Implicit learning impairment identified via predictive saccades in Huntington's disease correlates with extended cortico-striatal atrophy

Vaca‐Palomares, Israel; Brien, Donald C.; Coe, Brian C.; Ochoa, Adriana; Martínez-Ruano, Leticia; Munoz, Douglas P.; Fernández-Ruíz, Juan

doi:10.1016/j.cortex.2019.06.013

Cited by 6 publications

(7 citation statements)

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“…Neuronal firing in these areas correlates with the ISI of a periodic target, and pharmacological silencing impairs predictive movements (Buhusi and Meck, 2005;Merchant et al, 2013;Matsuyama and Tanaka, 2021;Tanaka et al, 2021). Additionally, an impaired ability to anticipate rhythmic stimuli to respond predictively is evident in multiple brain-related disorders, including developmental coordination disorder (Debrabant et al, 2013), developmental dyslexia (Lukasova et al, 2016), Huntington's disease (Vaca-Palomares et al, 2019), and spinocerebellar atrophy (Bares et al, 2007). Despite the important role temporal prediction plays in essential sensorimotor learning, and its clinical relevance to various neurologic conditions, its developmental timeline in normal controls remains unknown.…”

Section: Introductionmentioning

confidence: 99%

Maturation of Temporal Saccade Prediction from Childhood to Adulthood: Predictive Saccades, Reduced Pupil Size, and Blink Synchronization

et al. 2021

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When presented with a periodic stimulus, humans spontaneously adjust their movements from reacting to predicting the timing of its arrival, but little is known about how this sensorimotor adaptation changes across development. To investigate this, we analyzed saccade behavior in 114 healthy humans (ages 6-24 years) performing the visual metronome task, who were instructed to move their eyes in time with a visual target that alternated between two known locations at a fixed rate, and we compared their behavior to performance in a random task, where target onsets were randomized across five interstimulus intervals (ISIs) and thus the timing of appearance was unknown. Saccades initiated before registration of the visual target, thus in anticipation of its appearance, were labeled predictive [saccade reaction time (SRT) , 90 ms] and saccades that were made in reaction to its appearance were labeled reactive (SRT . 90 ms). Eye-tracking behavior including saccadic metrics (e.g., peak velocity, amplitude), pupil size following saccade to target, and blink behavior all varied as a function of predicting or reacting to periodic targets. Compared with reactive saccades, predictive saccades had a lower peak velocity, a hypometric amplitude, smaller pupil size, and a reduced probability of blink occurrence before target appearance. The percentage of predictive and reactive saccades changed inversely from ages 8-16, at which they reached adult-levels of behavior. Differences in predictive saccades for fast and slow target rates are interpreted by differential maturation of cerebellar-thalamic-striatal pathways.

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Section: Introductionmentioning

confidence: 99%

Maturation of Temporal Saccade Prediction from Childhood to Adulthood: Predictive Saccades, Reduced Pupil Size, and Blink Synchronization

et al. 2021

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“…On the other hand, no correlation was found with the dysarthria scores 90 and postural instability 93 . This may be because cognitive and motor abilities do not decline equally together 94 …”

Section: Discussionmentioning

confidence: 95%

“…The scale was used in six neuroimaging studies, 75 , 83 , 85 , 87 , 94 , 95 eight cognitive studies, 74 , 82 , 84 , 88 , 89 , 91 , 93 , 96 and three studies examining other clinical aspects of HD (eg, balance, dysphagia) 80 , 90 , 92 …”

Section: Resultsmentioning

confidence: 99%

“…In addition, all the diagnostic test accuracy studies 71 , 72 , 76–78 were published before 2017. In the last 4 years, 14 studies reported the use of MoCA in HD patients: one prevalence study, 86 five neuroimaging studies, 83 , 85 , 87 , 94 , 95 six cognitive studies, 84 , 88 , 89 , 91 , 93 , 96 and two studies investigating clinical aspects of HD 90 , 92 . Nonetheless, the last diagnostic test accuracy study was done in 2013 77 …”

Section: Discussionmentioning

confidence: 99%

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Montreal cognitive assessment for evaluating cognitive impairment in Huntington’s disease: a systematic review

Roşca

Simu

2020

CNS Spectr.

