Spatial Stream Segregation by Auditory Cortical Neurons

Abstract

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.

Six Degrees of Auditory Spatial Separation

“…At a population level, the resulting spatial unmasking of the target approaches what can be demonstrated behaviorally (Best et al 2005). Similarly, in the anesthetized cat, Middlebrooks and Breman found an order of magnitude improvement in spatial selectivity using two concurrent but interleaved streams of rhythmic stimuli (Middlebrooks and Bremen 2013). Spatial separation of only 8°was required for individual neurons to become entrained to one of the two streams and human subjects performed well on the same task at this separation (Middlebrooks and Onsan 2012).…”

“…Similarly, in the work in avian field-L discussed above, spatial modulation of song identity was the dependent variable (Maddox et al 2012). In the cat, it was the preferential tuning to one of two concurrent streams of rhythmic stimuli that was modulated by their relative location (Middlebrooks and Bremen 2013). These sorts of stimuli are better described as perceptual objects or streams rather than as the sum of the many physical parameters of the acoustic sources.…”

“…By contrast, the sensory receptors of the ear encode frequency so that space must be computed from binaural and monaural acoustical cues at the ears (Blauert 1997;Carlile et al 2005) and is dependent on the relative position of the head. Despite considerable progress, some fundamental questions remain: in particular, (i) how the binaural cues are encoded (see Grothe et al 2010;Ashida and Carr 2011); (ii) the way in which auditory space is represented, particularly at cortical levels (King and Middlebrooks 2010;Middlebrooks and Bremen 2013); and (iii) how audio-visual spatial information is so efficiently combined particularly given the different coordinate systems of the receptors. Understanding the higher-level architecture of the auditory spatial representation is key to understanding this efficient sensory convergence.…”

Neural processing of natural sounds

“…Similarly, responses in human auditory cortex use a gain control to emphasize the temporal modulations characteristic of speech. Neurophysiological studies in primates [130,131] and birds [132] have also begun to unravel how multiple auditory streams could be represented in the auditory system. In summary, auditory neuroscientists have mostly focused their attention to understanding the computations needed to passively recognize and categorize natural sounds and much more research is needed to understand how acoustical signals are processed in active communications and in natural soundscapes.…”

Physiology, Psychoacoustics and Cognition in Normal and Impaired Hearing

“…For example, when a rhythmic sequence of identical sound bursts is presented from a single location, it is often perceived as one source. But, when the sound sequence is presented from two different locations, it can be perceived as two sounds (Middlebrooks and Onsan 2012;Middlebrooks and Bremen 2013). Such findings suggest that a mixture of spatial and non-spatial auditory cues from both the dorsal and ventral pathways may be needed in order to create a coherent auditory-perceptual representation that guides behavior.…”