Spatial Receptive Fields of Inferior Colliculus Neurons to Auditory Apparent Motion in Free Field

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.

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Auditory Motion Induces Directionally Dependent Receptive Field Shifts in Inferior Colliculus Neurons

Journal of Neurophysiology ◽

10.1152/jn.1998.79.4.2040 ◽

1998 ◽

Vol 79 (4) ◽

pp. 2040-2062 ◽

Cited By ~ 33

Author(s):

Willard W. Wilson ◽

William E. O'Neill

Keyword(s):

Receptive Field ◽

Inferior Colliculus ◽

Apparent Motion ◽

Target Location ◽

Receptive Fields ◽

Silent Interval ◽

Auditory Motion ◽

Motion Direction ◽

Motion Sequence ◽

And Shifts

Wilson, Willard W. and William E. O'Neill. Auditory motion induces directionally dependent receptive field shifts in inferior colliculus neurons. J. Neurophysiol. 79: 2040–2062, 1998. This research focused on the response of neurons in the inferior colliculus of the unanesthetized mustached bat, Pteronotus parnelli, to apparent auditory motion. We produced the apparent motion stimulus by broadcasting pure-tone bursts sequentially from an array of loudspeakers along horizontal, vertical, or oblique trajectories in the frontal hemifield. Motion direction had an effect on the response of 65% of the units sampled. In these cells, motion in opposite directions produced shifts in receptive field locations, differences in response magnitude, or a combination of the two effects. Receptive fields typically were shifted opposite the direction of motion (i.e., units showed a greater response to moving sounds entering the receptive field than exiting) and shifts were obtained to horizontal, vertical, and oblique motion orientations. Response latency also shifted as a function of motion direction, and stimulus locations eliciting greater spike counts also exhibited the shortest neural latency. Motion crossing the receptive field boundaries appeared to be both necessary and sufficient to produce receptive field shifts. Decreasing the silent interval between successive stimuli in the apparent motion sequence increased both the probability of obtaining a directional effect and the magnitude of receptive field shifts. We suggest that the observed directional effects might be explained by “spatial masking,” where the response of auditory neurons after stimulation from particularly effective locations in space would be diminished. The shift in auditory receptive fields would be expected to shift the perceived location of a moving sound and may explain shifts in localization of moving sources observed in psychophysical studies. Shifts in perceived target location caused by auditory motion might be exploited by auditory predators such as Pteronotus in a predictive tracking strategy to capture moving insect prey.

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Single-Unit Responses in the Inferior Colliculus of Decerebrate Cats II. Sensitivity to Interaural Level Differences

Journal of Neurophysiology ◽

10.1152/jn.1999.82.1.164 ◽

1999 ◽

Vol 82 (1) ◽

pp. 164-175 ◽

Cited By ~ 41

Author(s):

Kevin A. Davis ◽

Ramnarayan Ramachandran ◽

Bradford J. May

Keyword(s):

Frequency Response ◽

Inferior Colliculus ◽

Free Field ◽

Central Nucleus ◽

Type I ◽

Discharge Rates ◽

Ipsilateral Stimulation ◽

Interaural Level Differences ◽

Type V ◽

Decerebrate Cats

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.

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

Journal of Neurophysiology ◽

10.1152/jn.00348.2003 ◽

2003 ◽

Vol 90 (4) ◽

pp. 2648-2659 ◽

Cited By ~ 51

Author(s):

Susanne J. Sterbing ◽

Klaus Hartung ◽

Klaus-Peter Hoffmann

Keyword(s):

White Noise ◽

Inferior Colliculus ◽

Transfer Functions ◽

Free Field ◽

Receptive Fields ◽

Sound Intensity ◽

Spatial Location ◽

Average Diameter ◽

Maximal Response ◽

Spatial Tuning

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.

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Responses of Neurons in the Inferior Colliculus to Dynamic Interaural Phase Cues: Evidence for a Mechanism of Binaural Adaptation

Journal of Neurophysiology ◽

10.1152/jn.2000.83.3.1356 ◽

2000 ◽

Vol 83 (3) ◽

pp. 1356-1365 ◽

Cited By ~ 56

Author(s):

David McAlpine ◽

Dan Jiang ◽

Trevor M. Shackleton ◽

Alan R. Palmer

Keyword(s):

