The remarkable signal-detection capabilities of the auditory and vestibular systems have been studied for decades. Much of the conceptual framework that arose from this research has suggested that these sensory systems rest on the verge of instability, near a Hopf bifurcation, in order to explain the detection specifications. However, this paradigm contains several unresolved issues. Critical systems are not robust to stochastic fluctuations or imprecise tuning of the system parameters. Further, a system poised at criticality exhibits a phenomenon known in dynamical systems theory as
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The auditory and vestibular systems exhibit remarkable sensitivity of detection, responding to deflections on the order of angstroms, even in the presence of biological noise. The auditory system exhibits high temporal acuity and frequency selectivity, allowing us to make sense of the acoustic world around us. As the acoustic signals of interest span many orders of magnitude in both amplitude and frequency, this system relies heavily on nonlinearities and power-law scaling. The vestibular system, which detects ground-borne vibrations and creates the sense of balance, exhibits highly sensitive, broadband detection. It likewise requires high temporal acuity so as to allow us to maintain balance while in motion. The behavior of these sensory systems has been extensively studied in the context of dynamical systems theory, with many empirical phenomena described by critical dynamics. Other phenomena have been explained by systems in the chaotic regime, where weak perturbations drastically impact the future state of the system. Using a Hopf oscillator as a simple numerical model for a sensory element in these systems, we explore the intersection of the two types of dynamical phenomena. We identify the relative tradeoffs between different detection metrics, and propose that, for both types of sensory systems, the instabilities giving rise to chaotic dynamics improve signal detection.
more » « less- Award ID(s):
- 2210316
- PAR ID:
- 10522947
- Publisher / Repository:
- Nature
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 14
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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critical slowing down , where the response time diverges as the system approaches the critical point. An alternative description of these sensory systems is based on the notion of chaotic dynamics, where the instabilities inherent to the dynamics produce high temporal acuity and sensitivity to weak signals, even in the presence of noise. This alternative description resolves the issues that arise in the criticality picture. We review the conceptual framework and experimental evidence that supports the use of chaos for signal detection by these systems, and propose future validation experiments. -
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Abstract Hair cells of the auditory and vestibular systems are capable of detecting sounds that induce sub-nanometer vibrations of the hair bundle, below the stochastic noise levels of the surrounding fluid. Furthermore, the auditory system exhibits a highly rapid response time, in the sub-millisecond regime. We propose that chaotic dynamics enhance the sensitivity and temporal resolution of the hair bundle response, and we provide experimental and theoretical evidence for this effect. We use the Kolmogorov entropy to measure the degree of chaos in the system and the transfer entropy to quantify the amount of stimulus information captured by the detector. By varying the viscosity and ionic composition of the surrounding fluid, we are able to experimentally modulate the degree of chaos observed in the hair bundle dynamics
in vitro . We consistently find that the hair bundle is most sensitive to a stimulus of small amplitude when it is poised in the weakly chaotic regime. Further, we show that the response time to a force step decreases with increasing levels of chaos. These results agree well with our numerical simulations of a chaotic Hopf oscillator and suggest that chaos may be responsible for the high sensitivity and rapid temporal response of hair cells. -
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Abstract Hearing impairment is a frequent clinical feature in patients with mitochondrial disease harbouring the pathogenic variant, m.3243A>G. However, auditory neural dysfunction, its perceptual consequences and implications for patient management are not established. Similarly, the association with vestibular impairment has not yet been explored. This case–control study investigated in 12 adults with genetically confirmed m.3243A>G adults [9 females; 45.5 ± 16.3 years (range 18–66); 47.1 ± 21.5 hearing level, dB] compared with 12 age, sex and hearing level-matched controls with sensory (cochlear level) hearing loss [9 females; 46.6 ± 11.8 years (range 23–59); 47.7 ± 25.4 hearing level, dB]. Participants underwent a battery of electroacoustic, electrophysiologic and perceptual tests, which included pure tone audiometry, otoacoustic emissions, auditory brainstem responses, auditory temporal processing measures, monaural/binaural speech perception, balance and vestibular testing and self-reported questionnaires (dizziness and hearing disability). Our findings showed evidence of auditory neural abnormality and perceptual deficits greater than expected for cochlear pathology. Compared with matched controls with sensory hearing loss, adults with mitochondrial disease harbouring m.3243A>G had abnormal electrophysiologic responses from the VIII nerve and auditory brainstem (P = 0.005), an impaired capacity to encode rapidly occurring acoustic signal changes (P = 0.005), a reduced ability to localize sound sources (P = 0.028) and impaired speech perception in background noise (P = 0.008). Additionally, vestibular dysfunction (P = 0.011), greater perceived dizziness (P = 0.001) and reduced stance time (balance, P = 0.009) were also seen in participants with m.3243A>G mitochondrial disease when compared with matched counterparts. This pilot study revealed that auditory evaluation including evoked potential responses from the auditory nerve/brainstem and speech perception in noise tests should form an important part of the management for individuals with m.3243A>G-related mitochondrial disease. Those presenting with hearing impairment and symptoms concerning balance and dizziness should undergo vestibular testing and appropriate management.
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The vestibular system (VS) allows humans to have a sense of balance and orientation. Within the VS, fluid displacement occurs within the ear canal, triggering nerve signals to be translated by the nervous system, allowing for the interpretation of the head's orientation. When there is a disturbance to this system, vestibular dysfunction occurs potentially causing vertigo and a loss of balance. It is estimated that 35 percent of adults 40 years or older in the United States have experienced vestibular dysfunction. The vestibular balance system poses a robust, unique topic for developing interdisciplinary education curricula as its function encapsulates many fundamental mechanical, chemical, biological, and physical phenomena that can be studied with engineering concepts and principles. In this work, we present a survey of models of the vestibular sensory system. Following which, selected models are presented in an experiential learning format for students to better understand the relationship and sensitivity of model parameters and external stimuli to physiological system behavior. By conducting simulations of these models, students can visualize outcomes, pose questions, and potentially identify areas of research interest. This paper is the outcome of an Innovations in Graduate Education project supported by the National Science Foundation. The authors are graduate students from three engineering majors from the University of Massachusetts Lowell and the University of the District of Columbia co-creating an educational module with faculty and experts on human balance. The developed module related to analyzing the vestibular balance system mechanics will be integrated into undergraduate courses across engineering departments in partnering institutions.more » « less
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The vestibular system (VS) allows humans to have a sense of balance and orientation. Within the VS, fluid displacement occurs within the ear canal, triggering nerve signals to be translated by the nervous system, allowing for the interpretation of the head's orientation. When there is a disturbance to this system, vestibular dysfunction occurs potentially causing vertigo and a loss of. balance. It is estimated that 35 percent of adults 40 years or older in the United States have experienced vestibular dysfunction. The vestibular balance system poses a robust, unique topic for developing interdisciplinary education curricula as its function encapsulates many fundamental mechanical, chemical, biological, and physical phenomena that can be studied with engineering concepts and principles. In this work, we present a survey of models of the vestibular sensory system. Following which, selected models are presented in an experiential learning format for students to better understand the relationship and sensitivity of model parameters and external stimuli to physiological system behavior. By conducting simulations of these models, students can visualize outcomes, pose questions, and potentially identify areas of research interest. This paper is the outcome of an Innovations in Graduate Education project supported by the National Science Foundation. The authors are graduate students from three engineering majors from the University of Massachusetts Lowell and the University of the District of Columbia co-creating an educational module with faculty and experts on human balance. The developed module related to analyzing the vestibular balance system mechanics will be integrated into undergraduate courses across engineering departments in partnering institutions.more » « less
