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• W2067266502 abstract "•Listeners’ eye gaze was manipulated in an auditory spatial cue discrimination task•Gazing toward a sound improves auditory spatial cue discrimination•Merely knowing where to listen does not account for the observed behavioral benefit•Results are consistent with oculomotor modulations of subcortical auditory activity The present study demonstrates, for the first time, a specific enhancement of auditory spatial cue discrimination due to eye gaze. Whereas the region of sharpest visual acuity, called the fovea, can be directed at will by moving one’s eyes, auditory spatial information is derived primarily from head-related acoustic cues. Past auditory studies have found better discrimination in front of the head [1Mills A.W. On the minimum audible angle.J. Acoust. Soc. Am. 1958; 30: 237-246Crossref Scopus (677) Google Scholar, 2Hafter E.R. De Maio J. Hellman W.S. Difference thresholds for interaural delay.J. Acoust. Soc. Am. 1975; 57: 181-187Crossref PubMed Scopus (67) Google Scholar, 3Middlebrooks J.C. Onsan Z.A. Stream segregation with high spatial acuity.J. Acoust. Soc. Am. 2012; 132: 3896-3911Crossref PubMed Scopus (50) Google Scholar] but have not manipulated subjects’ gaze, thus overlooking potential oculomotor influences. Electrophysiological studies have shown that the inferior colliculus, a critical auditory midbrain nucleus, shows visual and oculomotor responses [4Porter K.K. Metzger R.R. Groh J.M. Visual- and saccade-related signals in the primate inferior colliculus.Proc. Natl. Acad. Sci. USA. 2007; 104: 17855-17860Crossref PubMed Scopus (36) Google Scholar, 5Bulkin D.A. Groh J.M. Distribution of visual and saccade related information in the monkey inferior colliculus.Front. Neural Circuits. 2012; 6: 61Crossref PubMed Scopus (16) Google Scholar, 6Bulkin D.A. Groh J.M. Distribution of eye position information in the monkey inferior colliculus.J. Neurophysiol. 2012; 107: 785-795Crossref PubMed Scopus (15) Google Scholar] and modulations of auditory activity [7Maier J.X. Groh J.M. Comparison of gain-like properties of eye position signals in inferior colliculus versus auditory cortex of primates.Front. Integr. Neurosci. 2010; 4: 121PubMed Google Scholar, 8Bergan J.F. Knudsen E.I. Visual modulation of auditory responses in the owl inferior colliculus.J. Neurophysiol. 2009; 101: 2924-2933Crossref PubMed Scopus (27) Google Scholar, 9Groh J.M. Trause A.S. Underhill A.M. Clark K.R. Inati S. Eye position influences auditory responses in primate inferior colliculus.Neuron. 2001; 29: 509-518Abstract Full Text Full Text PDF PubMed Scopus (144) Google Scholar], and that auditory neurons in the superior colliculus show shifting receptive fields [10Jay M.F. Sparks D.L. Auditory receptive fields in primate superior colliculus shift with changes in eye position.Nature. 1984; 309: 345-347Crossref PubMed Scopus (275) Google Scholar, 11Jay M.F. Sparks D.L. Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals.J. Neurophysiol. 1987; 57: 35-55PubMed Google Scholar, 12Populin L.C. Tollin D.J. Yin T.C.T. Effect of eye position on saccades and neuronal responses to acoustic stimuli in the superior colliculus of the behaving cat.J. Neurophysiol. 2004; 92: 2151-2167Crossref PubMed Scopus (38) Google Scholar, 13Winkowski D.E. Knudsen E.I. Top-down gain control of the auditory space map by gaze control circuitry in the barn owl.Nature. 2006; 439: 336-339Crossref PubMed Scopus (84) Google Scholar]. How the auditory system leverages this crossmodal information at the behavioral level remains unknown. Here we directed subjects’ gaze (with an eccentric dot) or auditory attention (with lateralized noise) while they performed an auditory spatial cue discrimination task. We found that directing gaze toward a sound significantly enhances discrimination of both interaural level and time differences, whereas directing auditory spatial attention does not. These results show that oculomotor information variably enhances auditory spatial resolution even when the head remains stationary, revealing a distinct behavioral benefit possibly arising from auditory-oculomotor interactions at an earlier level of processing than previously demonstrated. The present study demonstrates, for the first time, a specific enhancement of auditory spatial cue discrimination due to eye gaze. Whereas the region of sharpest visual acuity, called the fovea, can be directed at will by moving one’s eyes, auditory