Spatial Tuning to Virtual Sounds in the Inferior Colliculus of the Guinea Pig

2003 ◽  
Vol 90 (4) ◽  
pp. 2648-2659 ◽  
Author(s):  
Susanne J. Sterbing ◽  
Klaus Hartung ◽  
Klaus-Peter Hoffmann

How do neurons in the inferior colliculus (IC) encode the spatial location of sound? We have addressed this question using a virtual auditory environment. For this purpose, the individual head-related transfer functions (HRTFs) of 18 guinea pigs were measured under free-field conditions for 122 locations covering the upper hemisphere. From 257 neurons, 94% responded to the short (50-ms) white noise stimulus at 70 dB sound pressure level (SPL). Out of these neurons, 80% were spatially tuned with a receptive field that is smaller than a hemifield (at 70 dB). The remainder responded omnidirectionally or showed fractured receptive fields. The majority of the neurons preferred directions in the contralateral hemisphere. However, preference for front or rear positions and high elevations occurred frequently. For stimulation at 70 dB SPL, the average diameter of the receptive fields, based on half-maximal response, was less than a quarter of the upper hemisphere. Neurons that preferred frontal directions responded weakly or showed no response to posterior directions and vice versa. Hence, front/back discrimination is present at the single-neuron level in the IC. When nonindividual HRTFs were used to create the stimuli, the spatial receptive fields of most neurons became larger, split into several parts, changed position, or the response became omnidirectional. Variation of absolute sound intensity had little effect on the preferred directions of the neurons over a range of 20 to 40 dB above threshold. With increasing intensity, most receptive fields remained constant or expanded. Furthermore, we tested the influence of binaural decorrelation and stimulus bandwidth on spatial tuning. The vast majority of neurons with a low characteristic frequency (<2.5 kHz) lost spatial tuning under stimulation with binaurally uncorrelated noise, whereas high-frequency units were mostly unaffected. Most neurons that showed spatial tuning under broadband stimulation (white noise and 1 octave wide noise) turned omnidirectional when stimulated with 1/3 octave wide noise.

1999 ◽  
Vol 81 (6) ◽  
pp. 2833-2851 ◽  
Author(s):  
Bertrand Delgutte ◽  
Philip X. Joris ◽  
Ruth Y. Litovsky ◽  
Tom C. T. Yin

Receptive fields and binaural interactions for virtual-space stimuli in the cat inferior colliculus. Sound localization depends on multiple acoustic cues such as interaural differences in time (ITD) and level (ILD) and spectral features introduced by the pinnae. Although many neurons in the inferior colliculus (IC) are sensitive to the direction of sound sources in free field, the acoustic cues underlying this sensitivity are unknown. To approach this question, we recorded the responses of IC cells in anesthetized cats to virtual space (VS) stimuli synthesized by filtering noise through head-related transfer functions measured in one cat. These stimuli not only possess natural combinations of ITD, ILD, and spectral cues as in free field but also allow precise control over each cue. VS receptive fields were measured in the horizontal and median vertical planes. The vast majority of cells were sensitive to the azimuth of VS stimuli in the horizontal plane for low to moderate stimulus levels. Two-thirds showed a “contra-preference” receptive field, with a vigorous response on the contralateral side of an edge azimuth. The other third of receptive fields were tuned around a best azimuth. Although edge azimuths of contra-preference cells had a broad distribution, best azimuths of tuned cells were near the midline. About half the cells tested were sensitive to the elevation of VS stimuli along the median sagittal plane by showing either a peak or a trough at a particular elevation. In general receptive fields for VS stimuli were similar to those found in free-field studies of IC neurons, suggesting that VS stimulation provided the essential cues for sound localization. Binaural interactions for VS stimuli were studied by comparing responses to binaural stimulation with responses to monaural stimulation of the contralateral ear. A majority of cells showed either purely inhibitory (BI) or mixed facilitatory/inhibitory (BF&I) interactions. Others showed purely facilitatory (BF) or no interactions (monaural). Binaural interactions were correlated with azimuth sensitivity: most contra-preference cells had either BI or BF&I interactions, whereas tuned cells were usually BF. These correlations demonstrate the importance of binaural interactions for azimuth sensitivity. Nevertheless most monaural cells were azimuth-sensitive, suggesting that monaural cues also play a role. These results suggest that the azimuth of a high-frequency sound source is coded primarily by edges in azimuth receptive fields of a population of ILD-sensitive cells.


