A Comprehensive Exploration of Motor, Sensory, and Physiological Factors in a Case of Limb Kinetic Apraxia Following Traumatic Brain Injury

Abstract

We herein report a 16-year-old boy who presented with limb-kinetic apraxia, which was presumed to be an impairment of sensorimotor integration due to brain damage localized to the central region after head trauma. The patient's basic sensory and motor functions were also preserved. However, deficits were noted in two-point discrimination (a higher-order sensory function), material identification, and three-dimensional geometric figure identification: sensorimotor tests that include active touch (a function of sensorimotor integration). The present case suggests that a thorough neurological examination from the perspective of sensorimotor integration is important to understand the pathology of limb-kinetic apraxia.

Introduction

According to Liepmann, the loss of the ability to make deft or dexterous movements is called ‘limb-kinetic apraxia’ (LKA) (1). In contrast to other variants of apraxia, such as ideational and ideomotor apraxia, LKA is not confined to movements directed by a conscious plan but rather affects the routine use of objects (2). Although it is defined as a fine movement disorder that is not caused by motor or sensory impairment, its evaluation criteria remain unclear. Baumard and Gall (3) also mentioned the unclear nature of the diagnostic parameters for LKA. In addition, the perception of LKA as a primary or elemental motor dysfunction (4) raises questions regarding its accurate classification as true apraxia, further complicating its recognition and treatment (5). Therefore, in this report, we adopted the Ishiai (6) position, which is that LKA is likely the result of minor motor disorders or disturbances in sensorimotor integration. In other words, LKA refers to “motor symptoms in which the hand and fingers can be moved separately, making it difficult to identify motor paralysis and in which dexterity is poor”. This definition includes a position that considers it a type of slight motor paralysis (6).

From this perspective, it seems important to examine in detail the sensory and motor functions, as well as the sensorimotor integration that combines them, in patients with LKA to understand one aspect of this condition. However, few reports have examined LKA in detail, particularly from the perspective of sensorimotor integration. Therefore, there is currently no consensus or sufficient understanding of the pathology and mechanism of LKA (7). Sensorimotor integration is the process of incorporating sensory input that provides information about one's body and external environment to shape movement (8-10). Katz noted that ‘smoothness and roughness do not arise when the tactile tissue is stationary but only when it moves relative to the tactile surface’ (11). This finding suggests the importance of movement in tactile perception. This perception of objects through hand exploration is called ‘active touch’ (12) and is achieved through sensorimotor integration (13). Therefore, to examine sensorimotor integration effectively, it is important to use motor control tasks that rely on sensory information along with perceptual discrimination tasks that require movement, in addition to evaluating sensory and motor functions (9,14). These tests include sensory evaluations through active touch, such as material identification and three-dimensional geometric figure identification (15). We believe that this approach allows us to assess the state of sensorimotor integration.

In the present case report, we conducted a comprehensive examination and integrative analysis of motor, sensory, and sensorimotor integration in a patient with LKA after focal central area injury due to head trauma.

Case Report

A 16-year-old right-handed boy was admitted to our hospital as an emergency case of fall-related injury. The diagnoses included subdural hematoma, traumatic subarachnoid hemorrhaging, cerebral contusion, and a fracture in the right metatarsal. At the time of transport, he had a score of 14 points on the Glasgow coma scale (E3, V5, and M6), and he was administered conservative treatment. Neuropsychological screening revealed an intact cognitive function. Computed tomography and fluid-attenuated inversion recovery brain magnetic resonance imaging (MRI) showed cerebral contusion changes in the central cortical area of the right cerebral hemisphere and middle frontal gyrus (Fig. 1A, B).

Figure 1.

(A) Axial noncontrast head computed tomography (CT) showing subdural hematoma on the right side on day of injury. (B) Axial fluid-attenuated inversion recovery (FLAIR) brain magnetic resonance imaging (MRI) showing contusions in right cortices on day 8 after the onset. The high- intensity areas (solid yellow circles) appear to include the precentral gyrus, postcentral gyrus, and middle frontal gyrus. These lesions seem to involve the motor and sensory cortices, as well as the premotor cortex.

