- Email: [email protected]
The process of learning a tool-use movement in monkeys, with special reference to vision
Available online at www.sciencedirect.com
Neuroscience Research 60 (2008) 452–456 www.elsevier.com/locate/neures
Rapid communication
The process of learning a tool-use movement in monkeys, with special reference to vision Shigeto Sasaki a, Toshinori Hongo a, Kimisato Naitoh a, Naoki Hirai b,* b
a Department of Neurophysiology, Tokyo Metropolitan Institute for Neuroscience, Fucyu-shi, Tokyo, Japan Department of Integrative Physiology, Kyorin University School of Medicine, Shinkawa, Mitaka-shi, Tokyo 181-8611, Japan
Received 31 October 2007; accepted 28 December 2007 Available online 16 January 2008
Abstract Monkeys learned to use forceps to pick up food. The learning progressed in two stages. After having understood the task to have to use forceps through guidance, they (1) brought forceps toward food without seeing food until it was reached (1st stage), and (2) made forceps reach accurately to food using vision (2nd stage). We suggest that the learning without vision was a process of incorporating grasped-forceps into the body-scheme, thus enabling reaching with the extension (forceps) to a certain place in space. Using vision at the final stage was to precisely reach and to pick up food with the extension. # 2008 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. Keywords: Motor learning; Sensorimotor integration; Eye-hand coordination; Proprioception; Vision; Forceps; Monkey
Non-human primates as well as humans possess the ability to manipulate an object (tool) with their hand to act on other objects (e.g., Ducoing and Thierry, 2003; Iriki et al., 1996; Ishibashi et al., 2000; Ko¨hler, 1917). Acting with a tool on the target involves transforming representations of properties of target object (location, orientation, shape) and of those of the tool (position, dimensions, etc.) into a motor plan for goaldirected actions (Johnson-Frey, 2003). Although we humans have some difficulty in using an unfamiliar tool initially, we can solve the problem with practice on the basis of representations of previously acquired skills. In the present study, we analyzed the learning processes of forceps-use in monkeys. Because monkeys neither have used forceps nor have motor memories of tool-use applicable to forceps, this gives us an opportunity to trace elementary processes of motor learning that requires high degrees of sensorimotor integration. Two Japanese monkeys (Macaca fuscata, one female of 2 years old and one male of 3 years old) were used. Procedures were approved by the committees for animal experiments of the Tokyo Metropolitan Institute for Neuroscience and Kyorin University School of Medicine, and conformed to Guiding
* Corresponding author. E-mail address: [email protected] (N. Hirai).
Principles for the Care and Use of Animals in the Field of Physiological Sciences of the Physiological Society of Japan. Under ketamine hydrochloride (50 mg/kg) and sodium pentobarbital (35 mg/kg) anesthesia, each animal was prepared for the experiment by implanting a scleral search coil under the conjunctiva of one eye and a socket with a head coil on the skull to record gaze angle and head angle with the magnetic searchcoil system (Enzanshi-Kogyo Ltd., Japan), the two coils being in parallel to each other and at the same rostro-caudal and medio-lateral levels. The head position in space was recorded with Optotrack (Northen Digital Inc., Canada, sample rate of 100 Hz) by measuring positions of three infrared light emitting diodes (IREDS) aligned on a rod implanted on the skull midsagittally, with the rostralmost one placed at the level of eye coil. This provided coordinates in space for calibrations of the coil position. To prevent monkey’s hand from reaching the devices on the head, but not to the mouth, a barrier of translucent plastic plates was placed around-to-front of the neck obliquely (cf. Fig. 1F). The hand movement was recorded using Optotrack; IREDS were placed over the wrist and/or interpharyngeal joint. These data were stored in a hard disk of a personal computer for the later analysis. Monkeys were seated in a monkey chair. Their behavior was monitored with video recorders set at front, above, right and left sides of animals. Onset of hand movement and the moment of
0168-0102/$ – see front matter # 2008 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. doi:10.1016/j.neures.2007.12.014
S. Sasaki et al. / Neuroscience Research 60 (2008) 452–456
453
