Lowered Rhythm Tapping Ability in Patients With Constructional Apraxia After Stroke

What the fuck is the solution to the problem you describe? No solution; you're fired. My director would have fired me in no time if my response was just that, describing a problem but offering no solution, or even a method to solve it.

 

Lowered Rhythm Tapping Ability in Patients With Constructional Apraxia After Stroke

 

Naomi Kobinata^1,2*, Hideto Yoshikawa³, Yuji Iwasaka⁴ and Nobuyuki Kawate¹

• ¹Department of Rehabilitation Medicine, School of Medicine, Showa University, Tokyo, Japan
• ²Department of Rehabilitation, Yoshieikai Hospital, Osaka, Japan
• ³Department of Medicine, Tokyo Chidori Hospital, Tokyo, Japan
• ⁴Department of Physical Therapy, Nihon Institute of Medical Science, Saitama, Japan

Rhythm tapping tasks are often used to explore temporal reproduction abilities. Many studies utilizing rhythm tapping tasks are conducted to evaluate temporal processing abilities with neurological impairments and neurodegenerative disorders. Among sensorimotor and cognitive disorders, rhythm processing abilities in constructional apraxia, a deficit in achieving visuospatial constructional activities, has not been evaluated. This study aimed to examine the rhythm tapping ability of patients with constructional apraxia after a stroke. Twenty-four patients were divided into two groups: with and without constructional apraxia. There were 11 participants in the constructional apraxia group and 13 in the without constructional apraxia group. The synchronization-continuation paradigm was employed in which a person performs a synchronized tapping activity to a metronome beat and continues tapping after the beat has stopped. For statistical analysis, a three-way mixed analysis of variance (2 × 2 × 3) was conducted. The factors were groups (with and without constructional apraxia), tapping tasks (synchronization and continuation), and inter-stimulus intervals (600, 750, and 1000 ms). A significant effect of group factor was found (F[1,132] = 16.62; p < 0.001). Patients in the without constructional apraxia group were able to more accurately reproduce intervals than those in the constructional apraxia group. Moreover, a significant effect of tapping tasks was found (F[1,132] = 8.22; p < 0.01). Intervals were reproduced more accurately for synchronization tasks than continuation tasks. There was no significant inter-stimulus interval effect. Overall, these results suggest that there might be a relation between temporal and spatial reproductions in a wide spectrum of processing levels, from sensory perception to cognitive function.

Introduction

Rhythm tapping tasks are often used to explore temporal reproduction abilities (see Repp and Su, 2013, for a review). It is often performed as a finger tapping task in synchrony with an external rhythm, usually a steady metronome beat (Repp and Su, 2013). Along with the synchronization paradigm, synchronization-continuation tasks are often used to assess entrainment to an external rhythm (Flach, 2005; Ullén et al., 2008; Avanzino et al., 2013; McPherson et al., 2018). With synchronization-continuation tasks, individuals tap in synchrony to an external beat and continue tapping after the external beat has stopped (Flach, 2005).

In synchronization tasks, automatic or cognitive control is involved depending on the speed of the external beat (Miyake et al., 2004; Repp and Su, 2013; Bååth et al., 2016). In time perception research, sub-second time processing is automatic and supra-second time processing involves cognitive control (Bååth et al., 2016). For example, Mangels et al. (1998) showed that patients with prefrontal lesions who had difficulty with a non-temporal working memory task also struggled with long duration temporal discrimination (4-s interval) but not with short duration temporal discrimination (400-ms interval). Miyake et al. (2004) conducted a study employing the dual tasks of synchronization tapping and word-memory; they found that with anticipatory tapping, synchronization with a stimulus interval of 1800 to 3600 ms was affected by a word-memory task but not synchronization with a stimulus interval of 1500 ms or less. Similar results were found with dual tasks involving executive control (Bååth et al., 2016).

Neural mechanisms for time measurement support the available behavioral evidence. Measurements of sub-second intervals revealed activity in the bilateral supplementary motor area, left sensorimotor cortex, right cerebellum, right lateral premotor area, left thalamus, left basal ganglia, and right superior temporal gyrus (Lewis and Miall, 2003). In cognitively controlled timing tasks, the right prefrontal and parietal cortices were involved in addition to some parts of the autonomic system (right premotor area and bilateral supplementary motor area) (Lewis and Miall, 2003).

