Altered phase and nonphase EEG activity expose impaired maintenance of a spatial-object attentional focus in multiple sclerosis patients

Abstract

Some of the anatomical and functional basis of cognitive impairment in multiple sclerosis (MS) currently remains unknown. In particular, there is scarce knowledge about modulations in induced EEG (nonphase activity) for diverse frequency bands related to attentional deficits in this pathology. The present study analyzes phase and nonphase alpha and gamma modulations in 26 remitting-relapsing multiple sclerosis patients during their participation in the attention network test compared with twenty-six healthy controls (HCs) matched in sociodemographic variables. Behavioral results showed that the MS group exhibited general slowing, suggesting impairment in alerting and orienting networks, as has been previously described in other studies. Time–frequency analysis of EEG revealed that the gamma band was related to the spatial translation of the attentional focus, and the alpha band seemed to be related to the expectancy mechanisms and cognitive processing of the target. Moreover, phase and nonphase modulations differed in their psychophysiological roles and were affected differently in the MS and HC groups. In summary, nonphase modulations can unveil hidden cognitive mechanisms for phase analysis and complete our knowledge of the neural basis of cognitive impairment in multiple sclerosis pathology.

Deficits in Early Sensory and Cognitive Processing Are Related to Phase and Nonphase EEG Activity in Multiple Sclerosis Patients

“…In this sense, the increase (synchronization) in alpha activity in regions irrelevant to the task has been associated with inhibition processes [ 17 ]. Additionally, some studies have proposed that the synchronization of alpha in latencies of ERPs (P1 and N1) [ 18 , 19 ] represents the early sensorial processing of stimulus [ 20 ]. In contrast, the decrease (desynchronization) in the alpha band has also been related to psychophysiological roles [ 21 ].…”

“…These contradictory results may be based on different cognitive demands, tasks and analyzed ranges. The gamma band has been fundamentally associated with visual binding [ 28 , 29 , 30 ], spatial attention [ 31 ], processing target stimuli [ 32 ] or translation of attentional focus [ 20 , 33 ]. One of the reasons that makes this band suitable for attentional mechanisms is its fine temporal tuning for neuronal firing (10–30 ms time precision) [ 34 ].…”

“…These studies have suggested that a smaller decrease in the alpha band for MS patients compared to healthy controls is associated with a poorer behavioural performance [ 13 , 35 , 36 ]. However, a larger decrease (desynchronization) in alpha activity in patients with MS has been described in certain conditions that demands more cognitive resources [ 20 ]. These authors have suggested that in some conditions, MS patients need a larger decrease in the alpha band to improve cognitive processing (compensatory mechanism).…”

“…It has been proposed that alterations in the gamma band may be related to deficits in cognitive processing [ 37 ]. More specifically, an increase (synchronization) in the gamma band in patients with MS compared to healthy controls has been associated with plasticity or compensatory attentional mechanisms [ 20 , 38 ].…”

“…The TSE allows EEG time-frequency information that includes both evoked (phase) and induced (nonphase) modulations for a spectral band related to a stimulus presentation to be obtained (for a detailed description of the TSE method, see [ 40 , 41 , 42 ]). Both evoked and induced activities have been demonstrated to represent different cognitive processes [ 20 ].…”