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 ϩ3 and ϩ10 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 cinguloopercular network activity is not simply a reflection of poor performance or error but also supports word recognition in difficult listening conditions.
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-by-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.
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 (M069.58, SD08.22 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.
This review examines findings from functional neuroimaging studies of speech recognition in noise to provide a neural systems level explanation for the effort and fatigue that can be experienced during speech recognition in challenging listening conditions. Neuroimaging studies of speech recognition consistently demonstrate that challenging listening conditions engage neural systems that are used to monitor and optimize performance across a wide range of tasks. These systems appear to improve speech recognition in younger and older adults, but sustained engagement of these systems also appears to produce an experience of effort and fatigue that may affect the value of communication. When considered in the broader context of the neuroimaging and decision making literature, the speech recognition findings from functional imaging studies indicate that the expected value, or expected level of speech recognition given the difficulty of listening conditions, should be considered when measuring effort and fatigue. We propose that the behavioral economics and/or neuroeconomics of listening can provide a conceptual and experimental framework for understanding effort and fatigue that may have clinical significance.
Speech recognition in noise can be challenging for older adults and elicits elevated activity throughout a cingulo-opercular network that is hypothesized to monitor and modify behaviors to optimize performance. A word recognition in noise experiment was used to test the hypothesis that cingulo-opercular engagement provides performance benefit for older adults. Healthy older adults (N ϭ 31; 50 -81 years of age; mean pure tone thresholds Ͻ32 dB HL from 0.25 to 8 kHz, best ear; species: human) performed word recognition in multitalker babble at 2 signal-to-noise ratios (SNR ϭ ϩ3 or ϩ10 dB) during a sparse sampling fMRI experiment. Elevated cingulo-opercular activity was associated with an increased likelihood of correct recognition on the following trial independently of SNR and performance on the preceding trial. The cingulo-opercular effect increased for participants with the best overall performance. These effects were lower for older adults compared with a younger, normal-hearing adult sample (N ϭ 18). Visual cortex activity also predicted trial-level recognition for the older adults, which resulted from discrete decreases in activity before errors and occurred for the oldest adults with the poorest recognition. Participants demonstrating larger visual cortex effects also had reduced fractional anisotropy in an anterior portion of the left inferior frontal-occipital fasciculus, which projects between frontal and occipital regions where activity predicted word recognition. Together, the results indicate that older adults experience performance benefit from elevated cingulo-opercular activity, but not to the same extent as younger adults, and that declines in attentional control can limit word recognition.
Meta-analysis of voxel-based morphometry dyslexia studies and direct analysis of 293 reading disability and control cases from six different research sites were performed to characterize defining gray matter features of reading disability. These analyses demonstrated consistently lower gray matter volume in left posterior superior temporal sulcus/middle temporal gyrus regions and left orbitofrontal gyrus/pars orbitalis regions. Gray matter volume within both of these regions significantly predicted individual variation in reading comprehension after correcting for multiple comparisons. These regional gray matter differences were observed across published studies and in the multisite dataset after controlling for potential age and gender effects, and despite increased anatomical variance in the reading disability group, but were not significant after controlling for total gray matter volume. Thus, the orbitofrontal and posterior superior temporal sulcus gray matter findings are relatively reliable effects that appear to be dependent on cases with low total gray matter volume. The results are considered in the context of genetics studies linking orbitofrontal and superior temporal sulcus regions to alleles that confer risk for reading disability.
Evidence has accumulated that posterior superior temporal sulcus (STS) is critically involved in phonological processing during speech perception, although there are conflicting accounts regarding the degree of lateralization. The current fMRI experiment aimed to identify phonological processing during speech perception through repetition-suppression effects. Repetition-suppression occurs when brain activity decreases from repetitive presentation of stimulus characteristics, in regions of cortex that process those characteristics. We manipulated the degree of phonological repetition among words in short lists to obtain systematic decreases in brain response, indicative of phonological processing. The fMRI experiment presented seventeen participants with recorded wordlists, of low, medium, or high phonological repetition, defined by how many phonemes were shared among words. Bilaterally, middle STS demonstrated activity differences consistent with our prediction of repetition-suppression, as responses decreased systematically with each increase in phonological repetition. Phonological repetition-suppression in bilateral STS converges with neuroimaging evidence for phonological processing, and word deafness resulting from bilateral superior temporal lesions.
The human superior temporal sulcus (STS) is responsive to visual and auditory information, including sounds and facial cues during speech recognition. We investigated the functional organization of STS with respect to modality-specific and multimodal speech representations. Twenty younger adult participants were instructed to perform an oddball detection task and were presented with auditory, visual, and audiovisual speech stimuli, as well as auditory and visual nonspeech control stimuli in a block fMRI design. Consistent with a hypothesized anterior-posterior processing gradient in STS, auditory, visual and audiovisual stimuli produced the largest BOLD effects in anterior, posterior and middle STS (mSTS), respectively, based on whole-brain, linear mixed effects and principal component analyses. Notably, the mSTS exhibited preferential responses to multisensory stimulation, as well as speech compared to nonspeech. Within the mid-posterior and mSTS regions, response preferences changed gradually from visual, to multisensory, to auditory moving posterior to anterior. Post hoc analysis of visual regions in the posterior STS revealed that a single subregion bordering the mSTS was insensitive to differences in low-level motion kinematics yet distinguished between visual speech and nonspeech based on multi-voxel activation patterns. These results suggest that auditory and visual speech representations are elaborated gradually within anterior and posterior processing streams, respectively, and may be integrated within the mSTS, which is sensitive to more abstract speech information within and across presentation modalities. The spatial organization of STS is consistent with processing streams that are hypothesized to synthesize perceptual speech representations from sensory signals that provide convergent information from visual and auditory modalities.
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