spatial information is derived primarily from head-related acoustic cues. Past auditory studies have found better discrimination in front of the head [1Mills A.W. On the minimum audible angle.J. Acoust. Soc. Am. 1958; 30: 237-246Crossref Scopus (677) Google Scholar, 2Hafter E.R. De Maio J. Hellman W.S. Difference thresholds for interaural delay.J. Acoust. Soc. Am. 1975; 57: 181-187Crossref PubMed Scopus (67) Google Scholar, 3Middlebrooks J.C. Onsan Z.A. Stream segregation with high spatial acuity.J. Acoust. Soc. Am. 2012; 132: 3896-3911Crossref PubMed Scopus (50) Google Scholar] but have not manipulated subjects’ gaze, thus overlooking potential oculomotor influences. Electrophysiological studies have shown that the inferior colliculus, a critical auditory midbrain nucleus, shows visual and oculomotor responses [4Porter K.K. Metzger R.R. Groh J.M. Visual- and saccade-related signals in the primate inferior colliculus.Proc. Natl. Acad. Sci. USA. 2007; 104: 17855-17860Crossref PubMed Scopus (36) Google Scholar, 5Bulkin D.A. Groh J.M. Distribution of visual and saccade related information in the monkey inferior colliculus.Front. Neural Circuits. 2012; 6: 61Crossref PubMed Scopus (16) Google Scholar, 6Bulkin D.A. Groh J.M. Distribution of eye position information in the monkey inferior colliculus.J. Neurophysiol. 2012; 107: 785-795Crossref PubMed Scopus (15) Google Scholar] and modulations of auditory activity [7Maier J.X. Groh J.M. Comparison of gain-like properties of eye position signals in inferior colliculus versus auditory cortex of primates.Front. Integr. Neurosci. 2010; 4: 121PubMed Google Scholar, 8Bergan J.F. Knudsen E.I. Visual modulation of auditory responses in the owl inferior colliculus.J. Neurophysiol. 2009; 101: 2924-2933Crossref PubMed Scopus (27) Google Scholar, 9Groh J.M. Trause A.S. Underhill A.M. Clark K.R. Inati S. Eye position influences auditory responses in primate inferior colliculus.Neuron. 2001; 29: 509-518Abstract Full Text Full Text PDF PubMed Scopus (144) Google Scholar], and that auditory neurons in the superior colliculus show shifting receptive fields [10Jay M.F. Sparks D.L. Auditory receptive fields in primate superior colliculus shift with changes in eye position.Nature. 1984; 309: 345-347Crossref PubMed Scopus (275) Google Scholar, 11Jay M.F. Sparks D.L. Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals.J. Neurophysiol. 1987; 57: 35-55PubMed Google Scholar, 12Populin L.C. Tollin D.J. Yin T.C.T. Effect of eye position on saccades and neuronal responses to acoustic stimuli in the superior colliculus of the behaving cat.J. Neurophysiol. 2004; 92: 2151-2167Crossref PubMed Scopus (38) Google Scholar, 13Winkowski D.E. Knudsen E.I. Top-down gain control of the auditory space map by gaze control circuitry in the barn owl.Nature. 2006; 439: 336-339Crossref PubMed Scopus (84) Google Scholar]. How the auditory system leverages this crossmodal information at the behavioral level remains unknown. Here we directed subjects’ gaze (with an eccentric dot) or auditory attention (with lateralized noise) while they performed an auditory spatial cue discrimination task. We found that directing gaze toward a sound significantly enhances discrimination of both interaural level and time differences, whereas directing auditory spatial attention does not. These results show that oculomotor information variably enhances auditory spatial resolution even when the head remains stationary, revealing a distinct behavioral benefit possibly arising from auditory-oculomotor interactions at an earlier level of processing than previously demonstrated. When making judgments about an object, we generally rely on the most informative sensory cues available [14Talsma D. Senkowski D. Soto-Faraco S. Woldorff M.G. The multifaceted interplay between attention and multisensory integration.Trends Cogn. Sci. 2010; 14: 400-410Abstract Full Text Full Text PDF PubMed Scopus (509) Google Scholar, 15Whitchurch E.A. Takahashi T.T. Combined auditory and visual stimuli facilitate head saccades in the barn owl (Tyto alba).J. Neurophysiol. 