Aging Affects Neural Precision of Speech Encoding

Abstract

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 auditory system’s temporal precision. 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 (ages 18 to 30) and older adult humans (60 to 67). 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. Taken together, our results support the theory that older adults have a loss of temporal precision in subcortical encoding of sound, which may account, at least in part, for their difficulties with speech perception.

Age-Related Changes in Processing Simultaneous Amplitude Modulated Sounds Assessed Using Envelope Following Responses

“…However, these compensatory mechanisms come at the cost of reduced synchrony of neural representations (Rabang et al 2012). This could result in the some of the decreased EFR amplitudes with age observed in this study and elsewhere (Clinard et al 2010;Parthasarathy and Bartlett 2011;Anderson et al 2012). However, modeling the loss of AN fibers and synapses recreated the majority of the trends observed due to age in this study, suggesting peripheral contributions for the decrease in EFR amplitudes at high SNRs and large AM depths.…”

Losing the Music: Aging Affects the Perception and Subcortical Neural Representation of Musical Harmony

“…There is a growing body of evidence demonstrating age-related deficits in temporal processing independently of hearing loss (Strouse et al, 1998;Clinard et al, 2010;Hopkins and Moore, 2011;Anderson et al, 2012;Neher et al, 2012;Ruggles et al, 2012;Marmel et al, 2013). Clinard et al (2010) found that age predicted pitch discrimination and magnitude of the FFR at the stimulus frequency, but did not find a significant correlation between the two measures.…”

Age-Related Changes in the Relationship Between Auditory Brainstem Responses and Envelope-Following Responses

“…Wave amplitudes measured from ABRs also provide insight into the representation of phasic information to short stimuli, based on clearly defined peaks that have been mapped onto specific generators in the auditory brainstem and midbrain (Lev and Sohmer 1972;Rowe 1981;Chen and Chen 1991). Frequency-following responses (FFRs) to tonal carriers or to the modulation envelope (envelopefollowing responses or EFRs), though still not widely used in the clinic, are rapidly gaining prominence as a means of assessing processing of complex sounds from the auditory pathway (Cunningham et al 2001;Aiken and Picton 2008;Swaminathan et al 2008;Basu et al 2010;Clinard et al 2010;Krishnan et al 2010;Parbery-Clark et al 2011;Anderson et al 2012). FFRs and EFRs are evoked in response to longer, often more spectro-temporally complex stimuli (Krishnan 1999(Krishnan , 2002Krishnan et al 2004;Swaminathan et al 2008), and are strongly influenced by rostral brainstem and midbrain generators (Kiren et al 1994;Kuwada et al 2002;Akhoun et al 2010;Chandrasekaran and Kraus 2010;Parthasarathy and Bartlett 2012).…”

“…FFRs and EFRs are evoked in response to longer, often more spectro-temporally complex stimuli (Krishnan 1999(Krishnan , 2002Krishnan et al 2004;Swaminathan et al 2008), and are strongly influenced by rostral brainstem and midbrain generators (Kiren et al 1994;Kuwada et al 2002;Akhoun et al 2010;Chandrasekaran and Kraus 2010;Parthasarathy and Bartlett 2012). They have been used to show differences in processing of complex stimuli under various pathological conditions, such as age-related hearing loss, dyslexia, and autism (McAnally and Stein 1997;Chandrasekaran et al 2009;Russo et al 2009;Anderson et al 2012;Clinard and Tremblay 2013).…”

“…Among listeners with matched thresholds, the actual amplitudes of the ABR waves are significantly lower with age (Boettcher et al 1993;Konrad-Martin et al 2012). Human studies using FFRs have found changes in neural timing and precision with age (Tremblay et al 2002(Tremblay et al , 2003Clinard et al 2010;Anderson et al 2012;Clinard and Tremblay 2013). Changes with age have also been observed at the level of single neurons in terms of decreased temporal coding and changes in rate coding in the dorsal cochlear nuclei (Schatteman et al 2008), inferior colliculus (IC) (Walton et al 1998;Palombi et al 2001;Walton et al 2002;Walton 2010;Rabang et al 2012), and auditory cortex (Mendelson and Ricketts 2001) and at a population level using EFRs in rodent aging models (Parthasarathy et al 2010;Parthasarathy and Bartlett 2011;Parthasarathy and Bartlett 2012).…”