Barre sign was negative, and he had no motor paralysis. However, a detailed evaluation of the upper extremities by an occupational therapist revealed LKA. The patient exhibited grip strength of 27 kg in the right hand and 17 kg in the left hand. Regarding his ability to manipulate objects, his scores on the simple test for evaluating hand function (STEF; 16, 17) were 100 points for the right hand and 90 points for the left hand. The STEF showed no abnormalities in grasping and releasing large-to-medium-sized objects, but there was a decrease in the manipulation of small objects, such as pins and gold discs. Deterioration of the hands and fingers owing to LKA was observed, including difficulty in folding and opposing fingers, picking up coins, and retrieving items from bags (Supplementary material). In terms of the sensory function, tactile sensation was slightly impaired at 3.61 in the Semmes-Weinstein monofilament test (index finger), and a 2-point discrimination (index finger) of 25 mm was not possible. The sensations of temperature, pain, vibration, and joint position, as well as the results of the thumb-finding test, were normal. However, as shown in Fig. 2A and B, identification of the material decreased to 6/18, and identification of a three-dimensional geometric figure decreased to 15/18 (18).

Figure 2.

Motor-sensory and electrophysiological assessments. (A) Identification of material: Initially, the patient was tasked with verbally identifying the material through active tactile exploration, and then he was asked to select a response from a set of six options that represented the perceived stimulus upon touch (a: leather split, b: leather grain, c: file, d: craft tape, e: velcro hook, f: velcro loop). (B) Identification of a three-dimensional geometric figure: initially, the patient was prompted to verbally identify the figure on his palm. Next, he was asked to select an answer from a pool of six options regarding the identified stimulus upon touch. Each figure in the set has a standardized height of 8 mm. For instance, the zebra geometric figure, measuring 48 mm in length and 69 mm in width, is made of wood (Ed. Inter, Amagasaki, Japan). (C) The somatosensory evoked potential (SEP) with median nerve stimulation of the right (a) and left (b) arms is depicted. SEPs recorded from the parietal lead located 2 cm posterior to C3 or C4. (D) Pinch adjustment ability test (pinch test): tests the tracking error, which reflects the regime of force control. The upper row on the left shows the test limb position. The lower monitor shows how the pinch force (Raw) follows the index. In the graph on the right, the black line is the index, and the red line is the raw pinch force.

Somatosensory evoked potentials (SEPs) and pinch tests were used to objectively examine the degree of sensory impairment and ability to adjust force in the hands and fingers (Fig. 2C, D). The N20-P25 amplitude values of SEPs with median nerve stimulation decreased to approximately 1/3 of those in the right upper extremity, but the latencies of N20 were normal on both sides. Although there was no decrease in tactile sensation, it strongly affected object manipulation. In the pinch adjustment ability test (pinch test), which requires motor and sensory functions (19,20), the patient showed the same ability as healthy subjects, with no marked difference between the left and right sides. Furthermore, the patient's poor handling of objects could not be compensated for, even under conditions with visual confirmation.

The patient underwent occupational therapy (OT), which resulted in a gradual improvement in dexterity. After approximately 50 days of hospitalization, the STEF score increased to 99, which was within the normal range for people of the same age. While there were no changes in tactile sensation or two-point discrimination ability, the scores for sensorimotor integration increased (identification of material: 14/18, identification of a three-dimensional geometric figure: 17/18).

Discussion

The primary aim of this case report was to provide a comprehensive examination and analysis of motor, sensory, and sensorimotor integration. Although slight reductions were observed in the tactile sensation and N20-P25 amplitudes of the SEP, the N20 latencies remained normal. In addition, assessments for temperature sense, pain perception, vibration sensitivity, joint position sense, and the thumb-finding test yielded normal results, indicating that basic motor and sensory functions were well preserved. The successful performance of the pinch test, which requires advanced motor and sensory skills, further supports this conclusion. Significant decline was recorded in tests involving active touch, particularly in the identification of materials and three-dimensional geometric figures (17), and in two-point discrimination, which is considered a higher-order sensory function (14).

