J Neurol Disord Stroke 1(3): 1020.
Submitted: 13 August 2013; Accepted: 13 September 2013; Published: 13 September 2013
Communicative Pointing Ameliorates Grasping Deficits after an Inactivation and Lesions of the Ventral Premotor Cortex in Japanese Monkeys (Macaca fuscata)
Mari Kumashiro1*, Osamu Yokoyama1 and Hidetoshi Ishibashi1,2
Section of Cognitive Neurobiology, Department of Maxillofacial Biology, Tokyo Medical and Dental University, Japan
Department of Neurophysiology, National Center of Neurology and Psychiatry, Japan
Mari Kumashiro, Section of Cognitive Neurobiology, Department of Maxillofacial Biology, Tokyo Medical and Dental University, Japan, Email: firstname.lastname@example.org
Pointing is the most convenient communication in social interaction: its gesture is highly visible and is found in all cultures with the identical form. However, the brain mechanisms of communicative pointing are still unknown. The pointing is, from a psychological point of view, considered to develop from grasping attempt with help from others. Thus, we hypothesized that pointing deficits would appear after lesions of the ventral premotor cortex (PMv) that was fundamental to grasping, and examined whether the pointing would be influenced by the PMv lesions in monkeys. The PMv-lesioned subjects showed deficits in reaching and grasping, and those deficits were, contrary to our expectation, ameliorated through the pointing. A subject with muscimol injection to PMv required 4. 02 sec to obtain food but the time was reduced to 1. 19 sec after communicative pointing. Another subject rarely used one limb after bilateral PMv ablations, but became to grasp food with the hand after the training of communicative pointing. These results suggest that communicative pointing is useful to recover the grasping and reaching deficits induced by PMv lesions.
Keywords: Communicative pointing; Grasping; Reaching; Ventral premotor cortex (PMv); Lesion
Pointing is the communicative gesture that is universal across cultures, and is also importantly related to language acquisition . However, the brain areas involved in the communicative pointing are unknown. From a psychological point of view, Vygotsky (1978) claimed that in humans, pointing is initially an unsuccessful movement to grasp something, and, as other individuals react to this movement, it becomes a movement that has communicative meaning . The ventral premotor cortex (PMv) is engaged in grasping [3,4]. Inactivation of the PMv impairs hand shaping that precedes grasping . Mirror neurons in the PMv has been shown to be active both when a monkey grasps food and when it observes a human grasping of food [6,7].
We attempted to find the brain area responsible for communicative pointing. We hypothesized that monkeys with PMv lesions would show the deficits of the pointing if it is processed in the PMv.
Subjects and communication training: the subjects were a male (Subject A) and a female (Subject B) Japanese monkeys (Macaca fuscata). They were separately housed and were not deprived of food or water. Before the inactivation or ablations, their motor abilities, such as reaching or grasping, were normal. This study was approved by the Animal Care and Use Committee of the Tokyo Medical and Dental University, and all husbandry and experimental procedures were in accordance with the institutional guidelines. Procedure: to investigate the brain area of communicative pointing, we inactivated or ablated the PMv before or after the acquisition of communicative pointing. The training of communicative pointing consists of gaze alternation between human eyes and a desired food, and directing the monkey’s arm and hand toward it. Subject A already had acquired the communicative pointing with gaze alternation, and received a surgical procedure for single neuron recording in PMv according to the previous study . Muscimol (0. 5 μL of 20μg/μL solution, at a rate of 0. 5μL/min) was injected to the right PMv according to the previous report . For Subject B, the single operator bilaterally ablated the PMv by sucking according to the previous report . She recovered within a few hours after the surgery. Two days after the ablation, we started to train her for gaze alternation between the desired food and experimenter’s eyes for two days. Then, we trained her for communicative pointing toward a distant food with the whole hand and for pointing to a nearby food with the index finger by using of a partitioned box for six days (see, [11-13]). This box was also used to test her finger movements.
The effects of muscimol injection were observed three minutes after the injection. Mouth movements and the ipsilateral hand of Subject A were normal after the muscimol injection. He was able to reach and grasp food with the contralateralhand as long as the food was on the table. When the experimenter showed food at a height between the contralateral elbow and shoulder level within a reachable distance in front of him, however, he could not extend the contralateral arm and fingers, i. e. , his fist remained to stop in front of food (Figure 1A). It took him 4. 02 sec (SD = 2. 71 sec, n = 5) to retrieve food. After communicative pointing, however, he became able to grasp food in 1. 19 sec (SD = 0. 47 sec, n = 13) (Figure 1B). Gradually, his reaching-to-grasp became normal. Then, he was able to reach and grasp them when we showed various objects to him. Surprisingly, he made no attempt to obtain the objects just after the experimenter stroked his contralateral upper arm and flank. He tried to get a new object, but he could not reach and grasp with the contralateral hand because of his flexed elbow and his fist. After he pointed to distant food, it led to successful grasping. The next day, the same deficits of the contralateral arm and hand appeared. He became gradually able to grasp without difficulties after communicative pointing.
Figure 1 A grasping deficit in Subject A after the muscimol injection and recovery.
(A) When the experimenter presented food after the muscimol injection, Subject A reached for food but did not open his hand for about 2 s. Arrow indicates food location. (B) Time to retrieve the food before and after the pointing. Each symbol represents single trial. Horizontal bars indicate average time.
