Rapid ocular responses are modulated by bottom-up driven auditory salience

• Published in: The Journal of neuroscience Vol. 39; no. 39; pp. 7703 - 7714
• Main Authors: Zhao, Sijia, Wai Yum, Nga, Benjamin, Lucas, Benhamou, Elia, Yoneya, Makoto, Furukawa, Shigeto, Dick, Fred, Slaney, Malcolm, Chait, Maria
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 25.09.2019
• Subjects: Acoustics; Attention; Auditory system; Brain; Correlation analysis; Crowdsourcing; Early warning systems; Freezing; Hearing; Orienting response; Roughness; Salience; Sound; Superior colliculus
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.0776-19.2019

Despite the prevalent use of alerting sounds in alarms and human-machine interface systems and the long-hypothesized role of the auditory system as the brain's 'early warning system', we have only a rudimentary understanding of what determines auditory salience-the automatic attraction of attention by sound-and which brain mechanisms underlie this process. A major roadblock has been the lack of a robust, objective means of quantifying sound-driven attentional capture. Here we demonstrate that: (1) a reliable salience scale can be obtained from crowd-sourcing (N=911), (2) acoustic roughness appears to be a driving feature behind this scaling, consistent with previous reports which implicate roughness in the perceptual distinctiveness of sounds, and (3) crowdsourced auditory salience correlates with objective autonomic measures. Specifically, we show that a salience ranking obtained from online raters correlated robustly with the superior colliculus (SC)-mediated ocular freezing response - microsaccadic inhibition (MSI) - measured in naïve, passively listening human participants (of either sex). More salient sounds evoked earlier MSI, consistent with a faster orienting response. These results are in line with the hypothesis that MSI reflects a general re-orienting response which is evoked by potentially behaviorally important events irrespective of their modality. Microsaccades are small, rapid, fixational eye movements, measurable with sensitive eye-tracking equipment. We reveal a novel, robust link between microsaccade dynamics and the subjective salience of brief sounds (salience rankings obtained from a large number of participants in an online experiment): Within 300 ms of sound onset, the eyes of naïve, passively listening participants demonstrate different microsaccade patterns as a function of the sound's crowdsourced salience. These results position the superior colliculus (hypothesized to underlie microsaccade generation) as an important brain area to investigate in the context of a putative multi-modal salience-hub. They also demonstrate an objective means for quantifying auditory salience.