Accelerated decline in motor suppression in patients with cerebrovascular disorders: A kinetic analysis using the square-tracing task

1 Introduction

Diller and Weinberg (1970)reported that the slowness and quickness of individuals with right and left hemiplegia, respectively, are associated with a history of multiple accidents. Rapport et al. (1993) suggested that impulsivity and attention disorders, assessed using a questionnaire and neurological assessments, are related to falls in patients with right hemisphere damage. In addition to the risk of falls and accidents, patients with cerebrovascular disorders (CVDs) tend to have difficulty adjusting the speed of intended actions to the situation, for example, they may eat too quickly or move a wheelchair before completing safety settings. Although these symptoms are well-known in clinical practice, to our knowledge, studies published in English have not investigated the underlying pathophysiology. However, rehabilitation research in Japan has focused on addressing this hasty nature of patients with CVD, and studies have investigated the pathophysiology of this symptom, an entity of higher brain dysfunction, ‘pacing impairment’ (Miyamori, 1988).

Most of these previous studies experimentally examined the relationship between the line-tracing speed of patients and other clinical symptoms or cerebral lesions using the ‘square-tracing task’ developed by Hirabayashi et al. (1998). The methods section of this manuscript describes the square-tracing task in detail. Thus far, pacing impairment has been associated with motor impersistence (MI) (Hirabayashi et al., 1991; Numata et al., 2003), unilateral spatial neglect (USN) (Hamada et al., 2000), and attention deficit (Yotsumoto et al., 2010), while no apparent association with MI (Hamada et al., 2000) or USN (Hirabayashi et al., 1991; Numata et al., 2003) has also been reported. It seems difficult to attribute pacing impairment to any previously known neuropsychological symptom. Concerning the lesion locus responsible for this symptom, studies have reported the right frontal lobe region perfused by the middle cerebral artery adjacent to the watershed region (Hirabayashi et al., 1991, 2008). However, lesions in the left hemisphere can also present pacing impairment (Hamada et al., 2000, Hirabayashi et al., 1998).

The current summary of these studies is that although pacing impairment and symptoms such as USN, MI, and attention deficit may share a partially common pathological basis, they are mutually independent symptoms (Hamada et al., 2000, Hirabayashi et al., 2008). However, previous studies have not considered this important question: Is the hastiness of patients with CVD uniformly fast, or does it change over time (does it gradually become faster, or does it start fast and slow down over time)?

Therefore, in this study, we aimed to clarify the detailed pathophysiology of pacing impairment by measuring the tracing speed (trace length within 120 seconds) as the conventional method as well as acceleration in the square-tracing task. The study also examined whether pacing impairment can be attributed to other symptoms and whether it is related to a specific cerebral lesion or lateralised to the left or right hemisphere by examining the relationships between these measurements and neuropsychological symptoms or lesion sites.

2 Material and methods

2.2 Square-tracing task

All participants performed the square-tracing task developed by Hirabayashi et al. (1998) (Fig. 1). In this task, the examiner asked the participants to trace a 200 mm -sided square printed on an A3-sized paper with a pencil as slowly as possible and measured the length traced in 120 seconds. The examiner instructed the participants in the CVD group to use only the hand ipsilateral to their cerebral lesions, whereas those in the OD and HC groups used both hands separately. In the original method (Hirabayashi et al., 1998), tracing was performed clockwise with either hand. However, in this study, tracing was performed clockwise if the right hand was used and counter-clockwise if the left hand was used, and the hand not used was placed on the knee or an armrest. Before performing the task, the examiner provided the following instruction: ‘From the start point, trace along the sides of the square drawn on the paper as slowly as possible, without stopping or lifting the pencil’. Each participant’s tracing motion was recorded using three video cameras installed at the front, contralateral to the hand, and above the front of the patient.

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Fig. 1

Square-tracing task. We instructed participants to trace a 200 mm -sided square as slowly as possible from the top midpoint, either clockwise with the right hand or counter-clockwise with the left hand, without stopping or lifting the pencil.

3 Results

3.1 Square-tracing task

We analysed the data of all participants without missing values. Figure 2 shows the performance of the three groups in the square-tracing task. Of the 53 patients, 20 (9 with right- and 11 with left-sided lesions) in the CVD group and 7 (2 traced using the right hand, 2 using the left hand, and 3 using both hands) of 20 patients in the OD group had ‘excessive speed’. In these patients, the trace lengths of each hand were above the third quartile plus 1.5 times the IQR of those in the HC group (626.9 mm using the right hand and 694.5 mm using the left hand).

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Fig. 2

Trace length and acceleration distribution. Patients with CVD performed the task using the hand on the non-paralysed side; however, the HC and OD groups performed this task with both hands. The dotted line indicates the cut-off value. CVD, cerebrovascular disorder; OD, orthopaedic disease; HC, healthy controls.

Regarding mean acceleration, 22 (11 with right- and 11 with left-sided lesions) of the 53 patients in the CVD group and 4 (2 traced using the right hand and 2 using the left hand) of the 20 patients in the OD group had ‘excessive acceleration’ above the third quartile plus 1.5 times the IQR of those in the HC group (0.0183 mm/s² using the right hand and 0.0164 mm/s² using the left hand).