Fig. 1. Gaze and hand movements during food-taking action. (A) Traces of gaze and hand during food-taking with aid of experimenter. (1) While reaching, the monkey directed gaze towards food and extended fingers to food as shown in panel E. (2) When the monkey abided the guide, she brought forceps without gaze-shift toward food. The vertical line indicates the timing of contact of finger (1) or forceps (2) with food/plate, which was measured by pressure (bottom traces). Arrow in (2) points the downward gaze-shifts toward food after reach. (B) Same as in A, but bringing forceps toward food was made without the experimenter’s aid. (1) and (2) were recorded on the transient and learned phases (see text). Hollowed arrow in (2) indicates late hand movement toward mouth. (C) Traces of gaze and hand movements during ordinary food-taking action using hand. (D) Top view of layout of experimental workspace. (E) Front view of hand posture in a guided trial: monkey was reluctant to be guided and extended fingers to the food on seeing the food. (F) Photos exemplify the difference of gaze-hand coordination in reaching movements in the learning phase. (1) The monkey did not look down toward the food throughout reaching movement. (2) When the monkey looked down toward food during reaching, the monkey extended index finger and thumb to pick the food (arrow). (G) The monkey looked down toward the food during reaching movement at the learned phase, and brought the forceps toward food (arrow) correctly.
the forceps to contact with food (or its surroundings) were determined by measuring pressure on hand-rest and that on food/plate, respectively. The task was, with a beep (go signal), to bring hand-held forceps to a piece of food (ca. 5 mm cube of sweet potato or commercial solid food (CMK-2, Clea Japan, Inc.)) placed 15– 20 cm in their mid-front (Fig. 1D), and to pick it up with the forceps to eat. Food was presented 2–3 s before the beep in each trial, and monkeys were free to see food before the movements. The forceps were made with steel (9 cm in length with an aperture of 12–15 mm). They were given 100–250 trials a day. When food was presented on the plate in front of monkeys, they took it by hand while seeing it. Fig. 1C shows the traces of the vertical components of gaze-shift and hand movement during food-taking with hand, which were aligned at the contact of hand with food (vertical line). Hand movement and gazeshift to food started 269–488 ms (mean S.D.: 385 52.4 ms, N = 16) and 274–436 ms (358 46.8 ms), respectively, prior to
the contact of fingers with food. Onset times of hand movement and gaze-shift were correlated significantly (Fig. 2, blue circles; Y = 0.725X 74.2; r = 0.812, p < 0.01). When the experimenter handed the forceps to monkeys, they refused to take it or threw it away several times. Therefore, the experimenter held the monkeys’ hand and forced them to grasp forceps. Although holding it, they did not use it upon the food. Then the experimenter held the monkeys’ hand (Fig. 1D) and led them to bring the forceps to food, and to pick it up with the forceps, although monkeys were reluctant to be guided. When their hand was moved by force, they often looked toward food and extended their fingers for food (Fig. 1A1 and E). Within 2 experimental days, they abided the experimenter’s guide. Figure 1A2 shows the behavior of hand and gaze during such guided actions. A prominent feature of such actions was that reaching was not accompanied by gaze-shift toward food. Rather, they even seemed to avoid looking toward food while reaching. It was only after the forceps contacted with the food/
454
S. Sasaki et al. / Neuroscience Research 60 (2008) 452–456
Fig. 2. Relationship between onsets of hand movement (ordinate) and gazeshift (abscissa) relative to contact of the forceps or hand with the food/plate (positive in the abscissa indicates that the gaze-shift toward food occurred after the end of reach). The broken line represents the unity. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
plate that they directed their gaze toward food (arrow in Fig. 1A2). After such a guided act was repeated (for 5 days in one and 2 days in the other), they brought the forceps toward food almost by themselves (Fig. 1F) and the only assistance necessary was the experimenter’s slight pushing upon the forceps. In most of these trials, the gaze was away from food (Figs. 1F1 and 3A) while reaching, and shifted toward food only after the forceps contacted with food/plate, as in the guided trials (see Fig. 1A2). When, however, the gaze-shift to the food occurred early, though infrequent at this stage, it triggered an action of picking up food with the fingers (Fig. 1F2), as observed during guided trials (Fig. 1E). On day 6, the first monkey began to look down toward the workspace while reaching toward the food with the forceps. The frequency of early seeing the workspace was 16% of the trials, and was increased to 53 and 74% on days 7 and 8, respectively (the transient phase). Fig. 1B1 shows traces of hand movement and gaze-shift of latter half of trials on day 7. Forceps reached the food or plate in 330–1815 ms (668 301 ms, N = 90). Gaze was shifted toward food at variable time prior to or after contact of the forceps with the food/plate, with one exceptional trial with no gaze-shift. The