Inferior Colliculus ◽

The Other ◽

Auditory Midbrain ◽

Adaptation Mechanism ◽

Motion Cues ◽

Depth Direction ◽

Discharge Rates ◽

Interaural Phase ◽

History Of ◽

Different Depths

Responses to sound stimuli that humans perceive as moving were obtained for 89 neurons in the inferior colliculus (IC) of urethan-anesthetized guinea pigs. Triangular and sinusoidal interaural phase modulation (IPM), which produced dynamically varying interaural phase disparities (IPDs), was used to present stimuli with different depths, directions, centers, and rates of apparent motion. Many neurons appeared sensitive to dynamic IPDs, with responses at any given IPD depending strongly on the IPDs the stimulus had just passed through. However, it was the temporal pattern of the response, rather than the motion cues in the IPM, that determined sensitivity to features such as motion depth, direction, and center locus. IPM restricted only to the center of the IPD responsive area, evoked lower discharge rates than when the stimulus either moved through the IPD responsive area from outside, or up and down its flanks. When the stimulus was moved through the response area first in one direction and then back in the other, and the same IPDs evoked different responses, the response to the motion away from the center of the IPD responsive area was always lower than the response to the motion toward the center. When the IPD was closer at which the direction of motion reversed was to the center, the response to the following motion was lower. In no case did we find any evidence for neurons that under all conditions preferred one direction of motion to the other. We conclude that responses of IC neurons to IPM stimuli depend not on the history of stimulation, per se, but on the history of their response to stimulation, irrespective of the specific motion cues that evoke those responses. These data are consistent with the involvement of an adaptation mechanism that resides at or above the level of binaural integration. We conclude that our data provide no evidence for specialized motion detection involving dynamic IPD cues in the auditory midbrain of the mammal.

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Physiological Studies of the Precedence Effect in the Inferior Colliculus of the Cat. I. Correlates of Psychophysics

Journal of Neurophysiology ◽

10.1152/jn.1998.80.3.1285 ◽

1998 ◽

Vol 80 (3) ◽

pp. 1285-1301 ◽

Cited By ~ 64

Author(s):

Ruth Y. Litovsky ◽

Tom C. T. Yin

Keyword(s):

Inferior Colliculus ◽

Free Field ◽

Median Plane ◽

Stimulus Level ◽

Central Nucleus ◽

Precedence Effect ◽

Discharge Rates ◽

Physiological Studies ◽

Echo Suppression ◽

Maximal Suppression

Litovsky, Ruth Y. and Tom C. T. Yin. Physiological studies of the precedence effect in the inferior colliculus of the cat. I. Correlates of psychophysics. J. Neurophysiol. 80: 1285–1301, 1998. The precedence effect (PE) is experienced when two spatially separated sounds are presented with such a brief delay that only a single auditory image at or toward the location of the leading source is perceived. The responses of neurons in the central nucleus of the inferior colliculus (ICC) of cats were studied using stimuli that are known to elicit the PE, focusing on the effects of changes in stimulus conditions that a listener might encounter in a natural situation. Experiments were conducted under both free-field (anechoic chamber) and dichotic (headphones) conditions. In free field, the PE was simulated by presenting two sounds from different loudspeakers with one sound delayed relative to the other. Either click or noise stimuli (2- to 10-ms duration) were used. Dichotically, the same conditions were simulated by presenting two click or noise pairs separated by an interstimulus delay (ISD) with interaural time differences (ITDs) imposed separately for each pair. At long ISDs, all neurons responded to both leading and lagging sources as if they were delivered alone. As the ISDs were shortened, the lagging response became suppressed. The ISD of half-maximal suppression varied considerably within the population of neurons studied, ranging from 2 to 100 ms, with means of 35 and 38 ms for free field and dichotic conditions, respectively. Several correlates of psychophysical findings were observed in ICC neurons: suppression was usually stronger with lower overall stimulus level and longer duration stimuli. Suppression also was compared along the azimuth and elevation in free field by placing the lagging source at (0°,0°), which is common to both axes, and the leading sources at locations along either plane that generated similar discharge rates. All neurons that showed suppression along the azimuth also did so in the elevation. In addition, there was a high correlation in the ISD of half-maximal suppression along the two planes ( r = 0.87). These findings suggest that interaural difference cues, which are robust along the horizontal axis but minimal in the median plane, are not necessary for neural correlates of the PE to be manifested. Finally, single-neuron responses did not demonstrate a correlate of build-up of suppression, a phenomenon whereby echo suppression accumulates with ongoing stimulation. This finding adds credibility to theories about the PE that argue for a “higher order” component of the PE.

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Receptive Fields and Binaural Interactions for Virtual-Space Stimuli in the Cat Inferior Colliculus

Journal of Neurophysiology ◽

10.1152/jn.1999.81.6.2833 ◽

1999 ◽

Vol 81 (6) ◽

pp. 2833-2851 ◽

Cited By ~ 51

Author(s):

Bertrand Delgutte ◽

Philip X. Joris ◽

Ruth Y. Litovsky ◽

Tom C. T. Yin

Keyword(s):

Inferior Colliculus ◽

Sound Localization ◽

Transfer Functions ◽

Sagittal Plane ◽

Free Field ◽

Receptive Fields ◽

Field Studies ◽

Contralateral Side ◽

Virtual Space ◽

Acoustic Cues

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.

