Travis White-Schwoch

Aging affects neural precision of speech encoding.

Older adults frequently report they can hear what is said but cannot understand the meaning, especially in noise. This difficulty may arise from the inability to process rapidly changing elements of speech. Aging is accompanied by a general slowing of neural processing and decreased neural inhibition, both of which likely interfere with temporal processing in auditory and other sensory domains. Age-related reductions in inhibitory neurotransmitter levels and delayed neural recovery can contribute to decreases in the temporal precision of the auditory system. Decreased precision may lead to neural timing delays, reductions in neural response magnitude, and a disadvantage in processing the rapid acoustic changes in speech. The auditory brainstem response (ABR), a scalp-recorded electrical potential, is known for its ability to capture precise neural synchrony within subcortical auditory nuclei; therefore, we hypothesized that a loss of temporal precision results in subcortical timing delays and decreases in response consistency and magnitude. To assess this hypothesis, we recorded ABRs to the speech syllable /da/ in normal hearing younger (18–30 years old) and older (60–67 years old) adult humans. Older adults had delayed ABRs, especially in response to the rapidly changing formant transition, and greater response variability. We also found that older adults had decreased phase locking and smaller response magnitudes than younger adults. Together, our results support the theory that older adults have a loss of temporal precision in the subcortical encoding of sound, which may account, at least in part, for their difficulties with speech perception.

Reversal of age-related neural timing delays with training

Neural slowing is commonly noted in older adults, with consequences for sensory, motor, and cognitive domains. One of the deleterious effects of neural slowing is impairment of temporal resolution; older adults, therefore, have reduced ability to process the rapid events that characterize speech, especially in noisy environments. Although hearing aids provide increased audibility, they cannot compensate for deficits in auditory temporal processing. Auditory training may provide a strategy to address these deficits. To that end, we evaluated the effects of auditory-based cognitive training on the temporal precision of subcortical processing of speech in noise. After training, older adults exhibited faster neural timing and experienced gains in memory, speed of processing, and speech-in-noise perception, whereas a matched control group showed no changes. Training was also associated with decreased variability of brainstem response peaks, suggesting a decrease in temporal jitter in response to a speech signal. These results demonstrate that auditory-based cognitive training can partially restore age-related deficits in temporal processing in the brain; this plasticity in turn promotes better cognitive and perceptual skills.

A dynamic auditory-cognitive system supports speech-in-noise perception in older adults

Understanding speech in noise is one of the most complex activities encountered in everyday life, relying on peripheral hearing, central auditory processing, and cognition. These abilities decline with age, and so older adults are often frustrated by a reduced ability to communicate effectively in noisy environments. Many studies have examined these factors independently; in the last decade, however, the idea of an auditory-cognitive system has emerged, recognizing the need to consider the processing of complex sounds in the context of dynamic neural circuits. Here, we used structural equation modeling to evaluate the interacting contributions of peripheral hearing, central processing, cognitive ability, and life experiences to understanding speech in noise. We recruited 120 older adults (ages 55-79) and evaluated their peripheral hearing status, cognitive skills, and central processing. We also collected demographic measures of life experiences, such as physical activity, intellectual engagement, and musical training. In our model, central processing and cognitive function predicted a significant proportion of variance in the ability to understand speech in noise. To a lesser extent, life experience predicted hearing-in-noise ability through modulation of brainstem function. Peripheral hearing levels did not significantly contribute to the model. Previous musical experience modulated the relative contributions of cognitive ability and lifestyle factors to hearing in noise. Our models demonstrate the complex interactions required to hear in noise and the importance of targeting cognitive function, lifestyle, and central auditory processing in the management of individuals who are having difficulty hearing in noise.

Older Adults Benefit from Music Training Early in Life: Biological Evidence for Long-Term Training-Driven Plasticity

Aging results in pervasive declines in nervous system function. In the auditory system, these declines include neural timing delays in response to fast-changing speech elements; this causes older adults to experience difficulty understanding speech, especially in challenging listening environments. These age-related declines are not inevitable, however: older adults with a lifetime of music training do not exhibit neural timing delays. Yet many people play an instrument for a few years without making a lifelong commitment. Here, we examined neural timing in a group of human older adults who had nominal amounts of music training early in life, but who had not played an instrument for decades. We found that a moderate amount (4–14 years) of music training early in life is associated with faster neural timing in response to speech later in life, long after training stopped (>40 years). We suggest that early music training sets the stage for subsequent interactions with sound. These experiences may interact over time to sustain sharpened neural processing in central auditory nuclei well into older age.

Beat synchronization predicts neural speech encoding and reading readiness in preschoolers

Significance Sensitivity to fine timing cues in speech is thought to play a key role in language learning, facilitating the development of phonological processing. In fact, a link between beat synchronization, which requires fine auditory–motor synchrony, and language skills has been found in school-aged children, as well as adults. Here, we show this relationship between beat entrainment and language metrics in preschoolers and use beat synchronization ability to predict the precision of neural encoding of speech syllables in these emergent readers. By establishing links between beat keeping, neural precision, and reading readiness, our results provide an integrated framework that offers insights into the preparative biology of reading. Temporal cues are important for discerning word boundaries and syllable segments in speech; their perception facilitates language acquisition and development. Beat synchronization and neural encoding of speech reflect precision in processing temporal cues and have been linked to reading skills. In poor readers, diminished neural precision may contribute to rhythmic and phonological deficits. Here we establish links between beat synchronization and speech processing in children who have not yet begun to read: preschoolers who can entrain to an external beat have more faithful neural encoding of temporal modulations in speech and score higher on tests of early language skills. In summary, we propose precise neural encoding of temporal modulations as a key mechanism underlying reading acquisition. Because beat synchronization abilities emerge at an early age, these findings may inform strategies for early detection of and intervention for language-based learning disabilities.