onset of gaze-shifts ranged from 660 ms before contact to 1200 ms after contact (145 264 ms before contact, N = 89), and delayed 520 410 ms (N = 89) to the onset of hand movement. No temporal coordination was observed between gaze and hand, as shown by the scatter of symbol x in Fig. 2. From day 9, gaze shifted toward food before forceps-contact with the food/plate in all trials (the learned phase). Fig. 1B2 and G shows the relation between gaze and hand movement in the learned phase on day 11 where hand movement started 283– 627 ms (387 75 ms, N = 56) and gaze-shifts started 190– 618 ms (347 81 ms) prior to forceps’ contact with food/plate. Timing of hand movement and gaze-shift was correlated (red open circles in Fig. 2; Y = 0.744X 59.9, r = 0.69, p < 0.01).
The process of the learning was similar in the other monkey. The transient phase was from day 8 (early gaze-shift to food in 10% of trials) through day 11 (78%). Finally, gazeshift preceded forceps-contact with the food/plate in all trials on day 12. When they failed to pick up food in the first attempt, they tried again by making small reaches to the food. If, then, the first reach was made without or with vision, the second reach was also without or with vision, respectively (Fig. 3A or B). Progress in performance without the visual guide is exemplified in Fig. 3C1 and C2, where forceps placement in the first 20 trials on days 5 and 6 is schematically illustrated for the second monkey (transient phase on 8–11 days). Accuracy (bias from the center of food to the tip of the forceps in the yaxis) was significantly improved from 17.7 10.3 mm on day 5 to 11.6 7.6 mm on day 6 (t-test; p < 0.05). With further practice, reaching without vision became more accurate ( 4.8 5.2 mm; Fig. 3C3) on day 10 and progressed in performance up to picking food (also see below). The effect of vision is shown in Fig. 3D where the accuracy of reaching is compared between trials with and without using vision, both of which occurred on the same day of the transient phase. The accuracy was rated into three classes (top three panels of Fig. 3D: 0, food outside of the forceps; 1, one arm of the forceps on food; 2, food just in-between forceps). Food was just in between the forceps in 12 out of 15 reaches with gazeshift (red column) and, by contrast, in only 4 out of 18 trials without gaze-shift (gray column). Thus, occurrence frequency of the top rank trial was significantly higher under visual guidance (Fischer’s exact test, p < 0.01). The whole task is completed by picking food that follows reaching. Processes of transition from reaching to gripping and of manipulating the forceps to pick are two main aspects to be analyzed for elucidating the learning process of forceps-use, which are now being studied. Reaching is achieved by integration of many sensory and motor systems. Eye and hand movements are temporarily well coordinated during goal-directed reaching, and it is generally accepted that the gaze directs to the target earlier, so that a cue for precise guidance of the hand can be provided (e.g., Biguer et al., 1982). This was the case with our monkeys when they took food by hand, but not when they were learning to take food with forceps. The present study revealed that a novel movement of food-taking with forceps was acquired through a few steps of characteristic processes. Initially, monkeys either quickly took food with the hand after seeing it or suppressed the action by not seeing the food. In the next stage, they performed and learned the task movement (forceps-reaching) which, however, did not accompany gaze-shift to the target, and finally gaze-shift occurred with hand movement as in reaching with hand. An interesting finding in the present study was that monkeys did not take advantage of using vision at the early stages of learning. In the beginning, there was a tendency to keep their eyes away from the food, but made a quick action of taking food with fingers once they looked at it. For monkeys, seeing and then taking food with hand had been the ordinary and automatic action in their everyday life. When taking with hand was not
S. Sasaki et al. / Neuroscience Research 60 (2008) 452–456
455
