Executive functioning affects verbal learning process in multiple sclerosis patients: Behavioural and imaging results

Pitteri, Marco; Dapor, Caterina; Pisani, Anna Isabella; Castellaro, Marco; DeLuca, John; Chiaravalloti, Nancy D.; Guandalini, Maddalena; Ziccardi, Stefano; Calabrese, Massimiliano

doi:10.1111/jnp.12198

Cited by 6 publications

(6 citation statements)

References 69 publications

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“…The lack of other differences between CI and ACN may be due to the low number of patients included in the study. Nevertheless, our results are in line with previous studies showing that the damage of the superior frontal cortex seems to play a crucial role in CI in pwMS [ 50 ] and being linked to verbal learning and delayed memory recall abilities [ 51 ]. The insula, especially the anterior part, has a central role in integrating different functional systems involved in affective and cognitive processing [ 52 , 53 ].…”

Section: Discussionsupporting

confidence: 93%

Microstructural MRI Correlates of Cognitive Impairment in Multiple Sclerosis: The Role of Deep Gray Matter

et al. 2021

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Although cognitive impairment (CI) is frequently observed in people with multiple sclerosis (pwMS), its pathogenesis is still controversial. Conflicting results emerged concerning the role of microstructural gray matter (GM) damage especially when involving the deep GM structures. In this study, we aimed at evaluating whether differences in cortical and deep GM structures between apparently cognitively normal (ACN) and CI pwMS (36 subjects in total) are present, using an extensive set of diffusion MRI (dMRI) indices and conventional morphometry measures. The results revealed increased anisotropy and restriction over several deep GM structures in CI compared with ACN pwMS, while no changes in volume were present in the same areas. Conversely, reduced anisotropy/restriction values were detected in cortical regions, mostly the pericalcarine cortex and precuneus, combined with reduced thickness of the superior frontal gyrus and insula. Most of the dMRI metrics but none of the morphometric indices correlated with the Symbol Digit Modality Test. These results suggest that deep GM microstructural damage can be a strong anatomical substrate of CI in pwMS and might allow identifying pwMS at higher risk of developing CI.

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Section: Discussionsupporting

confidence: 93%

Microstructural MRI Correlates of Cognitive Impairment in Multiple Sclerosis: The Role of Deep Gray Matter

et al. 2021

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“…A second phenotype, mild-verbal memory/semantic fluency, was characterized by mildly decreased performance in SRT and WLG. The data-driven cosegregation of decreased performance in verbal learning and memory and in semantic fluency 40 was likely associated with impaired common semantic clustering strategies 41,42 and lexical access modalities. 43 In line with this explanation, the MRI data in this study showed hippocampal atrophy as a potential pathological substrate.…”