Our findings suggest that, while the patient's sensorimotor integration was impaired in the active touch tests, no abnormalities were detected in the pinch test. This disparity emphasizes the complex nature of LKA and indicates that different aspects of sensorimotor integration may be affected (21). Effective object recognition by active touch is possible only if the hand can fully explore the object, i.e. if the hand maintains the motor control necessary to manipulate the object (22). Therefore, it is possible that impairments were more pronounced in the identification of materials and three-dimensional geometric figures, which require fine motor control. However, the pinch task required patients to adjust the force while keeping their fingers fixed in place and did not require them to explore the object. In addition, visual feedback may have made the task easier for the patients. The STEF score increased to normal after OT, indicating that the patient was able to manipulate objects more precisely. Consequently, he was able to explore objects more precisely, which may have led to improved performance in the discrimination task.

The inferior parietal lobule, a critical cortical area for processing tactile information during active touch and two-point discrimination, is also implicated in sensorimotor integration (23). Notably, research has shown that older individuals with a history of falls exhibit reduced two-point discrimination (24), and active touch has been linked to fine motor skills (25), reinforcing the significance of these sensory functions in daily activities and motor control.

Our patient developed LKA as a result of a brain contusion following a head injury. Considering the nature of head trauma, it is possible that the damage occurred in areas where no changes were evident on imaging. However, as shown in Fig. 1A and B, damage is likely to be localized in the central region of the brain, a common focal area for LKA, specifically in the sensorimotor cortex. This localized lesion aligns with areas typically implicated in LKA (25,26).

Our patient presented with Liepmann's definition of LKA, “a dexterity disorder not due to motor or sensory disorder,” and had a focal lesion in the central region, which is presumed to be the responsible lesion, so there was no inconsistency in the diagnosis of LKA (1,2). Although there have been few reports of detailed lesions in LKA using brain images, Kawamura et al. (25) investigated two cases with focal lesions in the central region using MRI scans (one with damage to the precentral gyrus and one with damage to the postcentral gyrus) and showed that LKA is caused by a lesion in the central region.

Yamadori (27) investigated a case of clumsiness of the left hand in the manipulation of objects in detail and proposed “palpatory apraxia” as a symptom, similar to LKA. Similarities to the findings in our patient include the preservation of basic sensation and deterioration of higher sensory function and sensory tests involving active touch. However, Yamadori's patient showed preserved finger counting and opposition movements and a better motor function (dexterity) of the fingers than our patient. The lesion in his patient was located in the sensorimotor cortex. Perhaps for this reason, the impairment in dexterity of the hand in his patient was prominent without visual feedback but often good with visual feedback; in contrast, our patient's dexterity impairment was prominent, even with visual feedback. Based on these findings, Yamadori concluded that the clumsiness of the hand in his patient was apraxia caused by dysfunction of the neural structures supporting the mechanism of active touch. Freund et al. (28) examined cases of premotor cortex damage in detail and suggested that LKA might result from the impaired initiation and coordination of movements associated with this lesion.

Binkofski et al. (29) conducted a detailed study of the motor and sensory functions, including active touch, in patients with clumsy behavior due to lesions of the parietal lobe (primary sensory cortex, superior and inferior parietal lobules) or frontal lobe (primary motor cortex, premotor cortex). They found that patients with parietal lobe lesions had a preserved ability to perform repetitive finger movements but showed impaired “active touch,” an exploratory finger movement necessary for collecting sensory information. They considered this impairment to be a form of apraxia related to clumsiness, known as “tactile apraxia.” In contrast, patients with frontal lobe lesions showed that the function of “active touch” was preserved in repetitive finger movements, despite impaired frequency and regularity of movements.

Our patient also had significant impairments, such as finger counting and opposition movements, so it is possible that he also had elements due to reduced coordination of muscle activity and disturbance of motor sequence, as suggested by Freund et al. (28) and Binkofski et al. (29). Because our patient presented with lesions in the premotor cortex in addition to the motor and sensory cortices, it is possible that he had an LKA caused by impaired sensorimotor integration, as described by Yamadori (27), Freund et al. (28), and Binkofski et al. (29), respectively. The location of the injury and the presence or absence of symptoms in previous reports as well as in our present case are summarized in Table.