1987 ◽  
Vol 57 (3) ◽  
pp. 688-701 ◽  
Author(s):  
J. C. Middlebrooks

This study explores the mechanisms of auditory spatial tuning in the superior colliculus of the anesthetized cat by correlating spatial tuning within specific regions of space with particular types of binaural interaction. The auditory spatial tuning of units was measured using a movable, broad-band stimulus presented in a free sound field. The contribution of each ear to the response of a unit was identified by acutely plugging one or the other ear. Every unit became largely or entirely unresponsive when a foam-rubber earplug was placed in the ear contralateral to the recording site. Thus, every unit exhibited an excitatory or facilitatory influence from the contralateral ear. A plug placed in the ipsilateral ear had different effects on different units. For half of the units (16/32), an ipsilateral earplug produced increases in the sizes of the units' receptive fields and increases in the magnitudes of their responses to stimuli presented from most locations. Thus, these units exhibited inhibition from the ipsilateral ear. Another class of units (9/32) exhibited ipsilateral facilitation, in that an ipsilateral earplug caused decreases in the sizes of the units' receptive fields and prominent decreases in their response magnitudes. For the remaining units (7/32), an ipsilateral earplug resulted in decreases in the sizes of the units' receptive fields, but produced both decreases in the responses of units to stimuli presented in their best areas and increases in the responses to stimuli presented away from the best areas. Thus these units exhibited mixed facilitatory and inhibitory ipsilateral influences. The influence of an ipsilateral earplug on a unit's response tended to correlate with its spatial tuning. The region of space within which a sound source was most effective in activating a unit was its “best area”. The best areas of units exhibiting ipsilateral inhibition were located furthest peripherally, those of units showing ipsilateral facilitation were located furthest frontally, and the best areas of units showing mixed ipsilateral influences were located in an intermediate area. The frequency tuning of units measured using a free-field tone source also tended to correlate with the locations of their best areas. Half of the units tested (27/54) responded to tones of the sound pressure levels (SPLs) that were used (up to 50 dB SPL).(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 60 (4) ◽  
pp. 1369-1383 ◽  
Author(s):  
J. J. Wenstrup ◽  
Z. M. Fuzessery ◽  
G. D. Pollak

1. Single-unit responses to closed-field, dichotic sound stimuli were obtained from EI neurons in the mustache bat's inferior colliculus; these neurons are excited by sound to the contralateral ear and inhibited by sound to the ipsilateral ear. All units were tuned to the 60-kHz component of the bat's sonar signal. The goal of the study was to describe basic features of the sensitivity to interaural intensity differences (IIDs) and sound intensity among an isofrequency population of EI neurons. The following paper describes how these features of IID sensitivity shape the response to free-field sounds. 2. Three features of IID sensitivity were considered. The inhibitory threshold (Figs. 1 and 2) described the IID at which inhibitory effects became pronounced; it was defined as the IID at which the excitatory response to contralateral sound was suppressed by 50%. Most units (68%) were inhibited at positive IID values, for which the ipsilateral (inhibitory) sound was more intense. The maximum inhibition (Figs. 1 and 3) described the strength of ipsilateral inhibition; it was defined as the percent that each unit was inhibited below its response to monaural stimulation of the contralateral ear. The majority of units (58%) were almost totally suppressed by a sufficiently intense ipsilateral sound. The IID range (Figs. 1 and 4) described the sharpness or slope of the IID cutoff; it was defined as the IID range over which the response changed from nearly unsuppressed (80% of maximum response) to near maximum suppression (20% of maximum response). Most units (71%) had IID ranges of less than or equal to 15 dB. 3. A significant correlation between the inhibitory threshold and the maximum inhibition (Fig. 5) among the sample of EI units suggests that some common neural mechanisms underlie these features of IID sensitivity. 4. The response of EI neurons to binaural stimuli was a function of sound intensity as well as IID (Fig. 7). In part, this resulted from intensity-dependent changes in properties of binaural inhibition. For most units, basic measures of IID sensitivity changed to a limited extent as the sound intensity changed.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 60 (4) ◽  
pp. 1384-1404 ◽  
Author(s):  
J. J. Wenstrup ◽  
Z. M. Fuzessery ◽  
G. D. Pollak

