Interaural time differences are an important cue for azimuthal sound localization. It is still unclear whether the same neuronal mechanisms underlie the representation in the brain of interaural time difference in different vertebrates and whether these mechanisms are driven by common constraints, such as optimal coding. Current sound localization models may be discriminated by studying the spectral distribution of response peaks in tuning curves that measure the sensitivity to interaural time difference. The sound localization system of the barn owl has been studied intensively, but data that would allow discrimination between currently discussed models are missing from this animal. We have therefore obtained extracellular recordings from the time-sensitive subnuclei of the barn owl's inferior colliculus. Response peaks were broadly scattered over the physiological range of interaural time differences. A change in the representation of the interaural phase differences with frequency was not observed. In some neurons, response peaks fell outside the physiological range of interaural time differences. For a considerable number of neurons, the peak closest to zero interaural time difference was not the behaviorally relevant peak. The data are in best accordance with models suggesting that a place code underlies the representation of interaural time difference. The data from the high-frequency range, but not from the low-frequency range, are consistent with predictions of optimal coding. We speculate that the deviation of the representation of interaural time difference from optimal-coding models in the low-frequency range is attributable to the diminished importance of low frequencies for catching prey in this species.
In a complex auditory scene, a "cocktail party" for example, listeners can disentangle multiple competing sequences of sounds. A recent psychophysical study in our laboratory demonstrated a robust spatial component of stream segregation showing ϳ8°acuity. Here, we recorded single-and multiple-neuron responses from the primary auditory cortex of anesthetized cats while presenting interleaved sound sequences that human listeners would experience as segregated streams. Sequences of broadband sounds alternated between pairs of locations. Neurons synchronized preferentially to sounds from one or the other location, thereby segregating competing sound sequences. Neurons favoring one source location or the other tended to aggregate within the cortex, suggestive of modular organization. The spatial acuity of stream segregation was as narrow as ϳ10°, markedly sharper than the broad spatial tuning for single sources that is well known in the literature. Spatial sensitivity was sharpest among neurons having high characteristic frequencies. Neural stream segregation was predicted well by a parameter-free model that incorporated single-source spatial sensitivity and a measured forwardsuppression term. We found that the forward suppression was not due to post discharge adaptation in the cortex and, therefore, must have arisen in the subcortical pathway or at the level of thalamocortical synapses. A linear-classifier analysis of single-neuron responses to rhythmic stimuli like those used in our psychophysical study yielded thresholds overlapping those of human listeners. Overall, the results indicate that the ascending auditory system does the work of segregating auditory streams, bringing them to discrete modules in the cortex for selection by top-down processes.
To program a goal-directed orienting response toward a sound source embedded in an acoustic scene, the audiomotor system should detect and select the target against a background. Here, we focus on whether the system can segregate synchronous sounds in the midsagittal plane (elevation), a task requiring the auditory system to dissociate the pinna-induced spectral localization cues. Human listeners made rapid head-orienting responses toward either a single sound source (broadband buzzer or Gaussian noise) or toward two simultaneously presented sounds (buzzer and noise) at a wide variety of locations in the midsagittal plane. In the latter case, listeners had to orient to the buzzer (target) and ignore the noise (nontarget). In the single-sound condition, localization was accurate. However, in the double-sound condition, response endpoints depended on relative sound level and spatial disparity. The loudest sound dominated the responses, regardless of whether it was the target or the nontarget. When the sounds had about equal intensities and their spatial disparity was sufficiently small, endpoint distributions were well described by weighted averaging. However, when spatial disparities exceeded ϳ45°, response endpoint distributions became bimodal. Similar response behavior has been reported for visuomotor experiments, for which averaging and bimodal endpoint distributions are thought to arise from neural interactions within retinotopically organized visuomotor maps. We show, however, that the auditory-evoked responses can be well explained by the idiosyncratic acoustics of the pinnae. Hence basic principles of target representation and selection for audition and vision appear to differ profoundly.
Stream segregation enables a listener to disentangle multiple competing sequences of sounds. A recent study from our laboratory demonstrated that cortical neurons in anesthetized cats exhibit spatial stream segregation (SSS) by synchronizing preferentially to one of two sequences of noise bursts that alternate between two source locations. Here, we examine the emergence of SSS along the ascending auditory pathway. Extracellular recordings were made in anesthetized rats from the inferior colliculus (IC), the nucleus of the brachium of the IC (BIN), the medial geniculate body (MGB), and the primary auditory cortex (A1). Stimuli consisted of interleaved sequences of broadband noise bursts that alternated between two source locations. At stimulus presentation rates of 5 and 10 bursts per second, at which human listeners report robust SSS, neural SSS is weak in the central nucleus of the IC (ICC), it appears in the nucleus of the brachium of the IC (BIN) and in approximately two-thirds of neurons in the ventral MGB (MGBv), and is prominent throughout A1. The enhancement of SSS at the cortical level reflects both increased spatial sensitivity and increased forward suppression. We demonstrate that forward suppression in A1 does not result from synaptic inhibition at the cortical level. Instead, forward suppression might reflect synaptic depression in the thalamocortical projection. Together, our findings indicate that auditory streams are increasingly segregated along the ascending auditory pathway as distinct mutually synchronized neural populations.
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