Bilateral brain regions associated with naming in older adults
Introduction
While classical aphasiological research identified peri-Sylvian cortical regions in the left-hemisphere as crucial to language, brain-imaging techniques have permitted appreciation of brain regions activated for language processes outside those areas in the left-hemisphere – especially in more anterior areas – as well as in the right hemisphere. Not only are posterior as well as anterior regions within peri-Sylvian cortex involved in lexical-retrieval, (e.g., Graves et al., 2007, Okada and Hickok, 2006); naming tasks can also be shown to involve left-hemisphere anterior cingulate gyrus and mid-frontal gyrus (Brodmann areas 46 and 9) in addition to Broca’s area (Brodmann areas 44 and 45; Abrahams, Goldstein, & Simmons, 2003). Moreover, when Fridriksson, Morrow, and Moser (2006) studied the intensity of activation in cortical areas in adults ranging in age from 20 to 82 performing a picture-naming task, they found activation in the right-hemisphere counterpart to Broca’s area in addition to the expected activation in the traditional Broca’s and Wernicke’s areas of the left-hemisphere.
What is unclear in studies of elderly individuals like that of Fridriksson et al. is the extent to which these additional regions implicated in naming are compensating for the atrophy that increases with advancing age. Structural imaging has shown age-related degradation of gray and white matter which particularly affects frontal and temporal regions (e.g., Raz, 2000, Raz et al., 1998, Resnick et al., 2003, Sullivan and Pfefferbaum, 2006). However, it appears that language performance does not decline proportionally to this atrophy (Park et al., 2002). We must assume, then, that other brain regions are involved in compensating for it, and it is plausible that the left pre-frontal regions and bilateral language-area regions are called on to compensate (e.g., Cabeza, 2002, Reuter-Lorenz, 2002).
To address this issue, Wierenga et al. (2008) studied overt naming of animals, tools, and vehicles in 20 younger (mean age 25.1) and 20 older (mean age 74.9) adults via event-related functional magnetic-resonance imaging (fMRI). Both groups performed at relatively high accuracy on this naming task. However the older adults recruited substantially more brain regions to perform the task. Most crucially, they showed the same regions for left-hemisphere activation that the younger adults showed. Their activation was greater in both medial and lateral frontal cortex bilaterally. As these older adults performed bimodally on the naming task, the authors then divided the group into ‘high’ (scoring above 90) and ‘low’ (scoring below 87) older namers, and noted, further, that the better namers showed greater activation of the pars orbitalis region of the right inferior frontal gyrus.
Bilateral involvement has been evidenced for other naming tasks as well: Ellis, Burani, Izura, Bromiley, and Venneri (2006) report bilateral frontal, parietal and mediotemporal activation during silent object naming (in young and middle-aged adults, aged 23–52), along with activation in left lingual and fusiform gyri. In their fMRI study of performance on a verb-generation task, Persson et al. (2004) reported that right inferior frontal gyrus was over-activated in older adults (aged 60–80), relative to younger ones (ages 18–30). In addition, Persson and colleagues observed underactivation of left frontal and inferior temporal gyri as well as anterior cingulate in their older participants, particularly for the task that required more challenges for selecting among possible responses, specifically among those older participants who performed more slowly on the task. They conclude that older adults recruit right-hemisphere areas and left-hemisphere areas beyond the traditional peri-Sylvian region to compensate for their increasing difficulties performing the task.
However, not all studies of language in older adults report right-hemisphere compensation; as Kan and Thompson-Schill (2004) point out, brain-region sites reported to activate in response to naming tasks are inconsistent across the studies. Such inconsistencies may arise from task differences of various types. Some authors deliberately choose high-frequency items for their naming task to assure participants name successfully; others deliberately choose lower frequency items in addition, or instead. Two naming tasks are frequently employed in imaging tests (though only one in a given study, as a rule): confrontation naming or list-generation. A third test, more similar to confrontation naming in that participants must come up with a single correct word, is that of responsive naming, in which a definition is read to participants who must then name the correct word. Tomaszewski Farias, Harrington, Broomand, and Seyal (2005) report that those of their participants (aged 28 to around 50) who were tested on a confrontation naming task displayed activation only in left-hemisphere middle temporal gyrus, whereas activation for responsive naming was seen in superior and inferior temporal gyri as well. Moreover, the responsive naming task evoked anterior temporal activation in more participants (90%) than did confrontation naming (60%).
Such task-related differences in activation may be explained by a model that Wingfield and Grossman (2006) propose, albeit for the variability of findings for brain activation during sentence-comprehension tasks in aging. They posit ‘core’ regions involved in a language task and ‘support’ or ‘resource’ regions – such as those subserving working memory in the case of sentence comprehension – that interact with them. The core network (they use the terms ‘region’ and ‘network’ interchangeably) is the one which brain-damage has revealed to be necessary for the task. The support regions, by contrast, are those additional regions that neuroimaging studies reveal in healthy adults that are outside the traditional language areas: various regions of frontal lobe and cingulate gyrus bilaterally, inferior temporal lobe on the left, etc. (e.g., Caplan et al., 2000, Friederici, 2002, Luke et al., 2002).
In a series of studies from the labs of Grossman and Wingfield, there is evidence of greater reliance on these support networks for tasks that involve sentence processing, including language-comprehension, with advancing age (e.g., Cooke et al., 2002, Cooke et al., 2006, Peelle et al., 2004). This is of interest, they remind us, because, except in stressed situations such as listening to speeded speech or syntactically complex materials, older adults’ sentence comprehension may be spared (Goral et al., submitted for publication, Nicholas et al., 1985, Wingfield et al., 2006, Wingfield et al., 2003). Situations in which listening conditions are stressful are, nevertheless, relatively common in daily life (e.g., listening to synthetic-speech choices when calling ‘service’ numbers, conversing in noise); a number of studies focus on age-related decline in comprehension in non-ideal conditions, even at the sentence level, rather than in the simpler conditions in which older adults’ comprehension remains at ceiling level. It is, then, all the more interesting to note the conclusions of Wingfield and Grossman, that even when older adults are performing well on comprehension tasks, they are employing more language areas than younger adults in doing so: right-hemisphere counterparts to posterior lateral temporal cortex and dorsal portion of the left inferior frontal cortex areas and left-hemisphere of dorsolateral pre-frontal cortex.