1. The responses to closed-field and free-field sound stimuli were obtained from EI neurons in the 60-kHz isofrequency representation of the mustache bat's inferior colliculus. The goals of the study were 1) to examine how binaural interactions and the directional properties of the ear shape the spatial response of 60-kHz EI neurons and 2) to examine features of the spatial responses of these isofrequency neurons which may encode the location of a sound. 2. The free-field response of monaural neurons was used to describe directional effects of the head and external ears at 60 kHz. Monaural neurons were most sensitive to sounds originating 26 degrees into the contralateral field, with sharply reduced sensitivity in the ipsilateral field and the lateral extreme of the contralateral field. The interaural intensity difference (IID), computed by assuming that the ears had mirror-image directional sensitivities, was greatest for sounds between 26 and 52 degrees off the vertical midline, where IIDs typically ranged from 20 to 30 dB. These values agree well with previous measures of the directional sensitivity of the ear obtained from cochlear microphonic recordings. 3. The response of a monaural unit to closed-field stimulation was used to predict its response to free-field stimulation. This prediction agreed closely with the observed free-field response, indicating that the monaural unit's free-field response could be explained by the directional sensitivity of the contralateral ear and the unit's response as a function of contralateral sound intensity. 4. EI neurons differed in basic features of their binaural response properties, as described in a companion paper. To examine how these features of binaural inhibition shaped spatial responses, we obtained responses to free-field sounds among neurons whose binaural properties had been thoroughly characterized. We then compared the spatial response to a prediction based upon the directional properties of the ear and the sensitivity of the EI neurons to IIDs and intensity. The close agreement between the observed and predicted spatial responses in 11 of 12 EI units indicated that the spatial responses were determined largely by sensitivity to IIDs and intensity and by the directional properties of the ear. 5. EI neurons in our sample were most sensitive, and responded best, to sounds originating 26-39 degrees into the contralateral field. These spatial response features were independent of the binaural properties of EI neurons. Instead, they depended upon the directional properties of the ears at 60 kHz.(ABSTRACT TRUNCATED AT 400 WORDS)


2002 ◽  
Vol 87 (2) ◽  
pp. 976-994 ◽  
Author(s):  
R. Y. Litovsky ◽  
B. Delgutte

The precedence effect (PE) is an auditory phenomenon involved in suppressing the perception of echoes in reverberant environments, and is thought to facilitate accurate localization of sound sources. We investigated physiological correlates of the PE in the inferior colliculus (IC) of anesthetized cats, with a focus on directional mechanisms for this phenomenon. We used a virtual space (VS) technique, where two clicks (a “lead” and a “lag”) separated by a brief time delay were each filtered through head-related transfer functions (HRTFs). For nearly all neurons, the response to the lag was suppressed for short delays and recovered at long delays. In general, both the time course and the directional patterns of suppression resembled those reported in free-field studies in many respects, suggesting that our VS simulation contained the essential cues for studying PE phenomena. The relationship between the directionality of the response to the lead and that of its suppressive effect on the lag varied a great deal among IC neurons. For a majority of units, both excitation produced by the lead and suppression of the lag response were highly directional, and the two were similar to one another. For these neurons, the long-lasting inhibitory inputs thought to be responsible for suppression seem to have similar spatial tuning as the inputs that determine the excitatory response to the lead. Further, the behavior of these neurons is consistent with psychophysical observations that the PE is strongest when the lead and the lag originate from neighboring spatial locations. For other neurons, either there was no obvious relationship between the directionality of the excitatory lead response and the directionality of suppression, or the suppression was highly directional whereas the excitation was not, or vice versa. For these neurons, the excitation and the suppression produced by the lead seem to depend on different mechanisms. Manipulation of the directional cues (such as interaural time and level differences) contained in the lead revealed further dissociations between excitation and suppression. Specifically, for about one-third of the neurons, suppression depended on different directional cues than did the response to the lead, even though the directionality of suppression was similar to that of the lead response when all cues were present. This finding suggests that the inhibitory inputs causing suppression may originate in part from subcollicular auditory nuclei processing different directional cues than the inputs that determine the excitatory response to the lead. Neurons showing such dissociations may play an important role in the PE when the lead and the lag originate from very different directions.