Compared to the synchronization paradigm, synchronization-continuation requires internal pacing without external cues and increases the neural resources required (Serrien, 2008). In Serrien (2008)’s study, electroencephalogram coherence increased in mesial-central connections under the continuation condition. Moreover, Ullén et al. (2008) reported a correlation between tapping stability and the volume of the right prefrontal white matter regions under a continuation condition. These studies show that performing a continuation task requires internal control and increases neural activities. Unlike the synchronization task, the continuous sub-second tapping task requires cognitive control. According to Ullén et al. (2008), intelligence and the stability of continuous sub-second tapping were correlated; also, Holm et al. (2017) reported that executive control and working memory were involved in continuous sub-second tapping.

Many studies utilizing rhythm tapping tasks are conducted to evaluate temporal processing abilities with neurological impairments and neurodegenerative disorders (Freeman et al., 1993; Schwartze et al., 2011, 2016; Avanzino et al., 2013; Roalf et al., 2018). Schwartze et al. (2016) reported that patients with cerebellar lesions display imprecise temporal processing compared to healthy participants in a control group. Similar results were reported with patients with basal ganglia lesions that might have impaired attention-dependent temporal processing (Schwartze et al., 2011). Furthermore, with Parkinson’s disease, temporal processing impairments were discussed in association with abnormalities of internal rhythm generation (Freeman et al., 1993) and motor planning impairments (Avanzino et al., 2013). Besides these reports, studies have shown time processing impairments in cases of Huntington’s disease (Agostino et al., 2017), Alzheimer’s disease (Roalf et al., 2018), mild cognitive impairment (Roalf et al., 2018), attention deficit hyperactivity disorder (Hove et al., 2017), and aphasia (Zipse et al., 2014).

Among sensorimotor and cognitive disorders, rhythm processing abilities in constructional apraxia have not been examined. Constructional apraxia is defined as a deficit in performing visuospatial constructional activities (Cubelli and Della Sala, 2018; Gainotti and Trojano, 2018) such as 2- or 3-dimensional copying or reproducing a drawing from memory and re-arranging patterns by blocks or sticks (Laeng, 2006; Russell et al., 2010); it is caused by cerebrovascular diseases such as stroke or brain damage on either hemisphere or neurodegenerative diseases such as Alzheimer’s disease (Mack and Levine, 1981; Trojano et al., 2004; Laeng, 2006; Gainotti and Trojano, 2018). With stroke patients, lesion sites associated with constructional apraxia include the basal ganglia, thalamus, posterior parietal lobule, lingual gyrus, calcarine, insula, temporal gyrus, temporo-parietal junction (Chechlacz et al., 2014), parietal lobes, frontal lobes, and occipital lobes (Cubelli and Della Sala, 2018). Notably, various regions of the brain are involved in the drawing process. Therefore, constructional apraxia is related to a broad range of symptoms including: dysfunctions in visuospatial abilities such as the processing of shapes and the interrelations between different components of objects, perception, attentional allocation to global and local features, executive functions such as planning, and motor mechanisms (Chechlacz et al., 2014; Gainotti and Trojano, 2018).

Based on studies on lowered cognitive abilities with constructional apraxia (Laeng, 2006; Chechlacz et al., 2014; Nagaratnam et al., 2014; Gainotti and Trojano, 2018) and on the involvement of cognitive control such as general intelligence, working memory, and executive control on temporal reproduction (Ullén et al., 2008; Holm et al., 2017), it is likely that patients with constructional apraxia would show lowered temporal processing that requires cognitive control. It is worth examining the automatic temporal processing abilities of patients with constructional apraxia, including impairments in visuospatial perception, given the shared temporal and spatial performance and shared neural resources in sensorimotor synchronization (Doumas and Wing, 2007; Comstock et al., 2018), the common magnitude system in spatial lines and temporal duration representation (De Corte et al., 2017), the left-to-right ordering system (Bonato et al., 2016), and the temporal coding of visual spaces (Rucci et al., 2018).

The current study aims to examine the rhythm tapping ability of patients with constructional apraxia after a stroke. The performance of patients was examined during synchronization and continuation tapping tasks with sub-second stimulus intervals. If the patients demonstrated a lowered ability to synchronize with sub-second stimulus intervals, then their automatic timing process was regarded as lowered. If the patients’ sub-second continuation tapping was less accurate than those without constructional apraxia, then a deficit in cognitive control on temporal reproduction was suggested. Based on previous studies (Laeng, 2006; Doumas and Wing, 2007; Ullén et al., 2008; Chechlacz et al., 2014; Nagaratnam et al., 2014; Bonato et al., 2016; De Corte et al., 2017; Holm et al., 2017; Comstock et al., 2018; Gainotti and Trojano, 2018; Rucci et al., 2018), we hypothesized that patients with constructional apraxia would perform less accurately with both sub-second synchronization and continuation tapping tasks than those without constructional apraxia.

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