Scale-Free Neural and Physiological Dynamics in Naturalistic Stimuli Processing

• Published in: eNeuro Vol. 3; no. 5; p. ENEURO.0191-16.2016
• Main Authors: Lin, Amy, Maniscalco, Brian, He, Biyu J.
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 01.09.2016
• Subjects: Acoustic Stimulation; Adult; Alpha Rhythm; Auditory Perception - physiology; Brain - physiology; Discrimination (Psychology) - physiology; Electrocardiography; Female; Heart Rate; Humans; Magnetoencephalography; Male; Neuropsychological Tests; New Research; Rest; Signal Processing, Computer-Assisted; Time Factors; Young Adult; slow cortical potentials; scale-free dynamics; natural stimuli; α oscillations; heart rate variability; arrhythmic brain activity
• ISSN: 2373-2822; 2373-2822
• DOI: 10.1523/ENEURO.0191-16.2016

Neural activity recorded at multiple spatiotemporal scales is dominated by arrhythmic fluctuations without a characteristic temporal periodicity. Such activity often exhibits a 1/ f -type power spectrum, in which power falls off with increasing frequency following a power-law function: P ( f ) ∝ 1 / f β , which is indicative of scale-free dynamics. Two extensively studied forms of scale-free neural dynamics in the human brain are slow cortical potentials (SCPs)—the low-frequency (<5 Hz) component of brain field potentials—and the amplitude fluctuations of α oscillations, both of which have been shown to carry important functional roles. In addition, scale-free dynamics characterize normal human physiology such as heartbeat dynamics. However, the exact relationships among these scale-free neural and physiological dynamics remain unclear. We recorded simultaneous magnetoencephalography and electrocardiography in healthy subjects in the resting state and while performing a discrimination task on scale-free dynamical auditory stimuli that followed different scale-free statistics. We observed that long-range temporal correlation (captured by the power-law exponent β) in SCPs positively correlated with that of heartbeat dynamics across time within an individual and negatively correlated with that of α-amplitude fluctuations across individuals. In addition, across individuals, long-range temporal correlation of both SCP and α-oscillation amplitude predicted subjects’ discrimination performance in the auditory task, albeit through antagonistic relationships. These findings reveal interrelations among different scale-free neural and physiological dynamics and initial evidence for the involvement of scale-free neural dynamics in the processing of natural stimuli, which often exhibit scale-free dynamics.