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)


2001 ◽  
Vol 85 (1) ◽  
pp. 23-33 ◽  
Author(s):  
Neil J. Ingham ◽  
Heledd C. Hart ◽  
David McAlpine

We examined responses from 91 single-neurons in the inferior colliculus (IC) of anesthetized guinea pigs to auditory apparent motion in the free field. Apparent motion was generated by presenting 100-ms tone bursts, separated by 50-ms silent intervals, at consecutive speaker positions in an array of 11 speakers, positioned in an arc ±112.5° around midline. Most neurons demonstrated discrete spatial receptive fields (SRFs) to apparent motion in the clockwise and anti-clockwise directions. However, SRFs showed marked differences for apparent motion in opposite directions. In virtually all neurons, mean best azimuthal positions for SRFs to opposite directions occurred at earlier positions in the motion sweep, producing receptive fields to the two directions of motion that only partially overlapped. Despite this, overall spike counts to the two directions were similar for equivalent angular velocities. Responses of 28 neurons were recorded to stimuli with different duration silent intervals between speaker presentations, mimicking different apparent angular velocities. Increasing the stimulus off time increased neuronal discharge rates, particularly at later portions of the apparent motion sweep, and reduced the differences in the SRFs to opposite motion directions. Consequently SRFs to both directions broadened and converged with decreasing motion velocity. This expansion was most obvious on the outgoing side of the each SRF. Responses of 11 neurons were recorded to short (90°) partially overlapping apparent motion sweeps centered at different spatial positions. Nonoverlapping response profiles were recorded in 9 of the 11 neurons tested and confirmed that responses at each speaker position were dependent on the preceding response history. Together these data are consistent with the suggestion that a mechanism of adaptation of excitation contributes to the apparent sensitivity of IC neurons to auditory motion cues. In addition, the data indicate that the sequential activation of an array of speakers to produce apparent auditory motion may not be an optimal stimulus paradigm to separate the temporal and spatial aspects of auditory motion processing.


2004 ◽  
Vol 92 (5) ◽  
pp. 3014-3029 ◽  
Author(s):  
Oliver Behrend ◽  
Benjamin Dickson ◽  
Elizabeth Clarke ◽  
Craig Jin ◽  
Simon Carlile

Virtual auditory space (VAS) stimuli based on outer ear transfer functions became increasingly important in spatial hearing research. However, few studies have investigated the match between responses of auditory neurons to VAS and free-field (FF) stimulation. This study validates acoustic spatial receptive fields (SRFs) of 183 individual midbrain units using both VAS and FF stimuli. The first-spike latency, which varied systematically across SRFs, was 14.9 ± 8.3 (SD) ms in FF, and 15.1 ± 8.3 ms in VAS. Spike-count-based SRFs measured 0–20 dB above the neural threshold covered on average 44.5 ± 18.0% of the recorded sphere in FF and 45.5 ± 18.7% in VAS. The average deviation of the centroid position of SRFs using FF and VAS stimuli was 7.4° azimuth and 3.3° elevation. The average spike rate remained unchanged. The SRF overlap recorded using FF and VAS stimuli (mean: 71.3 ± 12.6%) or repeated FF stimuli (70.2 ± 14.2%) was high and strongly correlated ( r = 0.96; P < 0.05). The SRF match observed with FF and VAS stimuli was not significantly altered over a range of stimulus levels (paired t-test P = 0.51; n = 6). Randomized VAS barely affected SRF sizes, centroids, or maximum spike count but decreased the average minimum response to 59% compared with sequential stimulation (paired t-test; P = 0.05; n = 26). SRF recordings in VAS excluding the acoustic distortions of the recording equipment differed from those in VAS incorporating the equipment (paired t-test P = 0.01; n = 5). In conclusion, neurophysiological recordings demonstrate that individualized VAS stimuli provided a good simulation of a FF environment.


