluated directly using frequency response maps and compared with results obtained from methods that rely on sensitivity to interaural level differences (ILDs). In general, there is a one-to-one correspondence between observed ipsilateral input characteristics and those inferred from ILD manipulations. Type V units receive ipsilateral excitation and show binaural facilitation (EE properties); type I and type O units receive ipsilateral inhibition and show binaural excitatory/inhibitory (EI) interactions. Analyses of binaural frequency response maps show that these ILD effects extend over the entire receptive field of ICC units. Thus the range of frequencies that elicits excitation from type V units is expanded with increasing levels of ipsilateral stimulation, whereas the excitatory bandwidth of type I and O units decreases under the same binaural conditions. For the majority of ICC units, application of bicuculline, an antagonist for GABAA-mediated inhibition, does not alter the basic effects of binaural stimulation; rather, it primarily increases spontaneous and maximum discharge rates. These results support our previous interpretations of the putative dominant inputs to ICC response types and have important implications for midbrain processing of competing free-field sounds that reach the listener with different directional signatures.


2021 ◽  
Vol 10 (14) ◽  
pp. 3078
Author(s):  
Sara Akbarzadeh ◽  
Sungmin Lee ◽  
Chin-Tuan Tan

In multi-speaker environments, cochlear implant (CI) users may attend to a target sound source in a different manner from normal hearing (NH) individuals during a conversation. This study attempted to investigate the effect of conversational sound levels on the mechanisms adopted by CI and NH listeners in selective auditory attention and how it affects their daily conversation. Nine CI users (five bilateral, three unilateral, and one bimodal) and eight NH listeners participated in this study. The behavioral speech recognition scores were collected using a matrix sentences test, and neural tracking to speech envelope was recorded using electroencephalography (EEG). Speech stimuli were presented at three different levels (75, 65, and 55 dB SPL) in the presence of two maskers from three spatially separated speakers. Different combinations of assisted/impaired hearing modes were evaluated for CI users, and the outcomes were analyzed in three categories: electric hearing only, acoustic hearing only, and electric + acoustic hearing. Our results showed that increasing the conversational sound level degraded the selective auditory attention in electrical hearing. On the other hand, increasing the sound level improved the selective auditory attention for the acoustic hearing group. In the NH listeners, however, increasing the sound level did not cause a significant change in the auditory attention. Our result implies that the effect of the sound level on selective auditory attention varies depending on the hearing modes, and the loudness control is necessary for the ease of attending to the conversation by CI users.


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