Section: Discussionmentioning

confidence: 99%

Identifying the Distinct Cognitive Phenotypes in Multiple Sclerosis

et al. 2021

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IMPORTANCECognitive impairment is a common and disabling feature of multiple sclerosis (MS), but a precise characterization of cognitive phenotypes in patients with MS is lacking.OBJECTIVES To identify cognitive phenotypes in a clinical cohort of patients with MS and to characterize their clinical and magnetic resonance imaging (MRI) features. DESIGN, SETTING, AND PARTICIPANTSThis multicenter cross-sectional study consecutively screened clinically stable patients with MS and healthy control individuals at 8 MS centers in Italy from January 1, 2010, to October 31, 2019. Patients with MS and healthy control individuals who were not using psychoactive drugs and had no history of other neurological or medical disorders, learning disability, severe head trauma, and alcohol or drug abuse were enrolled. MAIN OUTCOMES AND MEASURES Participants underwent a neurological examination and a cognitive evaluation with the Rao Brief Repeatable Battery and Stroop Color and Word Test. A subgroup of participants also underwent a brain MRI examination. Latent profile analysis was used on cognitive test z scores to identify cognitive phenotypes. Linear regression and mixed-effects models were used to define clinical and MRI features of each phenotype. RESULTS A total of 1212 patients with MS (mean [SD] age, 41.1 [11.1] years; 784 women [64.7%]) and 196 healthy control individuals (mean [SD] age, 40.4 [8.6] years; 130 women [66.3%]) were analyzed in this study. Five cognitive phenotypes were identified: preserved cognition (n = 235 patients [19.4%]), mild-verbal memory/semantic fluency (n = 362 patients [29.9%]), mild-multidomain (n = 236 patients [19.5%]), severe-executive/attention (n = 167 patients [13.8%]), and severe-multidomain (n = 212 patients [17.5%]) involvement. Patients with preserved cognition and mild-verbal memory/semantic fluency were younger (mean [SD] age, 36.5 [9.8] years and 38.2 [11.1] years) and had shorter disease duration (mean [SD] 8.0 [7.3] years and 8.3 [7.6] years) compared with patients with mild-multidomain (mean [SD] age, 42.6 [11.2] years; mean [SD] disease duration, 12.8 [9.6] years; P < .001), severe-executive/attention (mean [SD] age, 42.9 [11.7] years; mean [SD] disease duration, 12.2 [9.5] years; P < .001), and severe-multidomain (mean [SD] age, 44.0 [11.0] years; mean [SD] disease duration , 13.3 [10.2] years; P < .001) phenotypes. Severe cognitive phenotypes prevailed in patients with progressive MS. At MRI evaluation, compared with those with preserved cognition, patients with mild-verbal memory/semantic fluency exhibited decreased mean (SE) hippocampal volume (5.42 [0.68] mL vs 5.13 [0.68] mL; P = .04), patients with the mild-multidomain phenotype had decreased mean (SE) cortical gray matter volume (687.69 [35.40] mL vs 662.59 [35.48] mL; P = .02), patients with severe-executive/ attention had higher mean (SE) T2-hyperintense lesion volume (51.33 [31.15] mL vs 99.69 [34.07] mL; P = .04), and patients with the severe-multidomain phenotype had extensive brain damage, with decreased volume in a...

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“…Previous studies reported that general intelligence is preserved in MS, and PM in everyday life is one of the most affected cognitive domains in MS (5)(6)(7). Although MS is traditionally considered to be a demyelinating disease affecting the white matter (WM), gray matter (GM) atrophy and plaques in GM have been deemed crucial in cognitive disability of MS (8)(9)(10).…”

Section: Introductionmentioning

confidence: 99%

Prospective Memory Deficits in Multiple Sclerosis: Voxel-based Morphometry and Double Inversion Recovery Analysis

et al. 2021

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Objective Prospective memory (PM) is an important social cognitive function in everyday life. PM is one of the most affected cognitive domains in multiple sclerosis (MS) patients. Gray matter (GM) atrophy and plaques have been attracting attention for various cognitive impairments in MS patients. This study aimed to clarify the atrophic GM regions associated with PM deficits and investigate the relationship between the atrophic GM regions and GM plaques. Methods Twenty-one MS patients and 10 healthy controls (HCs) underwent neuropsychological tests and MRI. PM was assessed using subtests of the Rivermead Behavioural Memory Test. A lesion symptom analysis was performed using voxel-based morphometry (VBM). We then evaluated GM plaques in the corresponding areas using double inversion recovery (DIR). Results MS patients showed lower PM scores than HCs (p=0.0064). The GM volume of MS patients tended to be lower than those of HCs. VBM analyses revealed correlations of the PM score with the orbital part of the left inferior frontal gyrus, the left hippocampus, and the right parahippocampus. There was no GM plaque in the orbital part of the left inferior frontal gyrus and the right parahippocampus. Only one patient (4.8%) had GM plaque in the left hippocampus. Conclusion The left inferior frontal gyrus, the left hippocampus, and the right parahippocampus were associated with PM in MS, whereas these atrophic GM regions were not associated with GM plaque. Regardless of the location of plaques on DIR, both PM deficit and GM atrophy should be detected using neuropsychological tests and VBM in MS patients.

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Executive functioning affects verbal learning process in multiple sclerosis patients: Behavioural and imaging results

Cited by 6 publications

References 69 publications

Microstructural MRI Correlates of Cognitive Impairment in Multiple Sclerosis: The Role of Deep Gray Matter

Microstructural MRI Correlates of Cognitive Impairment in Multiple Sclerosis: The Role of Deep Gray Matter

Identifying the Distinct Cognitive Phenotypes in Multiple Sclerosis

Prospective Memory Deficits in Multiple Sclerosis: Voxel-based Morphometry and Double Inversion Recovery Analysis

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