Fig. 3. Relationship between gaze and hand movements during correction reaches (A and B), and accuracy of forceps placement (C and D). The vertical lines in A and B indicate the timing of downward movement of the hand. When the monkey failed to reach food in the first attempt, he tried again by making small reaches to the food. (A) The first reach was made without gaze-shift toward food (thick dashed line) and failed to pick food. After forceps-contact with floor, gaze was directed toward the food. When the monkey was lifting up forceps off the table to make a small correction reach, gaze remained still on the food, but just before he brought the forceps down to the food (vertical line), gaze was released from the food; gaze returned on the food after forceps touched down to the table. In this case, another correction was made following a similar procedure. (B) When the first reach was accompanied with gaze-shift on food (thick dashed line) and failed to take food, gaze remained on food throughout the correction reach. (C) Improvement of forceps placement by practice without visual guidance. Results of first 20 trials without vision of day 5 (1), day 6 (2), and day 10 (3) are schematically illustrated from top views as shown in D. The arrowhead represents the center of the tips of the forceps. Square in orange represents food. (D) Influence of vision on performance. Accuracy was rated into three grades: 0 (food outside of the forceps); 1 (one arm of the forceps on food); 2 (food just in-between forceps). Graph shows the score of 33 consecutive trials. Red or gray column indicates trial with or without gaze-shift accompanying hand movement. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
allowed, therefore, they seemed to have restrained themselves from doing so by not seeing food. After this period, when monkeys started learning the task, they still continued to avoid seeing food during reaching but this was for other reasons as discussed below. Based on the present findings, the process of motor learning may be considered, as followed. Monkeys could not exert the novel task movement (forceps-reaching) in the beginning, while repeated non-vision trials improved the movement progressively, until reaching out the hand-held forceps for the target became nearly accurate (Fig. 3C). This indicates that motor learning did occur with practice but monkeys did not use, or even avoided vision in the initial stage (Figs. 1F1 and 3C). We assume that the learning in this stage is a process of organizing many efferent and afferent movement-related signals to make-and-memorize a new motor program, where proprioceptive and various internal feedback (Oscarsson, 1973; Baldissera et al., 1981; Andersen et al., 1997) as well as knowledge of results play important roles (Kitazawa and Yin, 2002). The learning is concerned with the body movement itself, hence may be referred to as ‘learning of movement per se’. We postulate that the first step of learning a new movement is this ‘learning of movement per se’, and that on-line visual control can come after this step is achieved. The latter is
suggested by the finding that monkeys began to see food during the movement, just when forceps-reaching became almost accurate by non-vision learning. Next, concerning the role of vision in motor learning, an important question is why monkeys did not use vision during movement at the initial stage. One reason may be related to the nature of the reach movement that its main part is executed in one step following a program, either to an imagery (pre-seen) or to a real target, and does not necessarily need on-line visual information for control. Further, vision is possibly disadvantageous to the learning of reach-movement itself, as suggested by the reports showing that performance of target-reach produced by the practice under the vision is considerably degraded once vision is no longer available (Getz et al., 1995; Bernier et al., 2005). Our monkeys even avoided using vision actively, and it was remarkable that they did so even in short-distance reaching for correction (Fig. 3A). Presumably, there are some strong reasons for monkeys to have to avoid vision, such that vision disturbs monkey’s attention and concentration which may be paid to execution of the task, or they cannot accept and incorporate visual information into on-going CNS processes of producing movements. After the forceps-reaching is learned (program established), on the other hand, the
456
S. Sasaki et al. / Neuroscience Research 60 (2008) 452–456
movement can proceed automatically following the program, like in locomotion, and vision can come at any phase of the movement. Addition of visual information, at this stage, makes forceps-reach to food more accurate (Fig. 3D). We suggest that the learning of forceps-use at the initial stage without vision was a process of incorporating the grasped-forceps into the scheme of the body (cf. Maravita and Iriki, 2004), thus enabling reaching with the extension (forceps) to a certain place in space. Using vision at the final stage was to precisely reach and to pick up food with the extension. References Andersen, R.A., Snyder, L.H., Bradley, D.C., Xing, J., 1997. Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu. Rev. Neurosci. 20, 303–330. Baldissera, F., Hultborn, H., Illert, M., 1981. Integration in spinal neuronal systems. In: Brooks, V.B. (Ed.), Handbook of Physiology. Section 1, vol. II. Motor Control. American Physiological Society, Washington, D.C., pp. 509–595. Bernier, P.-M., Chua, R., Franks, I.M., 2005. Is proprioception calibrated during visually guided movements? Exp. Brain Res. 167, 292–296.