Unraveling the Biology of Auditory Learning: A Cognitive-Sensorimotor- Reward Framework

The auditory system is stunning in its capacity for change: a single neuron can modulate its tuning in minutes. Here we articulate a conceptual framework to understand the biology of auditory learning where an animal must engage cognitive, sensorimotor, and reward systems to spark neural remodeling. Central to our framework is a consideration of the auditory system as an integrated whole that interacts with other circuits to guide and refine life in sound. Despite our emphasis on the auditory system, these principles may apply across the nervous system. Understanding neuroplastic changes in both normal and impaired sensory systems guides strategies to improve everyday communication.

Effects of hearing loss on the subcortical representation of speech cues

Individuals with sensorineural hearing loss often report frustration with speech being loud but not clear, especially in background noise. Despite advanced digital technology, hearing aid users may resort to removing their hearing aids in noisy environments due to the perception of excessive loudness. In an animal model, sensorineural hearing loss results in greater auditory nerve coding of the stimulus envelope, leading to a relative deficit of stimulus fine structure. Based on the hypothesis that brainstem encoding of the temporal envelope is greater in humans with sensorineural hearing loss, speech-evoked brainstem responses were recorded in normal hearing and hearing impaired age-matched groups of older adults. In the hearing impaired group, there was a disruption in the balance of envelope-to-fine structure representation compared to that of the normal hearing group. This imbalance may underlie the difficulty experienced by individuals with sensorineural hearing loss when trying to understand speech in background noise. This finding advances the understanding of the effects of sensorineural hearing loss on central auditory processing of speech in humans. Moreover, this finding has clinical potential for developing new amplification or implantation technologies, and in developing new training regimens to address this relative deficit of fine structure representation.

Auditory Processing in Noise: A Preschool Biomarker for Literacy

Learning to read is a fundamental developmental milestone, and achieving reading competency has lifelong consequences. Although literacy development proceeds smoothly for many children, a subset struggle with this learning process, creating a need to identify reliable biomarkers of a child’s future literacy that could facilitate early diagnosis and access to crucial early interventions. Neural markers of reading skills have been identified in school-aged children and adults; many pertain to the precision of information processing in noise, but it is unknown whether these markers are present in pre-reading children. Here, in a series of experiments in 112 children (ages 3–14 y), we show brain–behavior relationships between the integrity of the neural coding of speech in noise and phonology. We harness these findings into a predictive model of preliteracy, revealing that a 30-min neurophysiological assessment predicts performance on multiple pre-reading tests and, one year later, predicts preschoolers’ performance across multiple domains of emergent literacy. This same neural coding model predicts literacy and diagnosis of a learning disability in school-aged children. These findings offer new insight into the biological constraints on preliteracy during early childhood, suggesting that neural processing of consonants in noise is fundamental for language and reading development. Pragmatically, these findings open doors to early identification of children at risk for language learning problems; this early identification may in turn facilitate access to early interventions that could prevent a life spent struggling to read.

Training changes processing of speech cues in older adults with hearing loss

Aging results in a loss of sensory function, and the effects of hearing impairment can be especially devastating due to reduced communication ability. Older adults with hearing loss report that speech, especially in noisy backgrounds, is uncomfortably loud yet unclear. Hearing loss results in an unbalanced neural representation of speech: the slowly-varying envelope is enhanced, dominating representation in the auditory pathway and perceptual salience at the cost of the rapidly-varying fine structure. We hypothesized that older adults with hearing loss can be trained to compensate for these changes in central auditory processing through directed attention to behaviorally-relevant speech sounds. To that end, we evaluated the effects of auditory-cognitive training in older adults (ages 55–79) with normal hearing and hearing loss. After training, the auditory training group with hearing loss experienced a reduction in the neural representation of the speech envelope presented in noise, approaching levels observed in normal hearing older adults. No changes were noted in the control group. Importantly, changes in speech processing were accompanied by improvements in speech perception. Thus, central processing deficits associated with hearing loss may be partially remediated with training, resulting in real-life benefits for everyday communication.

Partial maintenance of auditory-based cognitive training benefits in older adults

The potential for short-term training to improve cognitive and sensory functions in older adults has captured the publics interest. Initial results have been promising. For example, eight weeks of auditory-based cognitive training decreases peak latencies and peak variability in neural responses to speech presented in a background of noise and instills gains in speed of processing, speech-in-noise recognition, and short-term memory in older adults. But while previous studies have demonstrated short-term plasticity in older adults, we must consider the long-term maintenance of training gains. To evaluate training maintenance, we invited participants from an earlier training study to return for follow-up testing six months after the completion of training. We found that improvements in response peak timing to speech in noise and speed of processing were maintained, but the participants did not maintain speech-in-noise recognition or memory gains. Future studies should consider factors that are important for training maintenance, including the nature of the training, compliance with the training schedule, and the need for booster sessions after the completion of primary training.