Functional MRI evidence for the decline of word retrieval and generation during normal aging

Abstract

This fMRI study aimed to explore the effect of normal aging on word retrieval and generation. The question addressed is whether lexical production decline is determined by a direct mechanism, which concerns the language operations or is rather indirectly induced by a decline of executive functions. Indeed, the main hypothesis was that normal aging does not induce loss of lexical knowledge, but there is only a general slowdown in retrieval mechanisms involved in lexical processing, due to possible decline of the executive functions. We used three tasks (verbal fluency, object naming, and semantic categorization). Two groups of participants were tested (Young, Y and Aged, A), without cognitive and psychiatric impairment and showing similar levels of vocabulary. Neuropsychological testing revealed that older participants had lower executive function scores, longer processing speeds, and tended to have lower verbal fluency scores. Additionally, older participants showed higher scores for verbal automatisms and overlearned information. In terms of behavioral data, older participants performed as accurate as younger adults, but they were significantly slower for the semantic categorization and were less fluent for verbal fluency task. Functional MRI analyses suggested that older adults did not simply activate fewer brain regions involved in word production, but they actually showed an atypical pattern of activation. Significant correlations between the BOLD (Blood Oxygen Level Dependent) signal of aging-related (A > Y) regions and cognitive scores suggested that this atypical pattern of the activation may reveal several compensatory mechanisms (a) to overcome the slowdown in retrieval, due to the decline of executive functions and processing speed and (b) to inhibit verbal automatic processes. The BOLD signal measured in some other aging-dependent regions did not correlate with the behavioral and neuropsychological scores, and the overactivation of these uncorrelated regions would simply reveal dedifferentiation that occurs with aging. Altogether, our results suggest that normal aging is associated with a more difficult access to lexico-semantic operations and representations by a slowdown in executive functions, without any conceptual loss.

Keywords: Executive; Fluency; Lexical; Normal aging; Semantic; fMRI.

Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1

a Activated regions during the Verbal Fluency (VF) task (N = 30) projected onto 3D anatomical templates and 2D axial slices. b Cerebral regions, which are more activated in AG than in YG during VF. The color scale indicates the T value of the activation. AG, aged group; YG young group

Fig. 2

a shows activated regions during the Object Naming (ON) task (N = 30), projected onto 3D anatomical templates and 2D axial slices. b Cerebral regions, which are more activated in AG than in YG during ON. c Cerebral regions, which are more activated in YG than in AG during ON. The color scale indicates the T value of the activation. AG, aged group; YG, young group

Fig. 3

a Activated regions during the Semantic Categorization with the Pyramid Palm and Tree Test (PPTT) (N = 30) projected onto 3D anatomical templates and 2D axial slices. b Cerebral regions, which are more activated in AG than in YG during PPTT. The color scale indicates the T value of the activation. AG, aged group; YG, young group

Fig. 4

Significant correlation (positive or negative) between the BOLD signal measured in the aging-dependent regions with the neuropsychological scores for Verbal Fluency (VF, a) and Pyramid Palm Tree Test (PPTT, c) and with Age for Object Naming (ON, b). Activated regions were projected onto 2D axial slices and were shown next to the corresponding graphics. L, left hemisphere; R, right hemisphere