In this study we ask a similar question concerning naming tasks: How precisely is better naming in older adults associated with broader (or different) areas than poorer naming? Naming problems, of course, are even more commonly complained of with advancing age – and at earlier ages – than are comprehension problems. A substantial body of research has documented such naming problems via behavioral tasks, both confrontation naming ones (e.g., Au et al., 1995, Barresi et al., 2000, Burke et al., 1991, Connor et al., 2004, Goral et al., 2007, Kaplan et al., 1983, Nicholas et al., 1985, see Feyereisen, 1997, for a meta-analysis) and list-generation ones (Boone et al., 1990, Parkin and Walter, 1991, Pekkala et al., 2009, Troyer et al., 1997, Whelihan and Lesher, 1985). Most curious to us, in the series of studies from our Language in the Aging Brain Laboratory, is how some older participants, in their 70s and above, perform as well as some 30-year olds, even while peak performance on confrontation naming, for example, occurs in the late 30s, with accelerating decline into oldest adulthood. That there is increasing variability in performance on naming tasks with advancing age is not, in and of itself, surprising; a substantial literature documents increasing range of performance across all cognitive tasks. Rather, what remains of interest is determining what accounts for the age-related variability, since age per se is not a satisfactory explanation. In other studies we demonstrate the contributions of demographic factors such as education and gender to age-related naming performance (e.g., Goral et al., 2007) and of health-related factors such as hypertension (Albert et al., 2009; Spiro et al., 2008).
Asking about language and non-language regions recruited for naming is not sufficient, however. While there is substantial research on such “processing centers”, only recently have questions been asked concerning the connectivity among them that in fact drives language performance. For example, there are reports that additional bilateral and pre-frontal recruitment predicts better performance in older adults on executive function tasks, but such evidence is inconsistent (see Langenecker and Nielson, 2003, Nielson et al., 2002). The fact that such compensatory mechanisms are not always effective may be explained by impaired communication between frontal regions and “core” peri-Sylvian language regions. In fact, Stamatakis and Tyler (2006) infer reduced fronto-temporal connectivity in functional networks among their elderly participants performing a morphological processing task.
In the current study, then, we asked what cortical regions and associated connective tracts were associated with better or worse naming in older adults. We employed structural magnetic-resonance imaging (MRI) and diffusion tensor imaging (DTI) in order to address which pertinent brain areas and which connective tracts are available for processing to better older namers. Specifically, voxel-based morphometry provides local measures of white matter volume/density, whereas DTI-based fractional anisotropy (FA) is thought to reflect the amount of organization within the white matter. White-matter density reduction is related to macroscopic changes in white matter, such as lesions and atrophy (Ge et al., 2002, Meier-Ruge et al., 1992). FA reduction has been linked to axonal demyelination and loss (Bartzokis, 2004). Although considered more sensitive than structural MRI-derived measures (Hugenschmidt et al., 2008), FA alone is not a reliable indicator of white matter integrity: brain regions shared by major fiber tracts traveling in orthogonal directions will show dramatically reduced FA.
We employed tests of both nouns (Boston Naming Test – BNT, Kaplan et al., 1983) and verbs (Action Naming Test – ANT, Obler & Albert, 1986) because, while performance on these two tests is seen to decline in remarkably parallel fashion with advancing age (e.g., Goral et al., 2007), a substantial body of literature (e.g., Cappelletti et al., 2008, Shapiro et al., 2006) suggests differential engagement of frontal and temporal regions in processing them.
Section snippets
Participants
Our 24 participants were adults aged 56–79 who participated in our Language in the Aging Brain project. They volunteered for two days of language, cognitive, and health testing. These test sessions were conducted within six weeks of each other. From these sessions, the two tests discussed in this paper were administered on separate days: the BNT task during Visit 1 and the ANT task during Visit 2. Participants in the present study were then qualified to undergo an hour of MRI scanning on a
Behavioral data: naming performance and age
Accuracy and response time for the BNT and ANT tasks are presented in Table 2, also scatter plots of accuracy and response-time versus age for each of the two tasks are presented in Fig. 1, Fig. 2. Note that, unlike in our prior studies that include younger adults, for this small group of older adults, a correlation between age and task performance is not evident. (For BNT accuracy, BNT RT, ANT accuracy, and ANT RT we obtained correlation values (N = 24) of −0.01 (p = 0.47), 0.13 (p = 0.27), 0.03 (p =
Discussion
Complementary findings were evident from structural MRI and DTI measures. Both sets of measures suggest that performance on ANT and BNT naming tasks relates somewhat differently to brain volume and connectivity in older adults. Both suggest right-hemisphere regions are available to support good naming. Furthermore, it appears that better older-adult namers, consistent with what Wierenga et al. (2008) and with what Wingfield and Grossman (2006) report for successful comprehenders, may employ
Acknowledgments
This project was supported in part by the Clinical Science Research and Development Service, US Department of Veterans Affairs, by Grant AG14345 (PI: Martin L. Albert) from the National Institute on Aging, and by a Merit Review to Avron Spiro by the Clinical Science Research and Development Service, US Department of Veterans Affairs. We thank all our participants and are particularly appreciative of the helpful suggestions made by two anonymous reviewers.
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