Figure 1 A grasping deficit in Subject A after the muscimol injection and recovery. (A) When the experimenter presented food after the muscimol injection, Subject A reached for food but did not open his hand for about 2 s. Arrow indicates food location. (B) Time to retrieve the food before and after the pointing. Each symbol represents single trial. Horizontal bars indicate average time.
Subject B used both hands equally for grasping before the ablation. Mouth movements were normal after the ablations. She refused the experimenter’s stroking around her back. She grasped a small piece of food in the partitioned box with her right hand, while holding with her left hand although she failed first several times. Both arm movements and grasping behavior apparentlyseemed to be normal. However, a marked deficit of grasping appeared when food was on the table. She grasped food with her left hand even though she heldfood in the same hand. Her left arm and fingers seemed to lose muscle tone, as if they were in mild atony. This symptom gradually progressed in the following two days. She showed obvious preference for using her righthand to grasp food. But the number of trials she used the left hand for grasping increased after the first training in pointing to a distant food (Figure 2A,B). Then, she began moving her arm and extending her fingers,as if the muscle tone recovered to the normal level (Figure 2C). She had difficulty in extending her left index finger as pointing to nearby food and instead used the right index finger at the beginning of the training (Figure 3). In the fourth training, the left index finger gradually began to protrude. In the fifth training, the subject pointed to the nearby food with her left index finger.
Figure 2 A grasping deficit in Subject B after the ablations and recovery.
(A)The number of trials Subject B used each hand to grasp the food. She preferentially used her right hand after the ablations. (B) Before communicative pointing, Subject B did not grasp food with her left hand even at 77 seconds after the food presentation. (C) After the training, she grasped food with her left hand at 11 seconds.
Figure 2 A grasping deficit in Subject B after the ablations and recovery. (A)The number of trials Subject B used each hand to grasp the food. She preferentially used her right hand after the ablations. (B) Before communicative pointing, Subject B did not grasp food with her left hand even at 77 seconds after the food presentation. (C) After the training, she grasped food with her left hand at 11 seconds.
A grasping deficit and communicative pointing to nearby food in Subject B after the ablations. Upper panel: in the early phase of the training, she pointed to a desired food with her fist when her left hand did not open. Lower panel: she became to use her left index finger during communicative pointing.
Figure 3 A grasping deficit and communicative pointing to nearby food in Subject B after the ablations. Upper panel: in the early phase of the training, she pointed to a desired food with her fist when her left hand did not open. Lower panel: she became to use her left index finger during communicative pointing.
After the experiments, we histologically examined the sites of ablations and muscimol injection, and confirmed that the damaged areas of both subjects were the PMv (Figure 4).
Brain areas for the inactivation and ablations. The shaded area in the left panel indicates the site of the muscimol injection. The shaded areas in the center and right panels indicate the ablation areas.
Figure 4 Brain areas for the inactivation and ablations. The shaded area in the left panel indicates the site of the muscimol injection. The shaded areas in the center and right panels indicate the ablation areas.
Our subjects refused the experimenter stroking, especially Subject A did not try to get food or objects after being stroked. Premotor cortex receives cortico-cortical afferents from visual and somatosensory association cortex [14,15]. Subject A grasped food on the table, while Subject B grasped food despite of holding it. Fogassi and colleagues found that the monkeys grasp objects under tactile control . Somatosensory inputs of Subject A’s hand also may be almost intact, while one of Subject B’s hands may be mostly blocked. The partial blocking of somatosensory inputs by our lesioning probably leads to the deficits of reaching and grasping. The symptom in our subjects is presumably due to the error of somatosensory inputs.
A striking finding of this study was that we found the clenched fist of subjects when they tried to grasp food. The PMv deals with the visual information of object in grasping . Ablations of caudal part in the PMv caused hemi-spatial neglect in the monkey . In Fogassi and colleagues’ study, after inactivation of the rostral part in the PMv, a monkey showed neglect of objects in the hemi-space contralateral to the inactivation site in the brain, as well as inability to shape the hand according to the visual characteristics of an object while performing grasping movements . Thus, this area processes visual and attention information in grasping. Our subject’s fist deficit of grasping was ameliorated by communicative pointing, i. e. , the fingers became to extend after the pointing. Accordingly, this deficit might result from visual or attention failures.
In summary, communicative pointing overcomes the reaching and grasping deficits induced by the inactivation or lesions of the PMv. Considering the dramatic recovery in our subjects, the motor control in communicative pointing probably compensates for higher motor dysfunctions. Therefore, communicative pointing is useful as rehabilitation treatment after the grasping and reaching deficits induced by PMv dysfunction. It remains to clarify whether pointing is derived from the grasping as in Vygotsky’s hypothesis and which brain areas contribute for the amelioration.
This work was supported to H. I. by Takeda Science Foundation and by a grant-in-aid and by Support of Young Researchers with a Term from the Ministry of Education, Culture, Sports, Science and Technology of Japan. Finally, we profoundly appreciate Dr. Donna McMillan’s support.
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Cite this article:
Kumashiro M, Yokoyama O,Ishibashi H (2013) Communicative Pointing Ameliorates Grasping Deficits after an Inactivation and Lesions of the Ventral Premotor Cortex in Japanese Monkeys (Macaca fuscata). J Neurol Disord Stroke 1(3): 1020.