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Wednesday, May 28, 2014

Neural Synchrony Disorders: Opening a Biological Umbrella
By Nina Kraus, PhD
Dr. Kraus is professor in the Departments of Communication Sciences, Neurobiology & Physiology, and Otolaryngology at Northwestern University, as well as director of the Auditory Neuroscience Laboratory (brainvolts.northwestern.edu) there, investigating the neurobiology underlying speech and music perception and learning-associated brain plasticity.
 
In the early 1980s, a young man came to my lab. His parents were deeply frustrated. Although their son was bright and precocious, he had substantial hearing problems.
 
He responded inconsistently to sound and exhibited large discrepancies between his excellent visual cognition and poor auditory skills. The young man had normal audiometric thresholds, yet his auditory brainstem response (ABR) was absent.
 
This year marks the 30th anniversary of the paper in which we presented his case, and several others, identifying the dyssynchrony disorder that is now called auditory neuropathy (AN; Laryngoscope 1984;94[3]:400-406).
 
The field has come a long way since then, and we now view neuropathy as a spectrum encompassing several pathologies, including disorders of the brainstem, auditory nerve, and ribbon synapses (Brain 1996;119[pt 3]:741-753; J Basic Clin Physiol Pharmacol 2000;11[3]:215-230).
 
In this editorial, I propose we extend that spectrum to include another confounding and frustrating condition that audiologists must tackle: central auditory processing disorder (APD). That is, I propose we view both conditions under the biological umbrella of neural synchrony.
 
INCONSISTENT NEURAL FIRING
Auditory neuropathy and auditory processing disorder are characterized by normal cochlear function, at least as evaluated by conventional tests, coupled with downstream (central) dysfunction.
 
Both patient groups have problems with auditory attention and excessive difficulty understanding speech when the signal is degraded or the listening environment is acoustically challenging (Nature 1997;387[6629]:176-178).
 
Whereas patients with AN are deaf in noise (J Assoc Res Otolaryngol 2000;1[1]:33-45), those with APD understand speech much better, albeit abnormally.
 
We have investigated the neurobiology of APD, and of language-learning problems more broadly, using the auditory frequency following response (FFR), a variant of the ABR.
 
Like the auditory brainstem response, the FFR is generated by summed synchronous firing of brainstem nuclei. The FFR is the product of sustained phase locking to periodic sounds (Ear Hear 2010;31[3]:302-324).
 
The auditory brainstem response to complex sounds (cABR) combines processing of sustained and transient acoustic features.
 
Unlike the ABR, the frequency following response reflects the confluence of cognitive and sensory processing. (Kraus N, Nicol T. The cognitive auditory system: the role of learning in shaping the biology of the auditory system. In: Popper AN, Fay RR, eds. Perspectives on Auditory Research. Heidelberg: Springer–Verlag; 2014: 299-319.)
 
My lab has developed techniques to evaluate the trial-by-trial consistency of the FFR in response to speech sounds. These experiments have revealed the systematic relationship of reading and language ability with FFR consistency (J Neurosci 2013;33[8]:3500-3504).
 
FFR consistency improves through early childhood (Cereb Cortex 2013; doi: 10.1093/cercor/bht311); children with auditory processing disorder may experience deviant or developmentally delayed responses.
 
With older age, consistency declines, again in keeping with age-related difficulties in temporal processing and speech-in-noise understanding (J Neurosci 2012;32[41]:14156-14164).
 
Our findings suggest that subcortical neural synchrony exists on a continuum that tracks with auditory skills and, I believe, represents the bottleneck in a substantial number of auditory processing disorder cases.
 
Inconsistent neural firing in response to speech may prevent the meaningful interactions with sound that support auditory–cognitive skills and reinforce precise auditory processing.
 
The exact neurophysiological mechanisms underlying this spectrum of dyssynchrony remain open to question but likely include cochlear mechanics (Hearing Balance Commun 2013;11[3]:160-167), central inhibitory processes (J Exp Biol 2008;211[pt 11]:1781-1791), and descending input from the auditory cortex (Front Neural Circuits 2013;6:114).
 
Certain cases of dyssynchrony are treatable. We have shown that assistive listening devices (Proc Natl Acad Sci U S A 2012;109[41]:16731-16736) and auditory training, including music (Front Aging Neurosci 2012;4:30), language experience (Brain Lang 2014;128[1]:34-40), and computer training (Proc Natl Acad Sci U S A 2013;110[11]:4357-4362), improve neural synchrony and communication skills.