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Objective This study aims to systematically review evidence of the accuracy of the Montreal Cognitive Assessment (MoCA) for evaluating the presence of cognitive impairment in patients with Huntington’s disease (HD) and to outline the quality and quantity of research evidence available about the use of the MoCA in this population. Methods We conducted a systematic literature review, searching four databases from inception until April 2020. Results We identified 26 studies that met the inclusion criteria: two case–control studies comparing the MoCA to a battery of tests, three studies comparing MoCA to Mini-Mental State Examination, two studies estimating the prevalence of cognitive impairment in individuals with HD and 19 studies or clinical trials in which the MoCA was used as an instrument for the cognitive assessment of participants with HD. We found no cross-sectional studies in which participants received the index test (MoCA) and a reference standard diagnostic assessment composed of an extensive neuropsychological battery. The publication period ranged from 2010 to 2020. Conclusions In patients with HD, the MoCA provides information about disturbances in general cognitive function. Even if the MoCA demonstrated good sensitivity and specificity when used at the recommended threshold score of 26, further cross-sectional studies are required to examine the optimum cutoff score for detecting cognitive impairments in patients with HD. Moreover, more studies are necessary to determine whether the MoCA adequately assesses cognitive status in individuals with HD.

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“…Considering these outstanding questions, we aimed at assessing response inhibition and, hence, impulsivity, in an objective manner, by using an oculomotor paradigm with a component of inhibitory motor control and increasing cognitive load. Oculomotor impairments are precisely among the first manifestations of HD, with saccadic abnormalities having been frequently described in HD patients [1, 4, 22, 40–47]. Although mixed findings have been reported about premanifest HD individuals’ oculomotor performance [4, 40–43, 48–50], studies have shown significant alterations in antisaccade and memory-guided saccade measures of latency, higher variability of saccade latency and increased error rates [4, 40, 43, 45, 50].…”

Section: Introductionmentioning

confidence: 99%

The effect of impulsivity and inhibitory control deficits in the saccadic behavior of premanifest Huntington’s disease individuals

Júlio

Caetano

Januário

2019

Orphanet J Rare Dis

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Background: This study aims to test response inhibition in premanifest Huntington's disease individuals (Pre-HD), in the context of a saccadic paradigm with working memory demands and fronto-executive load as a way to measure inhibitory control deficits and impulsive behavior in Huntington's disease (HD). Methods: The oculomotor function of 15 Pre-HD and 22 Control individuals was assessed using an experimental paradigm comprising four horizontal saccadic tasks: prosaccade (PS), antisaccade (AS), 1-or 2-back memory prosaccade (MPS), and 1-or 2-back memory antisaccade (MAS). Success rate, latency, directional and timing errors were calculated for each task. A comprehensive battery of neuropsychological tests was also used to assess the overall cognitive functioning of study participants. Statistical correlations between oculomotor, clinical and cognitive measures were computed for the Pre-HD group. Results: Pre-HD participants showed reduced success rate in the AS task, increased direction errors in the AS and MAS tasks and decreased latency in the MAS task when compared to Controls, despite presenting similar executive and memory scores in the conventional neuropsychological tests applied. Significant associations were identified between specific AS and MAS parameters and disease-related measures, cognitive skills and other oculomotor results of Pre-HD participants. Conclusions: Our results show that oculomotor performance in premanifest Huntington's disease deteriorates once inhibitory control, working memory and/or fronto-executive load are added to the task. A more automatic pattern of performance, including a faster response time and directionally erroneous eye movements were detected in the oculomotor behavior of the Pre-HD group-these alterations were significantly correlated with disease stage and cognitive status. Our saccadic paradigm was able to capture impulsivity and inhibitory control deficits in a group of Pre-HD individuals on average far from symptom onset, thus holding the potential to identify the earliest diseaserelated changes.

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Implicit learning impairment identified via predictive saccades in Huntington's disease correlates with extended cortico-striatal atrophy

Cited by 6 publications

References 50 publications

Maturation of Temporal Saccade Prediction from Childhood to Adulthood: Predictive Saccades, Reduced Pupil Size, and Blink Synchronization

Maturation of Temporal Saccade Prediction from Childhood to Adulthood: Predictive Saccades, Reduced Pupil Size, and Blink Synchronization

Montreal cognitive assessment for evaluating cognitive impairment in Huntington’s disease: a systematic review

The effect of impulsivity and inhibitory control deficits in the saccadic behavior of premanifest Huntington’s disease individuals

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