Interaction of spatial and non-spatial cues in auditory stream segregation in the European starling.

Integrating sounds from the same source and segregating sounds from different sources in an acoustic scene are an essential function of the auditory system. Naturally, the auditory system simultaneously makes use of multiple cues. Here, we investigate the interaction between spatial cues and frequency cues in stream segregation of European starlings (Sturnus vulgaris) using an objective measure of perception. Neural responses to streaming sounds were recorded, while the bird was performing a behavioural task that results in a higher sensitivity during a one-stream than a two-stream percept. Birds were trained to detect an onset time shift of a B tone in an ABA- triplet sequence in which A and B could differ in frequency and/or spatial location. If the frequency difference or spatial separation between the signal sources or both were increased, the behavioural time shift detection performance deteriorated. Spatial separation had a smaller effect on the performance compared to the frequency difference and both cues additively affected the performance. Neural responses in the primary auditory forebrain were affected by the frequency and spatial cues. However, frequency and spatial cue differences being sufficiently large to elicit behavioural effects did not reveal correlated neural response differences. The difference between the neuronal response pattern and behavioural response is discussed with relation to the task given to the bird. Perceptual effects of combining different cues in auditory scene analysis indicate that these cues are analysed independently and given different weights suggesting that the streaming percept arises consecutively to initial cue analysis.

Animal models for auditory streaming.

Sounds in the natural environment need to be assigned to acoustic sources to evaluate complex auditory scenes. Separating sources will affect the analysis of auditory features of sounds. As the benefits of assigning sounds to specific sources accrue to all species communicating acoustically, the ability for auditory scene analysis is widespread among different animals. Animal studies allow for a deeper insight into the neuronal mechanisms underlying auditory scene analysis. Here, we will review the paradigms applied in the study of auditory scene analysis and streaming of sequential sounds in animal models. We will compare the psychophysical results from the animal studies to the evidence obtained in human psychophysics of auditory streaming, i.e. in a task commonly used for measuring the capability for auditory scene analysis. Furthermore, the neuronal correlates of auditory streaming will be reviewed in different animal models and the observations of the neurons' response measures will be related to perception. The across-species comparison will reveal whether similar demands in the analysis of acoustic scenes have resulted in similar perceptual and neuronal processing mechanisms in the wide range of species being capable of auditory scene analysis.This article is part of the themed issue 'Auditory and visual scene analysis'.

Enhancement of forward suppression begins in the ventral cochlear nucleus.

A neuron׳s response to a sound can be suppressed by the presentation of a preceding sound. It has been suggested that this suppression is a direct correlate of the psychophysical phenomenon of forward masking, however, forward suppression, as measured in the responses of the auditory nerve, was insufficient to account for behavioural performance. In contrast the neural suppression seen in the inferior colliculus and auditory cortex was much closer to psychophysical performance. In anaesthetised guinea-pigs, using a physiological two-interval forced-choice threshold tracking algorithm to estimate suppressed (masked) thresholds, we examine whether the enhancement of suppression can occur at an earlier stage of the auditory pathway, the ventral cochlear nucleus (VCN). We also compare these responses with the responses from the central nucleus of the inferior colliculus (ICc) using the same preparation. In both nuclei, onset-type neurons showed the greatest amounts of suppression (16.9-33.5dB) and, in the VCN, these recovered with the fastest time constants (14.1-19.9ms). Neurons with sustained discharge demonstrated reduced masking (8.9-12.1dB) and recovery time constants of 27.2-55.6ms. In the VCN the decrease in growth of suppression with increasing suppressor level was largest for chopper units and smallest for onset-type units. The threshold elevations recorded for most unit types are insufficient to account for the magnitude of forward masking as measured behaviourally, however, onset responders, in both the cochlear nucleus and inferior colliculus demonstrate a wide dynamic range of suppression, similar to that observed in human psychophysics.

Neural correlates of auditory streaming in an objective behavioral task.

