Cortical Activity Predicts Which Older Adults Recognize Speech in Noise and When

Abstract

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.

Is Listening in Noise Worth It? The Neurobiology of Speech Recognition in Challenging Listening Conditions

“…This observation has led to the hypothesis that cingulo-opercular activity reflects a compensatory mechanism to support performance when age-related sensory, perceptual, and cognitive declines increase the relative difficulty of a task (Wingfield & Grossman 2006; Reuter-Lorenz & Cappell 2008; Reuter-Lorenz & Park 2010). This view is supported by neuroimaging evidence that older adults with elevated cingulo-opercular activity perform better in challenging speech recognition tasks (Wingfield & Grossman 2006; Harris et al 2009; Peelle et al 2010; Erb & Obleser 2013; Vaden et al 2015; c.f. Meinzer et al 2012).…”

“…It is for this reason that we describe neural systems that are important for attention to stimuli and the intention to understand and perform some action with speech information (e.g., overt report of the words presented, button pressing, working memory tasks). In the context of challenging and changing listening conditions that affect speech recognition, we further consider effort as being dependent on adaptive control or the adjustment of behavior to optimize performance (Vaden et al 2013, 2015). We view fatigue as the consequence of using adaptive control systems over an extended period of time.…”

Hearing Impairment and Cognitive Energy: The Framework for Understanding Effortful Listening (FUEL)

“…Functional Magnetic Resonance Imaging • fMRI uses blood-oxygen-level-dependent contrast imaging to provide an estimate of brain activity based on the hemodynamic response to increased neuronal demand for oxygenated blood during a task. Notably, frontal brain regions in younger and older adults demonstrate an elevated hemodynamic response when listening tasks are challenging (Vaden et al 2013(Vaden et al , 2015. One interpretation of these kinds of blood-oxygen-level-dependent results related to task demands is that the elevated activity, particularly in the cingulate cortex, reflects a decision-making process about the expected value of working to optimize performance given the potential value realized from the task.…”

The Neural Consequences of Age-Related Hearing Loss

“…One strong candidate is the cingulo-opercular network, comprised of bilateral anterior frontal opercula and dorsal anterior cingulate, an attention network involved in top-down task maintenance and cognitive control [67,68]. Cingulo-opercular activity is regularly seen when participants listen to speech that is acoustically degraded (Figure 2B) [69-72]. Critically, cingulo-opercular activity depends on a listener's attention [73] and predicts success on the next trial [74], indicating that its involvement in speech comprehension is more than epiphenomenal.…”

“…(A) A core speech network comprised of bilateral temporal cortex is active during speech perception, supplemented by left ventral inferior frontal gyrus during sentence comprehension. When speech is acoustically challenging, additional regions are recruited: (B) Increased activity listening to single words in background babble includes portions of the cingulo-opercular network, adapted from [69]. (C) Increased activity in the left hemisphere related to perceptual effort when listening to noise-vocoded words, adapted from [77]; (D) Increased activity when listening to degraded sentences, adapted from [64].…”