Serial Recall Order of Category Fluency Words: Exploring Its Neural Underpinnings

Abstract

Background: Although performance on the category fluency test (CFT) is influenced by many cognitive functions (i.e., including language, executive functioning and speed of processing), item-level scoring methods of CFT performance might be a promising way to capture aspects of semantic memory that are less influenced by intervenient abilities. One such approach is based on the calculation of correlation coefficients that quantify the association between item-level features and the serial order with which words are recalled (SRO).Methods: We explored the neural underpinnings of 10 of these correlational indices in a sample of 40 healthy adults who completed a classic 1-min CFT and an MRI protocol inclusive of T1-weighted (analysed with voxel-based morphometry) and resting-state fMRI sequences for the evaluation of the default-mode network (DMN). Two sets of linear models were defined to test the association between neural maps and each correlational index: a first set in which major demographic and clinical descriptors were controlled for and a second set in which, additionally, all other 9 correlational indices were regressed out.Results: In the analysis of the DMN, ‘SRO-frequency’, ‘SRO-dominance’ and ‘SRO-body-object interaction’ correlational indices were all negatively associated with the anterior portion of the right temporoparietal junction. The ‘SRO-frequency’ correlational index was also negatively associated with the right dorsal anterior cingulate and the ‘SRO-dominance’ correlational index with the right lateral prefrontal cortex. From the second set of models, the ‘SRO-typicality’ correlational index was positively associated with the left entorhinal cortex. No association was found in relation to grey matter maps.Conclusion: The ability to retrieve more difficult words during CFT performance as measured by the correlational indices between SRO and item-level descriptors is associated with DMN expression in regions deputed to attentional reorienting and processing of salience of infrequent stimuli and dominance status. Of all item-level features, typicality appears to be that most closely linked with entorhinal functioning and may thus play a relevant role in assessing its value in testing procedures for early detection of subtle cognitive difficulties in people with suspected Alzheimer’s degeneration. Although exploratory, these findings warrant further investigations in larger cohorts.

Current Understanding of Verbal Fluency in Alzheimer’s Disease: Evidence to Date

“…Gender differences, for instance, exist in the ability to rely on a switching-based strategy. 49 Anecdotal evidence, moreover, indicates that a small proportion of participants decides to explore large categories such as animals via a letter-by-letter strategy, i.e., by naming words like “aardvark”, “armadillo” or “antelope” at the start of the performance, moving on, then, to entries starting with B, and progressing in alphabetical order at least for the first half of the minute 50 (Supplementary Material).…”

“… 67 In a follow-up study, in addition, this team of authors investigated the neural substrate of this scoring method, reporting significant associations between four of these correlational indices (i.e., those involving typicality, frequency of use, dominance and sensorimotor interaction) and aspects of the default-mode network that are linked to semantic control. 50 The idea that semantic memory and other cognitive functions do not sustain task performance in a regular and constant way during the course of the whole testing minute is reflected by other procedural approaches to CFT scoring. Other than the aforementioned approach based on the characterization of the first 5 retrieved words, 56 , 58 other authors 68 have proposed splitting the global count into four sub-scores, each related to a 15-sec interval.…”

Multivariate word properties in fluency tasks reveal markers of Alzheimer's dementia

“…18 Specific executive deficits (e.g., poor inhibition) may disfavor the retrieval of low-frequency words (whose access increases inhibitory demands to suppress more accessible items). 19 Moreover, frequency correlates with key neural vulnerabilities of AD, 20,21 including the volume of temporo-parietal, fronto-cingulate, and insular regions (measured via magnetic resonance imaging [MRI]) 22,23 and connectivity along the default-mode, salience, and executive networks (captured via fMRI). 23 Also, persons with AD exhibit reduced semantic granularity, choosing conceptually coarse over specific words (flower instead of rose).…”

“…19 Moreover, frequency correlates with key neural vulnerabilities of AD, 20,21 including the volume of temporo-parietal, fronto-cingulate, and insular regions (measured via magnetic resonance imaging [MRI]) 22,23 and connectivity along the default-mode, salience, and executive networks (captured via fMRI). 23 Also, persons with AD exhibit reduced semantic granularity, choosing conceptually coarse over specific words (flower instead of rose). 16 This pattern could reflect memory and/or executive dysfunction (e.g., reduced abstraction capacity) as well as abnormal fMRI connectivity along temporal regions 21 associated with conceptual precision.…”

“… 19 Moreover, frequency correlates with key neural vulnerabilities of AD, 20 , 21 including the volume of temporo‐parietal, fronto‐cingulate, and insular regions (measured via magnetic resonance imaging [MRI]) 22 , 23 and connectivity along the default‐mode, salience, and executive networks (captured via fMRI). 23 …”