2006; 96: 730-745Crossref PubMed Scopus (40) Google Scholar]. For visible objects, the eyes are more spatially reliable than the ears. As a result, auditory localization is strongly biased by a coincident visual stimulus [16Recanzone G.H. Interactions of auditory and visual stimuli in space and time.Hear. Res. 2009; 258: 89-99Crossref PubMed Scopus (97) Google Scholar]. Additionally, gazing toward a visual stimulus biases sound localization away from the direction of gaze over short time periods [17Lewald J. The effect of gaze eccentricity on perceived sound direction and its relation to visual localization.Hear. Res. 1998; 115: 206-216Crossref PubMed Scopus (70) Google Scholar, 18Lewald J. Ehrenstein W.H. The effect of eye position on auditory lateralization.Exp. Brain Res. 1996; 108: 473-485Crossref PubMed Scopus (78) Google Scholar] and toward it over longer ones [19Razavi B. O’Neill W.E. Paige G.D. Auditory spatial perception dynamically realigns with changing eye position.J. Neurosci. 2007; 27: 10249-10258Crossref PubMed Scopus (63) Google Scholar], suggesting multiple mechanisms by which eye position influences auditory localization. Previous studies, however, have focused on absolute tasks (locating a sound) instead of relative tasks (discriminating two sounds’ locations) and did not measure acuity. The observed oculomotor-based realignments of auditory localization behavior could reasonably emerge at any stage of processing from brainstem to cortex. However, performance on relative spatial discrimination tasks has been linked to the acuity of midbrain spatial receptive fields in owls [20Bala A.D.S. Spitzer M.W. Takahashi T.T. Prediction of auditory spatial acuity from neural images on the owl’s auditory space map.Nature. 2003; 424: 771-774Crossref PubMed Scopus (80) Google Scholar, 21Bala A.D.S. Spitzer M.W. Takahashi T.T. Auditory spatial acuity approximates the resolving power of space-specific neurons.PLoS ONE. 2007; 2: e675Crossref PubMed Scopus (30) Google Scholar]. Thus, gaze-driven improvements in auditory spatial cue discrimination could be linked to oculomotor modulation of subcortical coding of these cues observed in a number of studies [7Maier J.X. Groh J.M. Comparison of gain-like properties of eye position signals in inferior colliculus versus auditory cortex of primates.Front. Integr. Neurosci. 2010; 4: 121PubMed Google Scholar, 9Groh J.M. Trause A.S. Underhill A.M. Clark K.R. Inati S. Eye position influences auditory responses in primate inferior colliculus.Neuron. 2001; 29: 509-518Abstract Full Text Full Text PDF PubMed Scopus (144) Google Scholar, 10Jay M.F. Sparks D.L. Auditory receptive fields in primate superior colliculus shift with changes in eye position.Nature. 1984; 309: 345-347Crossref PubMed Scopus (275) Google Scholar, 11Jay M.F. Sparks D.L. Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals.J. Neurophysiol. 1987; 57: 35-55PubMed Google Scholar, 12Populin L.C. Tollin D.J. Yin T.C.T. Effect of eye position on saccades and neuronal responses to acoustic stimuli in the superior colliculus of the behaving cat.J. Neurophysiol. 2004; 92: 2151-2167Crossref PubMed Scopus (38) Google Scholar, 13Winkowski D.E. Knudsen E.I. Top-down gain control of the auditory space map by gaze control circuitry in the barn owl.Nature. 2006; 439: 336-339Crossref PubMed Scopus (84) Google Scholar]. Here we determined whether directing gaze to an auditory target increases behavioral sensitivity to binaural cues in that direction. We presented 16 subjects (11 female, 5 male; age 23.9 ± 3.1 years [mean ± SD]; thresholds ≤ 20 dB hearing level at octave frequencies 250–8,000 Hz) with trials consisting of an auditory or visual primer followed by a probe comprising two brief noise bursts at slightly different perceived positions (i.e., differing binaural cue values; Figure 1A) in a two-alternative forced-choice task. Sounds were presented via insert earphones. Subjects reported whether the second probe noise burst was to the right or to the left of the first probe noise burst (i.e., discriminated their relative positions). One subject was removed due to abnormal binaural perception, yielding N = 15. Typically, interaural level differences (ILDs) are more informative regarding azimuth at frequencies above ∼3 kHz and interaural time differences (ITDs) below ∼1.5 kHz. These binaural cues are extracted in auditory brainstem nuclei: ILDs in the lateral superior olive (LSO), and ITDs in the medial superior olive (MSO). Because oculomotor activity may influence these parallel pathways differently, we manipulated the cues independently, using octave-wide noise bursts in the relevant high-frequency (centered at 4 kHz) or low-frequency (500 Hz) ranges. This created a lateralized percept, but stimuli were generally not perceived to be externalized as they would have been using free-field presentation. Because ILD and ITD were