Biguer, B., Jeannerod, M., Prablanc, C., 1982. The coordination of eye, head, and arm movements during reaching at a single visual target. Exp. Brain Res. 46, 301–304. Ducoing, A.M., Thierry, B., 2005. Tool-use learning in Tonkean macaques (Macaca tonkeana). Anim. Cogn. 8, 103–113. Getz, C.J., Gordon, J., Ghilardi, M.F., 1995. Impairments of reaching movements in patients without proprioception. II. Effects of visual information on accuracy. J. Neurophysiol. 73, 361–372. Iriki, A., Tanaka, M., Iwamura, Y., 1996. Coding of modified body schema during tool use by macaque postcentral neurons. Neuroreport 7, 2325–2330. Ishibashi, H., Hihara, S., Iriki, A., 2000. Acquisition and development of monkey tool-use: behavioral and kinematic analyses. Can. J. Physiol. Pharmacol. 78, 958–966. Johnson-Frey, S.H., 2003. Cortical presentations of human tool use. In: Johnson-Frey, S.H. (Ed.), Taking Action. The MIT Press, Massachusetts, pp. 185–217. Kitazawa, S., Yin, P.-B., 2002. Prism adaptation with delayed visual error signals in the monkey. Exp. Brain Res. 144, 258–261. Ko¨hler, W., 1917. Intelligenzpru¨fungen an Menschenaffen. Springer, Berlin/Iwanami-Shoten, Tokyo, 1962, 328 pp. (translated into Japanese by Miya, K.). Maravita, A., Iriki, A., 2004. Tools for the body (schema). Trends Cogn. Sci. 8, 79–86. Oscarsson, O., 1973. Functional organization of spinocerebellar paths. In: Iggo, A. (Ed.), Handbook of Sensory Physiology, vol. II. Somatosensory System. Springer-Verlag, Berlin, pp. 339–380.
Neuroscience Research 60 (2008) 452–456 www.elsevier.com/locate/neures
Rapid communication
The process of learning a tool-use movement in monkeys, with special reference to vision Shigeto Sasaki a, Toshinori Hongo a, Kimisato Naitoh a, Naoki Hirai b,* b
a Department of Neurophysiology, Tokyo Metropolitan Institute for Neuroscience, Fucyu-shi, Tokyo, Japan Department of Integrative Physiology, Kyorin University School of Medicine, Shinkawa, Mitaka-shi, Tokyo 181-8611, Japan
Received 31 October 2007; accepted 28 December 2007 Available online 16 January 2008
Abstract Monkeys learned to use forceps to pick up food. The learning progressed in two stages. After having understood the task to have to use forceps through guidance, they (1) brought forceps toward food without seeing food until it was reached (1st stage), and (2) made forceps reach accurately to food using vision (2nd stage). We suggest that the learning without vision was a process of incorporating grasped-forceps into the body-scheme, thus enabling reaching with the extension (forceps) to a certain place in space. Using vision at the final stage was to precisely reach and to pick up food with the extension. # 2008 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. Keywords: Motor learning; Sensorimotor integration; Eye-hand coordination; Proprioception; Vision; Forceps; Monkey
Non-human primates as well as humans possess the ability to manipulate an object (tool) with their hand to act on other objects (e.g., Ducoing and Thierry, 2003; Iriki et al., 1996; Ishibashi et al., 2000; Ko¨hler, 1917). Acting with a tool on the target involves transforming representations of properties of target object (location, orientation, shape) and of those of the tool (position, dimensions, etc.) into a motor plan for goaldirected actions (Johnson-Frey, 2003). Although we humans have some difficulty in using an unfamiliar tool initially, we can solve the problem with practice on the basis of representations of previously acquired skills. In the present study, we analyzed the learning processes of forceps-use in monkeys. Because monkeys neither have used forceps nor have motor memories of tool-use applicable to forceps, this gives us an opportunity to trace elementary processes of motor learning that requires high degrees of sensorimotor integration. Two Japanese monkeys (Macaca fuscata, one female of 2 years old and one male of 3 years old) were used. Procedures were approved by the committees for animal experiments of the Tokyo Metropolitan Institute for Neuroscience and Kyorin University School of Medicine, and conformed to Guiding
* Corresponding author. E-mail address: [email protected] (N. Hirai).
