Aging-Resilient Associations between the Arcuate Fasciculus and Vocabulary Knowledge: Microstructure or Morphology?

UNLABELLED: Vocabulary knowledge is one of the few cognitive functions that is relatively preserved in older adults, but the reasons for this relative preservation have not been well delineated. We tested the hypothesis that individual differences in vocabulary knowledge are influenced by arcuate fasciculus macrostructure (i.e., shape and volume) properties that remain stable during the aging process, rather than white matter microstructure that demonstrates age-related declines. Vocabulary was not associated with age compared to pronounced age-related declines in cognitive processing speed across 106 healthy adults (19.92-88.29 years) who participated in this neuroimaging experiment. Fractional anisotropy in the left arcuate fasciculus was significantly related to individual variability in vocabulary. This effect was present despite marked age-related differences in a T1-weighted/T2-weighted ratio (T1w/T2w) estimate of myelin that were observed throughout the left arcuate fasciculus and associated with age-related differences in cognitive processing speed. However, atypical patterns of arcuate fasciculus morphology or macrostructure were associated with decreased vocabulary knowledge. These results suggest that deterioration of tissue in the arcuate fasciculus occurs with normal aging, while having limited impact on tract organization that underlies individual differences in the acquisition and retrieval of lexical and semantic information. SIGNIFICANCE STATEMENT: Vocabulary knowledge is resilient to widespread age-related declines in brain structure that limit other cognitive functions. We tested the hypothesis that arcuate fasciculus morphology, which supports the development of reading skills that bolster vocabulary, could explain this relative preservation. We disentangled (1) the effects of age-related declines in arcuate microstructure (mean diffusivity; myelin content estimate) that predicted cognitive processing speed but not vocabulary, from (2) relatively stable arcuate macrostructure (shape/volume) that explained significant variance in an age-independent association between fractional anisotropy and vocabulary. This latter result may reflect differences in fiber trajectory and organization that are resilient to aging. We propose that developmental sculpting of the arcuate fasciculus determines acquisition, storage, and access of lexical information across the adult lifespan.

Task-Related Vigilance During Word Recognition in Noise for Older Adults with Hearing Loss.

BACKGROUND/STUDY CONTEXT: Vigilance refers to the ability to sustain and adapt attentional focus in response to changing task demands. For older adults with hearing loss, vigilant listening may be particularly effortful and variable across individuals. This study examined the extent to which neural responses to sudden, unexpected changes in task structure (e.g., from rest to word recognition epochs) were related to pupillometry measures of listening effort. METHODS: Individual differences in the task-evoked pupil response during word recognition were used to predict functional magnetic resonance imaging (MRI) estimates of neural responses to salient transitions between quiet rest, noisy rest, and word recognition in unintelligible, fluctuating background noise. Participants included 29 older adults (M = 70.2 years old) with hearing loss (pure tone average across all frequencies = 36.1 dB HL [hearing level], SD = 6.7). RESULTS: Individuals with a greater average pupil response exhibited a more vigilant pattern of responding on a standardized continuous performance test (response time variability across varying interstimulus intervals r(27) = .38, p = .04). Across participants there was widespread engagement of attention- and sensory-related cortices in response to transitions between blocks of rest and word recognition conditions. Individuals who exhibited larger task-evoked pupil dilation also showed even greater activity in the right primary auditory cortex in response to changes in task structure. CONCLUSION: Pupillometric estimates of word recognition effort predicted variation in activity within cortical regions that were responsive to salient changes in the environment for older adults with hearing loss. The results of the current study suggest that vigilant attention is increased amongst older adults who exert greater listening effort.

The cingulo-opercular network provides word-recognition benefit.

Recognizing speech in difficult listening conditions requires considerable focus of attention that is often demonstrated by elevated activity in putative attention systems, including the cingulo-opercular network. We tested the prediction that elevated cingulo-opercular activity provides word-recognition benefit on a subsequent trial. Eighteen healthy, normal-hearing adults (10 females; aged 20-38 years) performed word recognition (120 trials) in multi-talker babble at +3 and +10 dB signal-to-noise ratios during a sparse sampling functional magnetic resonance imaging (fMRI) experiment. Blood oxygen level-dependent (BOLD) contrast was elevated in the anterior cingulate cortex, anterior insula, and frontal operculum in response to poorer speech intelligibility and response errors. These brain regions exhibited significantly greater correlated activity during word recognition compared with rest, supporting the premise that word-recognition demands increased the coherence of cingulo-opercular network activity. Consistent with an adaptive control network explanation, general linear mixed model analyses demonstrated that increased magnitude and extent of cingulo-opercular network activity was significantly associated with correct word recognition on subsequent trials. These results indicate that elevated cingulo-opercular network activity is not simply a reflection of poor performance or error but also supports word recognition in difficult listening conditions.