separately manipulated (alternate cue set to 0), some subjects may have perceived conflicting cues. This possibility was mitigated by filtering the stimuli to the relevant frequency ranges; furthermore, any potential impact on discrimination was taken into account by the initial calibration for each subject (see below). The ILD or ITD was set for each subject so that sounds were perceived to be centered (0° azimuth midpoint) or to the side (±25° midpoint), with offsets of 12.0 ± 5.0 dB for ILD and 231 ± 89 μs for ITD. The excluded subject gave unnaturally large ILD and ITD offsets (42 dB; 1,157 μs). ILD and ITD discrimination thresholds were determined for each subject (5.9 ± 1.3 dB; 217 ± 70 μs) at their measured offset; performance was tested at these values thereafter. These thresholds are larger than in previous studies, which may have resulted from differing stimulus parameters or subjects’ inexperience in interaural discrimination tasks [22Wright B.A. Fitzgerald M.B. Different patterns of human discrimination learning for two interaural cues to sound-source location.Proc. Natl. Acad. Sci. USA. 2001; 98: 12307-12312Crossref PubMed Scopus (129) Google Scholar]. Each experimental block employed either visual or auditory primers lasting 800 ms followed by a 200 ms pause before the probe started. Visual primers were a white fixation dot subtending 0.85° (turning gray after 800 ms to allow maintained fixation). Auditory primers were noise lateralized by the complementary binaural cue in the complementary frequency band (e.g., high-frequency ILD primer preceded low-frequency ITD probe), to test for effects of directed auditory attention. Primers were either directional, indicating the midpoint lateralization of the impending probe, or uninformative, occurring in the center regardless of the probe’s position. These variables resulted in four experimental blocks (Figure 1B). Fixation on visual primers was confirmed with eye tracking before each trial (see Figure S1 and Supplemental Experimental Procedures available online). The probe comprised two noise bursts lasting 70 ms each, with 30 ms between them. Subjects’ gaze was not controlled in auditory trials, and they gazed near the center in the majority of trials. Using four-factor within-subjects ANOVA, we found significant effects of probe position (F(1,14) = 96.0, p = 1.2 × 10−7), binaural cue type (F(1,14) = 6.15, p = 0.026), and an interaction between the two factors (F(1,14) = 13.7, p = 0.0024). Specifically, performance was better for center than for side probes (Figure 2), as expected [1Mills A.W. On the minimum audible angle.J. Acoust. Soc. Am. 1958; 30: 237-246Crossref Scopus (677) Google Scholar, 2Hafter E.R. De Maio J. Hellman W.S. Difference thresholds for interaural delay.J. Acoust. Soc. Am. 1975; 57: 181-187Crossref PubMed Scopus (67) Google Scholar, 3Middlebrooks J.C. Onsan Z.A. Stream segregation with high spatial acuity.J. Acoust. Soc. Am. 2012; 132: 3896-3911Crossref PubMed Scopus (50) Google Scholar]. Primer informativeness was significant (F(1,14) = 4.75, p = 0.047), but its interaction with primer modality was much more so (F(1,14) = 20.5, p = 0.00048), reflecting the fact that only directional visual primers improved performance. No other factors or interactions were significant. All statistics were performed on arcsine-transformed data. The biggest improvement was due to gazing toward a side probe. Subjects benefitted from informative visual primers on both ILD (p = 0.00083, one-tailed paired t test, Bonferroni-corrected α = 0.00625; Figures 2A and 3A , visual) and ITD trials (p = 0.0044; Figures 2B and 3B, visual). These results show that gazing toward an off-center stimulus enhances binaural discrimination, but could this come simply from knowing where to listen? Using an auditory primer instead of a visual one (meaning listeners were spatially primed but not directing gaze) provided no improvements (p = 0.53 ILD, p = 0.41 ITD). This result is surprising given that previous experiments have shown intelligibility benefits of knowing where to listen [23Best V. Ozmeral E.J. Shinn-Cunningham B.G. Visually-guided attention enhances target identification in a complex auditory scene.J. Assoc. Res. Otolaryngol. 2007; 8: 294-304Crossref PubMed Scopus (75) Google Scholar]. Those gains may come from facilitated selective attention, likely a cortical process [24Mesgarani N. Chang E.F. Selective cortical representation of attended speaker in multi-talker speech perception.Nature. 