Principles for the Care and Use of Animals in the Field of Physiological Sciences of the Physiological Society of Japan. Under ketamine hydrochloride (50 mg/kg) and sodium pentobarbital (35 mg/kg) anesthesia, each animal was prepared for the experiment by implanting a scleral search coil under the conjunctiva of one eye and a socket with a head coil on the skull to record gaze angle and head angle with the magnetic searchcoil system (Enzanshi-Kogyo Ltd., Japan), the two coils being in parallel to each other and at the same rostro-caudal and medio-lateral levels. The head position in space was recorded with Optotrack (Northen Digital Inc., Canada, sample rate of 100 Hz) by measuring positions of three infrared light emitting diodes (IREDS) aligned on a rod implanted on the skull midsagittally, with the rostralmost one placed at the level of eye coil. This provided coordinates in space for calibrations of the coil position. To prevent monkey’s hand from reaching the devices on the head, but not to the mouth, a barrier of translucent plastic plates was placed around-to-front of the neck obliquely (cf. Fig. 1F). The hand movement was recorded using Optotrack; IREDS were placed over the wrist and/or interpharyngeal joint. These data were stored in a hard disk of a personal computer for the later analysis. Monkeys were seated in a monkey chair. Their behavior was monitored with video recorders set at front, above, right and left sides of animals. Onset of hand movement and the moment of
0168-0102/$ – see front matter # 2008 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. doi:10.1016/j.neures.2007.12.014
S. Sasaki et al. / Neuroscience Research 60 (2008) 452–456
453
Fig. 1. Gaze and hand movements during food-taking action. (A) Traces of gaze and hand during food-taking with aid of experimenter. (1) While reaching, the monkey directed gaze towards food and extended fingers to food as shown in panel E. (2) When the monkey abided the guide, she brought forceps without gaze-shift toward food. The vertical line indicates the timing of contact of finger (1) or forceps (2) with food/plate, which was measured by pressure (bottom traces). Arrow in (2) points the downward gaze-shifts toward food after reach. (B) Same as in A, but bringing forceps toward food was made without the experimenter’s aid. (1) and (2) were recorded on the transient and learned phases (see text). Hollowed arrow in (2) indicates late hand movement toward mouth. (C) Traces of gaze and hand movements during ordinary food-taking action using hand. (D) Top view of layout of experimental workspace. (E) Front view of hand posture in a guided trial: monkey was reluctant to be guided and extended fingers to the food on seeing the food. (F) Photos exemplify the difference of gaze-hand coordination in reaching movements in the learning phase. (1) The monkey did not look down toward the food throughout reaching movement. (2) When the monkey looked down toward food during reaching, the monkey extended index finger and thumb to pick the food (arrow). (G) The monkey looked down toward the food during reaching movement at the learned phase, and brought the forceps toward food (arrow) correctly.
