Abstract

Semantic verbal fluency (VF), assessed by animal category, is a task widely used for early detection of dementia. A feature not regularly assessed is the occurrence of errors such as perseverations and intrusions. So far, no investigation has analyzed the how and when of error occurrence during semantic VF in aging populations, together with their possible neural correlates. The present study aims to address the issue using a combined methodology based on latent Dirichlet allocation (LDA) analysis for word classification together with a time-course analysis identifying exact time of errors’ occurrence. LDA is a modeling technique that discloses hidden semantic structures based on a given corpus of documents. We evaluated a sample of 66 participants divided into a healthy young group (n = 24), healthy older adult group (n = 23), and group of patients with mild Alzheimer’s disease (AD) (n = 19). We performed DTI analyses to evaluate the white matter integrity of three frontal tracts purportedly underlying error commission: anterior thalamic radiation, frontal aslant tract, and uncinate fasciculus. Contrasts of DTI metrics were performed on the older groups who were further classified into high-error rate and low-error rate subgroups. Results demonstrated a unique deployment of error commission in the patient group characterized by high incidence of intrusions in the first 15 s and higher rate of perseverations toward the end of the trial. Healthy groups predominantly showed very low incidence of perseverations. The DTI analyses revealed that the patients with AD committing high-error rate presented significantly more degenerated frontal tracts in the left hemisphere. Thus, our findings demonstrated that the appearance of intrusions, together with left hemisphere degeneration of frontal tracts, is a pathognomic trait of mild AD. Furthermore, our data suggest that the error commission of patients with AD arises from executive and working memory impairments related partly to deteriorated left frontal tracts.

Highlights

  • Besides memory complaints, one of the most characteristic dysfunctions in Alzheimer’s disease (AD) is verbal deterioration

  • The goal of the present study is two-fold: (a) perform a fine behavioral evaluation of the occurrence of perseverations and intrusions in semantic verbal fluency (VF) in the category most frequently employed for the assessment of dementia (Moreno-Martinez et al, 2017), namely “animals” (Ardila et al, 2006); and (b) assess frontal tracts purportedly associated to error behavior

  • Because mean diffusivity (MD) is an average of the three eigenvectors calculated in diffusion tensor imaging (DTI), increased MD values in our study cannot be translated into precise neurobiological changes; rather, these results indicate clear pathognomic signs of the selected frontal tracts, especially among patients committing the largest number of semantic VF errors

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Summary

Introduction

One of the most characteristic dysfunctions in Alzheimer’s disease (AD) is verbal deterioration. AD impairs verbal fluency (VF), which is the ability to generate words as fast as possible according to either a letter of the alphabet or a semantic category within a time limit, usually one minute. VF abilities are evaluated with tasks, such as the Controlled Oral Word Association Test (COWAT, Benton, 1967) for the assessment of phonemic fluency, or by categories, such as animals or supermarket items (see e.g., the Dementia Rating Scale, Mattis, 1976), for the assessment of semantic fluency. Impairments in semantic fluency comprise reduction in the number of correct responses and increment in errors, which are prominent in AD (Gomez and White, 2006) even in the early stages (Fagundo et al, 2008)

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