2012; 485: 233-236Crossref PubMed Scopus (542) Google Scholar]. The present results are consistent with a gaze-directed refinement of subcortical binaural cue coding. Within one experimental block, all trials had either directional or uninformative primers. In trials with a central probe, directional visual primers improved discrimination for ILD probes (p = 0.0051). Auditory primers offered no benefit (p ≈ 0.9 for ILD, ITD). Thus, while only knowing where to listen is not enough to improve discrimination, it does appear to affect whether a centered visual stimulus improves performance, at least for ILD-lateralized stimuli. Gaze-mediated modulations of auditory spatial processing have often been discussed in the context of bringing auditory information (innately head-centric) and visual information (innately eye-centric) into a common reference frame [9Groh J.M. Trause A.S. Underhill A.M. Clark K.R. Inati S. Eye position influences auditory responses in primate inferior colliculus.Neuron. 2001; 29: 509-518Abstract Full Text Full Text PDF PubMed Scopus (144) Google Scholar, 10Jay M.F. Sparks D.L. Auditory receptive fields in primate superior colliculus shift with changes in eye position.Nature. 1984; 309: 345-347Crossref PubMed Scopus (275) Google Scholar, 11Jay M.F. Sparks D.L. Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals.J. Neurophysiol. 1987; 57: 35-55PubMed Google Scholar, 12Populin L.C. Tollin D.J. Yin T.C.T. Effect of eye position on saccades and neuronal responses to acoustic stimuli in the superior colliculus of the behaving cat.J. Neurophysiol. 2004; 92: 2151-2167Crossref PubMed Scopus (38) Google Scholar, 25Lee J. Groh J.M. Auditory signals evolve from hybrid- to eye-centered coordinates in the primate superior colliculus.J. Neurophysiol. 2012; 108: 227-242Crossref PubMed Scopus (37) Google Scholar]. However, as in vision, dynamically directing the region of highest auditory acuity (even if that region is broad, unlike the visual fovea) also likely has important behavioral benefits. When a listener attends to one speech stream while suppressing others, spatial separation between these sources increases intelligibility, an effect known as spatial release from masking that improves with increasing separations [26Marrone N. Mason C.R. Kidd G. Tuning in the spatial dimension: evidence from a masked speech identification task.J. Acoust. Soc. Am. 2008; 124: 1146-1158Crossref PubMed Scopus (101) Google Scholar]. Functionally speaking, improving spatial cue discrimination could effectively increase the perceptual separation (by decreasing the spatial ambiguity) of two sources that are physically close together. Studies of concurrent minimum audible angles (in which probe sounds were presented at the same time, rather than sequentially) [27Perrott D.R. Saberi K. Minimum audible angle thresholds for sources varying in both elevation and azimuth.J. Acoust. Soc. Am. 1990; 87: 1728-1731Crossref PubMed Scopus (152) Google Scholar, 28Divenyi P.L. Oliver S.K. Resolution of steady-state sounds in simulated auditory space.J. Acoust. Soc. Am. 1989; 85: 2042-2052Crossref Scopus (22) Google Scholar], the spatial acuity with which streams can be segregated [3Middlebrooks J.C. Onsan Z.A. Stream segregation with high spatial acuity.J. Acoust. Soc. Am. 2012; 132: 3896-3911Crossref PubMed Scopus (50) Google Scholar], and the angles by which two sources need to be separated to be perceived distinctly [29Best V. van Schaik A. Carlile S. Separation of concurrent broadband sound sources by human listeners.J. Acoust. Soc. Am. 2004; 115: 324-336Crossref PubMed Scopus (45) Google Scholar] all suggest that there is indeed room for improvement when segregating lateral sound sources. Over short periods of directed gaze, like those used here, shifts in the apparent sound-source location away from the direction of gaze have been demonstrated behaviorally [17Lewald J. The effect of gaze eccentricity on perceived sound direction and its relation to visual localization.Hear. Res. 1998; 115: 206-216Crossref PubMed Scopus (70) Google Scholar, 18Lewald J. Ehrenstein W.H. The effect of eye position on auditory lateralization.Exp. Brain Res. 1996; 108: 473-485Crossref PubMed Scopus (78) Google Scholar]. Unlike changes in acuity, such biases in perceived location could conceivably emerge at any level of processing, including in the cortex. However, it is worth speculating whether there is a physiological mechanism that could explain such shifts together with the discrimination enhancements of the current study (Figures 4A and 4C , centered gaze; Figures 4B and 4D, eccentric gaze). Such a mechanism may arise from the fact that auditory brainstem spatial receptive fields are typically nonlinear, with many showing a transition zone between low and high spike rates where the slope is steepest. The best coding resolution, i.e., the most information, is found in this steeper region [30Harper N.S. McAlpine D. Optimal neural population coding of an auditory spatial cue.Nature. 