1984 ◽  
Vol 52 (4) ◽  
pp. 709-723 ◽  
Author(s):  
E. I. Knudsen

Auditory units in the optic tectum of the barn owl (Tyto alba) were studied under free-field conditions with a movable sound source. These units are selective for sound location and their spatial tuning varies systematically across the tectum, forming a map of space (8). I found that frequency tuning, response latencies, and thresholds of units changed in parallel with their spatial tuning, suggesting that as a consequence these properties also are topographically distributed in the optic tectum. Response rates were determined primarily by the location of the sound source. Regardless of sound intensity, only stimuli delivered from a restricted “best area” elicited vigorous responses. Minimum response latencies were shortest for units with frontal best areas and increased systematically for units with best areas located more peripherally. The response latencies of units with best areas centered within 25 degrees of the owl's visual axis were virtually independent of sound intensity and speaker position. The latencies of units with more peripheral best areas varied with speaker position and were shortest when the speaker was in the best area. Thresholds to noise stimuli were lowest for units with best areas directly in front of the owl and increased systematically for units with best areas located more peripherally. Thus, in the representation of frontal space, where units have the smallest receptive fields and the magnification of space is the greatest (8), units also respond to the weakest sound fields. Many units (20%) could not be driven with tonal stimuli; of those that could, most were broadly tuned for frequency. Characteristic frequencies and high-frequency cutoffs shifted lower as best areas moved peripherally. High-frequency tones, which excited units with frontal best areas, either inhibited or failed to drive units with peripheral best areas. These systematic changes in unit response properties influence how sounds from different locations are represented in the tectum and reflect integrative strategies used by the owl's auditory system in deriving a representation of auditory space.


2010 ◽  
Vol 103 (5) ◽  
pp. 2642-2651 ◽  
Author(s):  
Joshua P. van Kleef ◽  
Gert Stange ◽  
Michael R. Ibbotson

Motion processing in visual neurons is often understood in terms of how they integrate light stimuli in space and time. These integrative properties, known as the spatiotemporal receptive fields (STRFs), are sometimes obtained using white-noise techniques where a continuous random contrast sequence is delivered to each spatial location within the cell's field of view. In contrast, motion stimuli such as moving bars are usually presented intermittently. Here we compare the STRF prediction of a neuron's response to a moving bar with the measured response in second-order interneurons (L-neurons) of dragonfly ocelli (simple eyes). These low-latency neurons transmit sudden changes in intensity and motion information to mediate flight and gaze stabilization reflexes. A white-noise analysis is made of the responses of L-neurons to random bar stimuli delivered either every frame (densely) or intermittently (sparsely) with a temporal sequence matched to the bar motion stimulus. Linear STRFs estimated using the sparse stimulus were significantly better at predicting the responses to moving bars than the STRFs estimated using a traditional dense white-noise stimulus, even when second-order nonlinear terms were added. Our results strongly suggest that visual adaptation significantly modifies the linear STRF properties of L-neurons in dragonfly ocelli during dense white-noise stimulation. We discuss the ability to predict the responses of visual neurons to arbitrary stimuli based on white-noise analysis. We also discuss the likely functional advantages that adaptive receptive field structures provide for stabilizing attitude during hover and forward flight in dragonflies.


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