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Responses of neurons in inferior colliculus to variations in sound-source azimuth

Journal of Neurophysiology ◽

10.1152/jn.1984.52.1.1 ◽

1984 ◽

Vol 52 (1) ◽

pp. 1-17 ◽

Cited By ~ 58

Author(s):

L. M. Aitkin ◽

G. R. Gates ◽

S. C. Phillips

Keyword(s):

Inferior Colliculus ◽

Horizontal Plane ◽

Free Field ◽

Noise Burst ◽

Single Units ◽

Central Nucleus ◽

Lateral Part ◽

Binaural Interaction ◽

Azimuthal Position ◽

Discharge Rates

This study aimed to classify the responses of single units in the auditory midbrain to acoustic stimuli presented in the free field in order to characterize those units likely to have a role in sound localization in the horizontal plane. The responses of 131 single units in the inferior colliculus of the cat and the brush-tailed possum were studied using tone and noise-burst stimuli presented from a speaker capable of movement at any point along a plane 10 degrees above the horizontal plane. Speaker positions along this plane are referred to as speaker azimuths; those on the same side as the recorded inferior colliculus as ipsilateral, and on the opposite side as contralateral, azimuths. For each unit, spike counts were measured as a function of azimuth either at the best frequency (BF) or using noise bursts. These functions are referred to as azimuth functions and were usually measured for at least two intensities, between 10 and 70 dB above threshold. The recording sites of most units were identified histologically with the aid of microlesions and were related to the major subdivisions of the inferior colliculus: the central nucleus (ICC), the lateral part of the external nucleus (ICX), and the rostroventral process (R-ICX). Two units were located in the pericentral nucleus and two in the dorsal nucleus of the lateral lemniscus. Two major classes of neuron were identified: omnidirectional and directionally sensitive. Omnidirectional units exhibited azimuth functions that were either flat or that declined gradually at progressively ipsilateral azimuths. For the latter units, discharge rates at all points monotonically increased with stimulus intensity. There was no indication, for either type of omnidirectional unit, of significant binaural interaction. A good correlation was found between the summed proportions of excitatory-excitatory (EE) and monaural (EO) units observed in dichotic studies (46-55%) and the proportion of omnidirectional units in the present study (47%). A subgroup of directionally sensitive units (36% of the total) displayed azimuth functions for which the azimuthal position of the discharge border or peak firing azimuth remained essentially unaltered over a range of stimulus intensities. These azimuth-selective units are likely to have a role in the detection of the location of stimuli in the horizontal plane and appear to include units that would be considered excitatory-inhibitory (EI) or delay sensitive in dichotic studies. The azimuths over which directionally sensitive units showed their marked directional effects were influenced by the position of the contralateral pinna.(ABSTRACT TRUNCATED AT 400 WORDS)

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Auditory response properties of neurons in deep layers of cat superior colliculus

Journal of Neurophysiology ◽

10.1152/jn.1983.49.3.674 ◽

1983 ◽

Vol 49 (3) ◽

pp. 674-685 ◽

Cited By ~ 70

Author(s):

L. Z. Wise ◽

D. R. Irvine

Keyword(s):

Superior Colliculus ◽

Free Field ◽

Receptive Fields ◽

Great Majority ◽

Noise Burst ◽

Preliminary Evidence ◽

Excitatory Input ◽

Response Properties ◽

Deep Layers ◽

Spatial Fields

1. The auditory responses of 207 single neurons in the intermediate and deep layers of the superior colliculus (SC) of barbiturate -or chloralose-anesthetized cats were recorded extracellularly. Sealed stimulating systems incorporating calibrated probe microphone assemblies were employed to present tone- and noise-burst stimuli. 2. All acoustically activated neurons responded with onset responses to noise bursts. Of those neurons also tested with tonal stimuli, approximately 30% were unresponsive over the frequency range tested (0.1-40 kHz), while the others had higher thresholds to tones than to noise. 3. Details of frequency responsiveness were obtained for 55 neurons; 21 were broadly tuned, while 34 were sharply tuned with clearly defined characteristic frequencies (CFs). All sharply tuned neurons had CFs greater than or equal to 10 kHz. 4. The majority of neurons (81%) responded with latencies in the range 8-20 ms; only 11% of neurons had latencies greater than 30 ms. 5. Binaural response properties were examined for 165 neurons. The great majority (79%) received monaural excitatory input only from the contralateral ear (EO). However, most EO cells were binaurally influenced, the contralateral response being either inhibited (EO/I; 96 of 131 units) or facilitated (EO/F; 33 of 131 units) by simultaneous ipsilateral stimulation. Small subgroups were monaurally excited by either ear (EE cells; 8%) or were unresponsive monaurally but responded strongly to binaural stimulation (OO/F cells; 7%). 6. EO/I, EO/F, and OO/F neurons showed characteristic forms of sensitivity to interaural intensity differences (IIDs). The IID functions of EO/I neurons would be expected to produce large contralateral spatial receptive fields with clearly defined medial borders, such as have been described in studies of deep SC neurons employing free-field stimuli. 7. Preliminary evidence suggests a possible topographic organization of IID sensitivity in deep SC, such that the steeply sloping portion of the function (corresponding to the medial edge of the receptive field) is shifted laterally for EO/I neurons located more caudally in the nucleus. 8. The auditory properties of deep SC neurons are compared with previous reports and implications for the organization of auditory input are considered. The binaural properties and auditory spatial fields of deep SC neurons suggest that any representation of auditory space in this structure is unlikely to be based on restricted spatial fields.

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