Training to Improve Hearing Speech in Noise: Biological Mechanisms

Judy H. Song 1 2 3 Erika Skoe 1 2 3 Karen Banai 0 2 Nina Kraus 1 2 3 4 5 0 Department of Communication Sciences and Disorders, University of Haifa , Haifa 31905, Israel 1 Department of Communication Sciences, Northwestern University , Evanston, IL 60208, USA 2 The Author 2011. Published by Oxford University Press. All rights reserved. For permissions , please 3 Auditory Neuroscience Laboratory 4 Department of Otolaryngology, Northwestern University , Evanston, IL 60208, USA 5 Department of Neurobiology and Physiology We investigated training-related improvements in listening in noise and the biological mechanisms mediating these improvements. Training-related malleability was examined using a program that incorporates cognitively based listening exercises to improve speech-in-noise perception. Before and after training, auditory brainstem responses to a speech syllable were recorded in quiet and multitalker noise from adults who ranged in their speech-innoise perceptual ability. Controls did not undergo training but were tested at intervals equivalent to the trained subjects. Trained subjects exhibited significant improvements in speech-in-noise perception that were retained 6 months later. Subcortical responses in noise demonstrated training-related enhancements in the encoding of pitch-related cues (the fundamental frequency and the second harmonic), particularly for the time-varying portion of the syllable that is most vulnerable to perceptual disruption (the formant transition region). Subjects with the largest strength of pitch encoding at pretest showed the greatest perceptual improvement. Controls exhibited neither neurophysiological nor perceptual changes. We provide the first demonstration that shortterm training can improve the neural representation of cues important for speech-in-noise perception. These results implicate and delineate biological mechanisms contributing to learning success, and they provide a conceptual advance to our understanding of the kind of training experiences that can influence sensory processing in adulthood. Introduction In everyday listening situations, accurate speech perception relies on the capacity of the auditory system to process complex sounds in the presence of background noise. This process is often challenging even for young adults with normal hearing and normal cognitive abilities (Neff and Green 1987; Assmann and Summerfield 2004). In this study, we examined the extent to which speech-in-noise perception improved for young adult listeners who have undergone auditory training exercises that mimic real-world listening conditions, such as listening to a target speaker amid multiple background speakers. In addition, we measured the effects of this training on aspects of auditory brainstem processing that underlie speech perception in noise and the extent to which brainstem encoding of speech could predict learning success. There is ample evidence of auditory training resulting in perceptual enhancements (Wright et al. 1997; Amitay et al. 2005; Moore et al. 2005; Mossbridge et al. 2006; Johnston et al. 2009) as well as plasticity in single neurons (Kraus and Disterhoft 1982; Diamond and Weinberger 1984, 1986, 1989) and neuronal populations (Olds et al. 1972; Bakin and Weinberger 1990; Recanzone et al. 1992; Edeline et al. 1993; Weinberger 1993; Gaab et al. 2006). In humans, learning-related cortical plasticity has been found after discrimination training using tones (Naatanen et al. 1993) and synthetic speech stimuli (Kraus et al. 1995; Tremblay et al. 2001, 2009). However, there have been surprisingly few investigations of how training impacts speech-in-noise perception (Burk and Humes 2007; Cainer et al. 2008; Yund and Woods 2010). These studies, which used small stimulus sets, indicate that while speech-innoise perception can improve when training on words or sentences in artificial listening conditions, generalization to untrained materials is limited. These findings suggest that learning resulting from such training paradigms is specific to the trained speech materials and the parameters of the background noise (i.e., signal-to-noise ratio [SNR], babble vs. white noise, etc.) (Burk et al. 2006; Yund and Woods 2010). Nevertheless, long term auditory training (musical training) can improve speech perception under challenging conditions (Parbery-Clark et al. 2009a, Parbery-Clark et al. 2011, Bidelman and Krishnan 2010). To investigate the biological mechanisms driving neural changes under more naturalistic conditions, we used a training program that has been shown to benefit speechin-noise perception in older adults. This commercially available program, Listening and Communication Enhancement (LACE), utilizes a large stimulus set (i.e., open-set speech material presented in a variety of difficult listening conditions often encountered in real life), incorporates feedback, and activates higher level cognitive skillsall of which have been suggested to promote perceptual learning and engender generalization (Kujala et al. 2001; Schaffler et al. 2004; Moore et al. 2005; Moore and Amitay 2007; Smith et al. 2009). This is the first study to examine the effects of speech-innoise training on human subcortical processing of sound. The auditory brainstem response (ABR), a noninvasive objective measurement of brainstem integrity (Hall 1992; Hood 1998), is ideal for examining the biological mechanisms underlying improvements in hearing in noise because the response is stable from session to session even when recorded in the presence of an acoustic masker (Russo et al. 2005; Song, Nicol, et al. 2010a). This response, which is reflective of synchronized potentials produced by populations of neurons along the subcortical auditory pathway (Mller and Jannetta 1985; Chandrasekaran and Kraus 2010), can be elicited by a wide range of acoustic stimuli, including speech syllables (King et al. 2002; Krishnan 2002; Galbraith et al. 2004; Krishnan et al. 2004, 2005; Russo et al. 2004; Xu et al. 2006; Wong, Skoe, et al. 2007; Aiken and Picton 2008; Akhoun et al. 2008; Swaminathan et al. 2008). Brainstem synchronization is so precise that disparities on the order of tenths of milliseconds are clinically significant (Jacobson 1985; Hood 1998). Consequently, even subtle training-related differences in the speech-evoked ABR could be indicative of meaningful neural plasticity. To examine the malleability of the biological mechanisms underlying improvements in speech-in-noise perception, we measured ABRs from a group of young adults immediately before and after auditory training. Because long-term retention of behavioral and neurophysiologic changes has not been demonstrated previously, we also obtained neural and behavioral measurements 6 months after training. Behavioral and neurophysiological measures were also obtained from untrained control subjects at intervals equivalent to the trained group. By including nonnative English speakers into ou (...truncated)