Segregating streams of sounds from sources in complex acoustic scenes is crucial for perception in real world situations. We analyzed an objective psychophysical measure of stream segregation obtained while simultaneously recording forebrain neurons in the European starlings to investigate neural correlates of segregating a stream of A tones from a stream of B tones presented at one-half the rate. The objective measure, sensitivity for time shift detection of the B tone, was higher when the A and B tones were of the same frequency (one stream) compared with when there was a 6- or 12-semitone difference between them (two streams). The sensitivity for representing time shifts in spiking patterns was correlated with the behavioral sensitivity. The spiking patterns reflected the stimulus characteristics but not the behavioral response, indicating that the birds' primary cortical field represents the segregated streams, but not the decision process.

Auditory streaming by phase relations between components of harmonic complexes: a comparative study of human subjects and bird forebrain neurons.

Auditory streaming describes a percept in which a sequential series of sounds either is segregated into different streams or is integrated into one stream based on differences in their spectral or temporal characteristics. This phenomenon has been analyzed in human subjects (psychophysics) and European starlings (neurophysiology), presenting harmonic complex (HC) stimuli with different phase relations between their frequency components. Such stimuli allow evaluating streaming by temporal cues, as these stimuli only vary in the temporal waveform but have identical amplitude spectra. The present study applied the commonly used ABA- paradigm (van Noorden, 1975) and matched stimulus sets in psychophysics and neurophysiology to evaluate the effects of fundamental frequency (f0), frequency range (f(LowCutoff)), tone duration (TD), and tone repetition time (TRT) on streaming by phase relations of the HC stimuli. By comparing the percept of humans with rate or temporal responses of avian forebrain neurons, a neuronal correlate of perceptual streaming of HC stimuli is described. The differences in the pattern of the neurons' spike rate responses provide for a better explanation for the percept observed in humans than the differences in the temporal responses (i.e., the representation of the periodicity in the timing of the action potentials). Especially for HC stimuli with a short 40-ms duration, the differences in the pattern of the neurons' temporal responses failed to represent the patterns of human perception, whereas the neurons' rate responses showed a good match. These results suggest that differential rate responses are a better predictor for auditory streaming by phase relations than temporal responses.

Neural correlates of auditory streaming of harmonic complex sounds with different phase relations in the songbird forebrain.

It has been suggested that successively presented sounds that are perceived as separate auditory streams are represented by separate populations of neurons. Mostly, spectral separation in different peripheral filters has been identified as the cue for segregation. However, stream segregation based on temporal cues is also possible without spectral separation. Here we present sequences of ABA- triplet stimuli providing only temporal cues to neurons in the European starling auditory forebrain. A and B sounds (125 ms duration) were harmonic complexes (fundamentals 100, 200, or 400 Hz; center frequency and bandwidth chosen to fit the neurons' tuning characteristic) with identical amplitude spectra but different phase relations between components (cosine, alternating, or random phase) and presented at different rates. Differences in both rate responses and temporal response patterns of the neurons when stimulated with harmonic complexes with different phase relations provide first evidence for a mechanism allowing a separate neural representation of such stimuli. Recording sites responding >1 kHz showed enhanced rate and temporal differences compared with those responding at lower frequencies. These results demonstrate a neural correlate of streaming by temporal cues due to the variation of phase that shows striking parallels to observations in previous psychophysical studies.

Auditory streaming of amplitude-modulated sounds in the songbird forebrain.

Streaming in auditory scene analysis refers to the perceptual grouping of multiple interleaved sounds having similar characteristics while sounds with different characteristics are segregated. In human perception, auditory streaming occurs on the basis of temporal features of sounds such as the rate of amplitude modulation. We present results from multiunit recordings in the auditory forebrain of awake European starlings (Sturnus vulgaris) on the representation of sinusoidally amplitude modulated (SAM) tones to investigate the effect of temporal envelope structure on neural stream segregation. Different types of rate modulation transfer functions in response to SAM tones were observed. The strongest responses were found for modulation frequencies (fmod) <160 Hz. The streaming stimulus consisted of sequences of alternating SAM tones with the same carrier frequency but differing in fmod (ABA-ABA-ABA-...). A signals had a modulation frequency evoking a large excitation, whereas the fmod of B signals was