Common Brain Structure Findings Across Children with Varied Reading Disability Profiles.

Dyslexia is a developmental disorder in reading that exhibits varied patterns of expression across children. Here we examined the degree to which different kinds of reading disabilities (defined as profiles or patterns of reading problems) contribute to brain morphology results in Jacobian determinant images that represent local brain shape and volume. A matched-pair brain morphometry approach was used to control for confounding from brain size and research site effects in this retrospective multi-site study of 134 children from eight different research sites. Parietal operculum, corona radiata, and internal capsule differences between cases and controls were consistently observed across children with evidence of classic dyslexia, specific comprehension deficit, and language learning disability. Thus, there can be common brain morphology findings across children with quite varied reading disability profiles that we hypothesize compound the developmental difficulties of children with unique reading disability profiles and reasons for their reading disability.

Speech-perception training for older adults with hearing loss impacts word recognition and effort.

The current pupillometry study examined the impact of speech-perception training on word recognition and cognitive effort in older adults with hearing loss. Trainees identified more words at the follow-up than at the baseline session. Training also resulted in an overall larger and faster peaking pupillary response, even when controlling for performance and reaction time. Perceptual and cognitive capacities affected the peak amplitude of the pupil response across participants but did not diminish the impact of training on the other pupil metrics. Thus, we demonstrated that pupillometry can be used to characterize training-related and individual differences in effort during a challenging listening task. Importantly, the results indicate that speech-perception training not only affects overall word recognition, but also a physiological metric of cognitive effort, which has the potential to be a biomarker of hearing loss intervention outcome.

White matter hyperintensities predict low frequency hearing in older adults.

Vascular disease has been proposed as a contributing factor for presbyacusis (age-related hearing loss). While this hypothesis is supported by pathological evidence of vascular decline in post-mortem human and animal studies, evidence in human subjects has been mixed with associations typically reported between a measure of vascular health and low frequency hearing in older women. Given the difficulty of characterizing the in vivo health of the cochlear artery in humans, an estimate of cerebral small vessel disease was used to test the prediction that age-related change in low frequency hearing and not high frequency hearing is related to a global decline in vascular health. We examined the extent to which these associations were specific to women and influenced by a history of high blood pressure in 72 older adults (mean age 67.12 years, SD = 8.79). Probability estimates of periventricular white matter hyperintensities (WMH) from T1- and fluid attenuated T2-weighted magnetic resonance images were significantly associated with a low frequency hearing metric across the sample, which were independent of age, but driven by women and people with a history of high blood pressure. These results support the premise that vascular declines are one mechanism underlying age-related changes in low frequency hearing.

Pupil size varies with word listening and response selection difficulty in older adults with hearing loss.

Listening to speech in noise can be exhausting, especially for older adults with impaired hearing. Pupil dilation is thought to track the difficulty associated with listening to speech at various intelligibility levels for young and middle-aged adults. This study examined changes in the pupil response with acoustic and lexical manipulations of difficulty in older adults with hearing loss. Participants identified words at two signal-to-noise ratios (SNRs) among options that could include a similar-sounding lexical competitor. Growth Curve Analyses revealed that the pupil response was affected by an SNR × Lexical competition interaction, such that it was larger and more delayed and sustained in the harder SNR condition, particularly in the presence of lexical competition. Pupillometry detected these effects for correct trials and across reaction times, suggesting it provides additional evidence of task difficulty than behavioral measures alone.

Auditory cortex signs of age-related hearing loss.

Age-related hearing loss, or presbyacusis, is a major public health problem that causes communication difficulties and is associated with diminished quality of life. Limited satisfaction with hearing aids, particularly in noisy listening conditions, suggests that central nervous system declines occur with presbyacusis and may limit the efficacy of interventions focused solely on improving audibility. This study of 49 older adults (M = 69.58, SD = 8.22 years; 29 female) was designed to examine the extent to which low and/or high frequency hearing loss was related to auditory cortex morphology. Low and high frequency hearing constructs were obtained from a factor analysis of audiograms from these older adults and 1,704 audiograms from an independent sample of older adults. Significant region of interest and voxel-wise gray matter volume associations were observed for the high frequency hearing construct. These effects occurred most robustly in a primary auditory cortex region (Te1.0) where there was also elevated cerebrospinal fluid with high frequency hearing loss, suggesting that auditory cortex atrophies with high frequency hearing loss. These results indicate that Te1.0 is particularly affected by high frequency hearing loss and may be a target for evaluating the efficacy of interventions for hearing loss.