2004; 430: 682-686Crossref PubMed Scopus (213) Google Scholar]. Intensity and ITD response functions have been shown to shift as result of adapting to stimulus statistics [31Maier J.K. Hehrmann P. Harper N.S. Klump G.M. Pressnitzer D. McAlpine D. Adaptive coding is constrained to midline locations in a spatial listening task.J. Neurophysiol. 2012; 108: 1856-1868Crossref PubMed Scopus (19) Google Scholar, 32Dean I. Robinson B.L. Harper N.S. McAlpine D. Rapid neural adaptation to sound level statistics.J. Neurosci. 2008; 28: 6430-6438Crossref PubMed Scopus (149) Google Scholar]. Such shifts of nonlinear response functions change the operating point, resulting in larger differences in neural firing rates. Shifting rate-azimuth curves in the direction of eye gaze (Figures 4C and 4D, orange sound sources) is one mechanism that would allow the sound sources’ locations to be better distinguished, improving discrimination (Figure 4B, orange circles more punctate than in Figure 4A). Moving the receptive field in this manner would predict that localization estimates would move opposite gaze direction to some degree, as has been observed previously [17Lewald J. The effect of gaze eccentricity on perceived sound direction and its relation to visual localization.Hear. Res. 1998; 115: 206-216Crossref PubMed Scopus (70) Google Scholar, 18Lewald J. Ehrenstein W.H. The effect of eye position on auditory lateralization.Exp. Brain Res. 1996; 108: 473-485Crossref PubMed Scopus (78) Google Scholar] (Figure 4, blue sources). For example, gazing leftward would shift the receptive field to the left, resulting in (1) better discrimination of the left-lateralized sounds, and (2) a rightward shift in the centered sound source’s perceived azimuth (Figure 4D, blue arrow meeting perceived azimuth axis right of center). This shifting receptive field would not explain long-term localization biases in the same direction as gaze [19Razavi B. O’Neill W.E. Paige G.D. Auditory spatial perception dynamically realigns with changing eye position.J. Neurosci. 2007; 27: 10249-10258Crossref PubMed Scopus (63) Google Scholar], but further investigation with varied timing may reconcile the present results with these findings. Furthermore, behavioral work has shown that gaze’s interaction with sound localization is frequency dependent, implicating centers of the brain with tonotopic organization such as those in the ascending auditory pathway [33Van Grootel T.J. Van Wanrooij M.M. Van Opstal A.J. Influence of static eye and head position on tone-evoked gaze shifts.J. Neurosci. 2011; 31: 17496-17504Crossref PubMed Scopus (12) Google Scholar]. Gaze’s effect on ILD discrimination may stem from such mechanisms. There is evidence of gaze-mediated shifts of auditory spatial receptive fields in superior colliculus (SC) and its avian analog [11Jay M.F. Sparks D.L. Sensorimotor integration in the primate superior colliculus. II. Coordinates of auditory signals.J. Neurophysiol. 1987; 57: 35-55PubMed Google Scholar, 12Populin L.C. Tollin D.J. Yin T.C.T. Effect of eye position on saccades and neuronal responses to acoustic stimuli in the superior colliculus of the behaving cat.J. Neurophysiol. 2004; 92: 2151-2167Crossref PubMed Scopus (38) Google Scholar, 13Winkowski D.E. Knudsen E.I. Top-down gain control of the auditory space map by gaze control circuitry in the barn owl.Nature. 2006; 439: 336-339Crossref PubMed Scopus (84) Google Scholar]. The SC is the principal midbrain nucleus involved in executing saccadic eye movements and is thought to integrate spatial information across modalities [34Lewald J. Dörrscheidt G.J. Spatial-tuning properties of auditory neurons in the optic tectum of the pigeon.Brain Res. 1998; 790: 339-342Crossref PubMed Scopus (10) Google Scholar]. It contains spatially tuned auditory neurons that typically respond to high frequencies and are generally more sensitive to ILDs [35Slee S.J. Young E.D. Linear processing of interaural level difference underlies spatial tuning in the nucleus of the brachium of the inferior colliculus.J. Neurosci. 