Trace length and mean acceleration were positively correlated in the CVD group (ρ= 0.731, p < 0.01). While ‘excessive speed’ and ‘excessive acceleration’ were present and overlapped in 16 patients, ‘excessive speed’ alone was observed in 4 patients and ‘excessive acceleration’ alone in 6 others.

Trace lengths in the CVD and OD groups were significantly longer than those in the HC group (p < 0.05). No significant difference in trace length was observed between the CVD and OD groups. The mean acceleration in the CVD group was significantly higher than those in the OD and HC groups (p < 0.05). No significant difference in trace length or mean acceleration was observed between the two CVD subgroups in the right and left hemispheres.

Statistical power was calculated as the post hoc test for above significant results. 1-β error for all of them was≥0.80.

4 Discussion

The novelty of this study is the attempt to measure and analyse changes in speed during the square-tracing task and, based on the results, the attempt to re-examine whether pacing impairment is due to known symptoms of higher brain dysfunction or the involvement of specific brain lesions, which are unresolved issues in the literature.

There was a significant difference in the mean acceleration between the CVD and OD groups, which could not be demonstrated using the conventional measure of trace length at 120 seconds, i.e., speed. In other words, motor suppression rapidly attenuates on a timescale of tens of seconds in patients with CVD.

The correlation between trace length/mean acceleration and neuropsychological assessments in the CVD group also presents several new findings (Table 1). First, MI showed no apparent association with either mean acceleration or trace length, regardless of whether it was a right or left hemisphere lesion. Second, the degree of USN (linear bisection test) correlated with trace length and mean acceleration only in patients with right hemisphere lesions.

Third, the results of various subtests for frontal lobe dysfunction and generalised attention disorder showed that the functional deficits in the right hemisphere lesion subgroup correlated only with mean acceleration and not with trace length. In contrast, the functional deficits in the left hemisphere lesion subgroup had more items that correlated with trace length than with mean acceleration. This third finding suggests that the correlation reflects the different roles of the right and left hemispheres in maintaining movement control. However, despite these different characteristics, no apparent difference in performance on the tracing task was observed between the two subgroups.

In summary, the results of the present study and those of previous studies suggest that it is difficult to attribute pacing impairment to any known specific neuropsychological symptom. Rather, these findings suggest that this symptom can be manifested by disorders of various attentional functions scattered across a wide range of cerebral regions; whether directional or generalised attention and whether right or left hemispheric function.

The results of the present study at the lesion site also support this hypothesis. Most studies have emphasised the association between pacing impairment and lesions in the right hemisphere (Hirabayashi et al., 1991, 1998, 2008; Miyamori, 1988; Yotsumoto et al., 2010), particularly in the deep frontal lobe (Hirabayashi et al., 1991); however, the incidence of trace length and excessive acceleration did not differ between right and left hemisphere lesions, and no specific common lesion was found.

It is easy to speculate that damage to the supplementary motor cortex, which is involved in deliberate motor control, the dorsolateral prefrontal cortex, which is involved in sustained attention and self-monitoring, or the cortico-basal ganglia-thalamo-cortical loop (Alexander & Crutcher, 1990), which carries those functional systems, would cause pacing impairment. The presence of these lesions may be sufficient for the development of this symptom; however, these lesions may not always be necessary. Damage to the posterior cerebral regions involved in the visual, somatosensory, or other perceptual aspects of attentional function required to perform the tracing task is also presumed to cause this symptom.

From the results of this study, it should be noted that excessive speed and acceleration were also observed in patients with ODs. High load-bearing tasks, such as maintenance of deliberate motor control for extended periods, are only possible with a well-developed and fully functioning brain. Moreover, even central nervous system dysfunction without obvious organic damage, including ageing or physically inactive states, may interfere with such higher cognitive tasks. One of the results of this study that the age correlated with the trace length in the HC group may also support this speculation. It is possible to interpret higher brain function from a holistic perspective, in which symptoms are not solely determined by the local function of the damaged region but result from a breakdown in the integration of brain function and regression to an earlier developmental level of function.

This study has several limitations. First, we excluded patients with severe aphasia, obvious motor deficits, or visual and spatial deficits. Therefore, we included only a few cases with lesions expanding to the cerebral cortex, and patients with subcortical lesions were prominent in the sample population. Hence, the extent to which the relationship between lesion location and neuropsychological symptoms could be examined was limited. Second, most of the participants with CVD in this study were in the subacute phase, and whether similar experimental findings of pacing impairment can be obtained in the chronic phase is unclear. Third, the acceleration of movement was observed in the experiment using the tracing task alone, and the relationship between the change in movement speed and the risk of falling in actual activities of daily living situations was not examined. Future studies should examine the correlation between the results of the present experimental study and other ecological assessments of pacing disorder based on behavioural observations to confirm the validity of the assessment method.

5 Conclusion

Many patients with CVD present with a rapid decline in their ability to maintain deliberate motor control due to various lesions. Rehabilitation efforts focused on motor speed control may reduce the risk of falls and other accidents and improve activities of daily living in patients with CVD.