Table.

Comparison of Lesion Area, Preserved and Impaired Functions, and Active Touch Evaluation in Limb-kinetic Apraxia, Palpatory Apraxia, and Tactile Apraxia.

Reference	Term of clumsiness-related apraxia	Lesion area (diagnostic imaging methods)	Preserved function	Impaired function
(27)	Palpatory apraxia	Sensorimotor cortex (CT: n=1)	Motor aspect Mobility and power of individual fingers Simple dynamic coordination Sensory aspect Sense of touch, pain, temperature, vibration	Motor aspect Complex dynamic coordination fine manipulation of object Sensory aspect Point localization Two-point discrimination Active touch (Sensorimotor integration) Sense of active movement Texture evaluation Stereognosis
(28)	Limb-kinetic apraxia	Premotor cortex (CT: n=5)	Motor aspect Power of individual fingers Simple dynamic coordination	Motor aspect Weakness of proximal musculature Initiation disturbance of movement Coordination task in which temporal sequence
(25)	Limb-kinetic apraxia	(A) primary motor cortex and premotor cortex (CT and MRI: n=1) (B) primary sensory cortex (CT and MRI: n=1)	Motor aspect (A and B) power of individual fingers Sensory aspect (A and B) sense of touch, pain, temperature, vibration Active touch (Sensory motor integration) (A) stereognosis	Motor aspect (A and B) complex dynamic coordination fine manipulation of object (A and B) mobility of individual finger Active touch (sensorimotor integration) (B) texture evaluation (B) stereognosis
(29)	Tactile apraxia	(A) primary sensory cortex and superior parietal lobule (MRI: n=5) (B) primary sensory cortex and inferior parietal lobule (MRI: n=5)	Motor aspect (A and B) mobility and power of individual fingers (A and B) simple dynamic coordination Sensory aspect (B) sense of touch	Sensory aspect (A) sense of touch Active touch (sensorimotor integration) (A and B) stereognosis (A and B) exploratory finger movement (A and B) object recognition
Present case	Limb-kinetic apraxia	Primary motor cortex, primary sensory cortex and premotor cortex (MRI: n=1)	Motor aspect Power of hand grip Sensory aspect Sense of touch, pain, vibration, joint position Thumb-finding test Latencies of SEP Sensorimotor integration with visual feedback Pinch test	Motor aspect Complex dynamic coordination fine manipulation of object Folding and opposing fingers Mobility of individual fingers Sensory aspect Two-point discrimination Amplitude of SEP Active touch (sensorimotor integration) Identification of material Identification of a three-dimensional geometric figure

CT: computed tomography, MRI: magnetic resonance imaging, Pinch test: the pinch adjustment ability test, SEP: somatosensory evoked potential

As this report is based on a single case, it is difficult to generalize the present outcome to all pathomechanisms of LKA. In the future, we aim to increase the number of cases and conduct studies using techniques such as functional brain imaging to further clarify the pathological mechanisms. Although the mechanisms and diagnostic criteria for LKA remain unclear, we believe that a thorough examination of this case may provide new insights into LKA from the perspective of sensorimotor integration.

The authors state that they have no Conflict of Interest (COI).

Supplementary Material

Deterioration of hand and finger function owing to limb-kinetic apraxia

(A) Disorders in the flexion of the fingers sequentially and finger tapping were clearly observed. (B) Difficulty in picking up coins. (C) Difficulty in visually confirming and retrieving items from transparent bags. Finger mass flexion and extension were possible (A). Although the patient was unable to pick up the eraser, rapid finger movements were intact, indicating no obvious paralysis (C). However, the patient was unable to flex the fingers sequentially and perform finger tapping (A). He also had difficulty visually performing precise actions, such as pinching a coin (B) or picking up an eraser (C), demonstrating impaired dexterity. Based on these findings, we concluded that he met the criteria for limb-kinetic apraxia as defined by Ishiai (6): "motor symptoms lacking dexterity that are difficult to distinguish from obvious motor paralysis because the hand and fingers can be moved separately.”

Funding Statement

This study was supported in part by JSPS KAKENHI Grant Number JP23H03247.