2013; 33: 3891-3904Crossref PubMed Scopus (23) Google Scholar, 36Wise L.Z. Irvine D.R. Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus: implications for auditory spatial representation.J. Neurophysiol. 1985; 54: 185-211PubMed Google Scholar]. It is not clear whether these spatial receptive field shifts originate in SC, or whether they emerge in a previous level of processing, such as the external and pericentral nuclei of the inferior colliculus (IC) and the nucleus of the brachium of the IC, which project to SC [35Slee S.J. Young E.D. Linear processing of interaural level difference underlies spatial tuning in the nucleus of the brachium of the inferior colliculus.J. Neurosci. 2013; 33: 3891-3904Crossref PubMed Scopus (23) Google Scholar, 37Sparks D.L. Hartwich-Young R. The deep layers of the superior colliculus.Rev. Oculomot. Res. 1989; 3: 213-255PubMed Google Scholar] or the superior olivary complex (which projects to IC [38Huffman R.F. Henson Jr., O.W. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus.Brain Res. Brain Res. Rev. 1990; 15: 295-323Crossref PubMed Scopus (358) Google Scholar]). In IC, gaze interacts in a complex way with auditory responses, producing a representation that is neither fully head- nor eye-centered but can be used to compute an eye-centric representation [7Maier J.X. Groh J.M. Comparison of gain-like properties of eye position signals in inferior colliculus versus auditory cortex of primates.Front. Integr. Neurosci. 2010; 4: 121PubMed Google Scholar, 9Groh J.M. Trause A.S. Underhill A.M. Clark K.R. Inati S. Eye position influences auditory responses in primate inferior colliculus.Neuron. 2001; 29: 509-518Abstract Full Text Full Text PDF PubMed Scopus (144) Google Scholar]. Combinations of these responses, especially of units tuned to opposite azimuths, could result in shifting receptive fields downstream, which could in turn help to explain the improvements seen here in ILD discrimination for eccentric probes. For ITD, a possible physiological mechanism for the improvements in discrimination may lie in the MSO, where ITD cues are calculated. Recordings in the MSO show that rate-ITD curves often peak outside the physiological range, with their region of maximal slope covering the relevant range [39Pecka M. Brand A. Behrend O. Grothe B. Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition.J. Neurosci. 2008; 28: 6914-6925Crossref PubMed Scopus (162) Google Scholar]. Inhibition plays a role in ITD processing in the MSO [39Pecka M. Brand A. Behrend O. Grothe B. Interaural time difference processing in the mammalian medial superior olive: the role of glycinergic inhibition.J. Neurosci. 2008; 28: 6914-6925Crossref PubMed Scopus (162) Google Scholar], and while the details are debated, modulating this inhibition could shift ITD receptive fields [40Zhou Y. Carney L.H. Colburn H.S. A model for interaural time difference sensitivity in the medial superior olive: interaction of excitatory and inhibitory synaptic inputs, channel dynamics, and cellular morphology.J. Neurosci. 2005; 25: 3046-3058Crossref PubMed Scopus (88) Google Scholar]. It is conceivable that this modulatory signal could originate from nonauditory regions of the brainstem, midbrain, or cortex, although this is yet to be demonstrated. While not related to gaze, adaptive changes to ITD response functions observed in IC (which receives MSO inputs [38Huffman R.F. Henson Jr., O.W. The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus.Brain Res. Brain Res. Rev. 1990; 15: 295-323Crossref PubMed Scopus (358) Google Scholar]) indicate that such modulations are at least feasible [31Maier J.K. Hehrmann P. Harper N.S. Klump G.M. Pressnitzer D. McAlpine D. Adaptive coding is constrained to midline locations in a spatial listening task.J. Neurophysiol. 2012; 108: 1856-1868Crossref PubMed Scopus (19) Google Scholar]. What is driving these modulations of discrimination performance? The cortical network controlling visual attention is well studied [41Corbetta M. Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain.Nat. Rev. Neurosci. 2002; 3: 201-215Crossref PubMed Scopus (8630) Google Scholar], and the frontal eye field (FEF) region, an important node in this network, has strong connections to SC [42Leichnetz G.R. Spencer R.F. Hardy S.G.P. Astruc J. The prefrontal corticotectal projection in the monkey; an anterograde and retrograde horseradish peroxidase study.Neuroscience. 