Neural Processing during Older Adults' Comprehension of Spoken Sentences: Age Differences in Resource Allocation and Connectivity

Abstract

Speech comprehension remains largely preserved in older adults despite significant age-related neurophysiological change. However, older adults' performance declines more rapidly than that of young adults when listening conditions are challenging. We investigated the cortical network underlying speech comprehension in healthy aging using short sentences differing in syntactic complexity, with processing demands further manipulated through speech rate. Neural activity was monitored using blood oxygen level-dependent functional magnetic resonance imaging. Comprehension of syntactically complex sentences activated components of a core sentence-processing network in both young and older adults, including the left inferior and middle frontal gyri, left inferior parietal cortex, and left middle temporal gyrus. However, older adults showed reduced recruitment of inferior frontal regions relative to young adults; the individual degree of recruitment predicted accuracy at the more difficult fast speech rate. Older adults also showed increased activity in frontal regions outside the core sentence-processing network, which may have played a compensatory role. Finally, a functional connectivity analysis demonstrated reduced coherence between activated regions in older adults. We conclude that decreased activation of specialized processing regions, and limited ability to coordinate activity between regions, contribute to older adults' difficulty with sentence comprehension under difficult listening conditions.

Neural changes associated with semantic processing in healthy aging despite intact behavioral performance

“…To our knowledge, very few studies have found or interpreted differences between young and older healthy adults in this region during a semantic task (Berlingeri, et al, 2010;Peelle, et al, 2010). Consistent with our own findings, Ansado et al (2013) found a pattern of hyperactivation in the bilateral temporal pole for older adults during a semantic judgment task on visually-presented words using fMRI.…”

“…Both of these regions have been reported to play a key role in semantic control processes (Jefferies, 2013;Noonan, et al, 2013;Whitney, Kirk, O'Sullivan, Lambon Ralph, & Jefferies, 2012). Other studies have also reported greater recruitment of temporoparietal regions during semantic processing in normal aging (Grossman, et al, 2002;Nielson, et al, 2006;Peelle, et al, 2010). Grossman et al (2002) concluded that greater activation in the right posterolateral temporoparietal regions for older adults during a sentence comprehension task may reflect a compensatory mechanism enabling older adults to maintain sentence comprehension at the same level as younger adults.…”

“…Since picture naming (language production) is inherently different from semantic judgment (language comprehension), such differences in the nature of the tasks may account for the dissimilar patterns of prefrontal activation reported in the current study. Indeed, studies investigating the neural bases of semantic processing in normal aging using receptive tasks have reported mainly a pattern of prefrontal hypoactivation in healthy older adults relative to younger adults (Berlingeri, et al, 2010;Grossman, et al, 2002;Peelle, Troiani, Wingfield, & Grossman, 2010;Tyler, et al, 2010), in contrast with a prefrontal hyperactivation in production tasks. These studies, however, focused mainly on syntactic processing of sentence comprehension, which recruits a number of high-order cognitive processes, including complex syntactic comprehension and working memory, which are also known to decline with age (Burke & Shafto, 2008;Wingfield & Grossman, 2006).…”

A Temporal Bottleneck in the Language Comprehension Network

“…This point is problematic for studies that modeled sentence duration into the stipulated neural profile of activation before convolution with the HRF (Adank and Devlin, 2010); this choice surreptitiously amounts to assuming a linear dependency of brain activity with duration and only allows the experimenters to discover brain areas that deviate from this ideal pattern. Other studies do not describe how they addressed this issue (Peelle et al, 2004(Peelle et al, , 2010 or introduce confounds in their block design by having more sentences per unit of time in blocks with faster compression rates (Poldrack et al, 2001).…”

“…Unlike previous fMRI studies of speech compression that used block designs (Poldrack et al, 2001;Peelle et al, 2004Peelle et al, , 2010Adank and Devlin, 2010), we used a slow event-related design to measure the fMRI response to a single sentence, thus allowing us to determine whether cortical processing speed, indexed by the phase of the fMRI response, accelerates when the stimulus is speeded; which regions show a sudden collapse of activation in parallel to the sudden loss of intelligibility at fast presentation rates; and how these effects differ for spoken and written language.…”