1981; 6: 1023-1041Crossref PubMed Scopus (218) Google Scholar] as well as to the auditory cortex (AC) [43Barbas H. Mesulam M.-M. Organization of afferent input to subdivisions of area 8 in the rhesus monkey.J. Comp. Neurol. 1981; 200: 407-431Crossref PubMed Scopus (394) Google Scholar]. FEF is also important to auditory attention [44Lee A.K.C. Rajaram S. Xia J. Bharadwaj H. Larson E. Hämäläinen M.S. Shinn-Cunningham B.G. Auditory selective attention reveals preparatory activity in different cortical regions for selection based on source location and source pitch.Front. Neurosci. 2013; 6: 190Crossref PubMed Scopus (54) Google Scholar], and studies have shown sharpening of auditory spatial receptive fields by microstimulation in the avian FEF analog [13Winkowski D.E. Knudsen E.I. Top-down gain control of the auditory space map by gaze control circuitry in the barn owl.Nature. 2006; 439: 336-339Crossref PubMed Scopus (84) Google Scholar], suggesting a role in supramodal attention. Although AC is likely important to selective auditory attention [24Mesgarani N. Chang E.F. Selective cortical representation of attended speaker in multi-talker speech perception.Nature. 2012; 485: 233-236Crossref PubMed Scopus (542) Google Scholar], electrophysiological work has shown only weak effects of gaze in AC [7Maier J.X. Groh J.M. Comparison of gain-like properties of eye position signals in inferior colliculus versus auditory cortex of primates.Front. Integr. Neurosci. 2010; 4: 121PubMed Google Scholar] compared with stronger modulations in IC [6Bulkin D.A. Groh J.M. Distribution of eye position information in the monkey inferior colliculus.J. Neurophysiol. 2012; 107: 785-795Crossref PubMed Scopus (15) Google Scholar, 9Groh J.M. Trause A.S. Underhill A.M. Clark K.R. Inati S. Eye position influences auditory responses in primate inferior colliculus.Neuron. 2001; 29: 509-518Abstract Full Text Full Text PDF PubMed Scopus (144) Google Scholar]. We posit that the improvement in discrimination observed here when directing gaze but not auditory attention alone results from modulation of subcortical auditory activity by the oculomotor, and even possibly the visual attentive system [45Müller J.R. Philiastides M.G. Newsome W.T. Microstimulation of the superior colliculus focuses attention without moving the eyes.Proc. Natl. Acad. Sci. USA. 2005; 102: 524-529Crossref PubMed Scopus (275) Google Scholar], independent of auditory attention. Here we observed an enhancement in auditory spatial cue discrimination when gazing toward an auditory stimulus lateralized by manipulating either ILD or ITD. Crucially, discrimination saw no improvement in any experimental conditions where location was cued acoustically (leaving gaze undirected), demonstrating that simply knowing where to listen is not enough to improve discrimination, and that the oculomotor system is a necessary part of the observed enhancements. ILD discrimination also improved when the subject gazed toward a centered visual primer and knew the auditory probe would also be centered, suggesting that attention may affect gaze’s impact on auditory spatial perception. Taken together, the results of this study are consistent with interaction of the oculomotor system with subcortical binaural processing pathways benefitting human spatial hearing. All methods were approved by the University of Washington Institutional Review Board. Acoustic stimuli were ramped on/off by a 10 ms cos2 envelope. Filtering was performed as frequency domain multiplication, yielding negligible energy outside passbands. There were 40 trials per data point per subject. Individual ILD and ITD offsets were determined for each subject by aligning repeating acoustic noise bursts with a visual fixation dot at ±25° several times and averaging those estimates. We used a weighted up/down adaptive track to measure ILD and ITD discrimination at 75% performance at the center-gaze, side-probe condition, and these values separated probe bursts for the entire experiment. ITDs were applied to both envelope and fine structure. We thank Mihwa Kim for assistance with data collection and Eric Larson and Jennifer L. Thornton for comments. This work was funded by NIH grants R00 DC010196 and R01 DC013260 (A.K.C.L.) and T32 DC005361 (R.K.M.). Download .pdf (.1 MB) Help with pdf files Document S1. Supplemental Experimental Procedures and Figure S1" @default.
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