the forceps to contact with food (or its surroundings) were determined by measuring pressure on hand-rest and that on food/plate, respectively. The task was, with a beep (go signal), to bring hand-held forceps to a piece of food (ca. 5 mm cube of sweet potato or commercial solid food (CMK-2, Clea Japan, Inc.)) placed 15– 20 cm in their mid-front (Fig. 1D), and to pick it up with the forceps to eat. Food was presented 2–3 s before the beep in each trial, and monkeys were free to see food before the movements. The forceps were made with steel (9 cm in length with an aperture of 12–15 mm). They were given 100–250 trials a day. When food was presented on the plate in front of monkeys, they took it by hand while seeing it. Fig. 1C shows the traces of the vertical components of gaze-shift and hand movement during food-taking with hand, which were aligned at the contact of hand with food (vertical line). Hand movement and gazeshift to food started 269–488 ms (mean S.D.: 385 52.4 ms, N = 16) and 274–436 ms (358 46.8 ms), respectively, prior to
the contact of fingers with food. Onset times of hand movement and gaze-shift were correlated significantly (Fig. 2, blue circles; Y = 0.725X 74.2; r = 0.812, p < 0.01). When the experimenter handed the forceps to monkeys, they refused to take it or threw it away several times. Therefore, the experimenter held the monkeys’ hand and forced them to grasp forceps. Although holding it, they did not use it upon the food. Then the experimenter held the monkeys’ hand (Fig. 1D) and led them to bring the forceps to food, and to pick it up with the forceps, although monkeys were reluctant to be guided. When their hand was moved by force, they often looked toward food and extended their fingers for food (Fig. 1A1 and E). Within 2 experimental days, they abided the experimenter’s guide. Figure 1A2 shows the behavior of hand and gaze during such guided actions. A prominent feature of such actions was that reaching was not accompanied by gaze-shift toward food. Rather, they even seemed to avoid looking toward food while reaching. It was only after the forceps contacted with the food/
454
S. Sasaki et al. / Neuroscience Research 60 (2008) 452–456
Fig. 2. Relationship between onsets of hand movement (ordinate) and gazeshift (abscissa) relative to contact of the forceps or hand with the food/plate (positive in the abscissa indicates that the gaze-shift toward food occurred after the end of reach). The broken line represents the unity. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
plate that they directed their gaze toward food (arrow in Fig. 1A2). After such a guided act was repeated (for 5 days in one and 2 days in the other), they brought the forceps toward food almost by themselves (Fig. 1F) and the only assistance necessary was the experimenter’s slight pushing upon the forceps. In most of these trials, the gaze was away from food (Figs. 1F1 and 3A) while reaching, and shifted toward food only after the forceps contacted with food/plate, as in the guided trials (see Fig. 1A2). When, however, the gaze-shift to the food occurred early, though infrequent at this stage, it triggered an action of picking up food with the fingers (Fig. 1F2), as observed during guided trials (Fig. 1E). On day 6, the first monkey began to look down toward the workspace while reaching toward the food with the forceps. The frequency of early seeing the workspace was 16% of the trials, and was increased to 53 and 74% on days 7 and 8, respectively (the transient phase). Fig. 1B1 shows traces of hand movement and gaze-shift of latter half of trials on day 7. Forceps reached the food or plate in 330–1815 ms (668 301 ms, N = 90). Gaze was shifted toward food at variable time prior to or after contact of the forceps with the food/plate, with one exceptional trial with no gaze-shift. The onset of gaze-shifts ranged from 660 ms before contact to 1200 ms after contact (145 264 ms before contact, N = 89), and delayed 520 410 ms (N = 89) to the onset of hand movement. No temporal coordination was observed between gaze and hand, as shown by the scatter of symbol x in Fig. 2. From day 9, gaze shifted toward food before forceps-contact with the food/plate in all trials (the learned phase). Fig. 1B2 and G shows the relation between gaze and hand movement in the learned phase on day 11 where hand movement started 283– 627 ms (387 75 ms, N = 56) and gaze-shifts started 190– 618 ms (347 81 ms) prior to forceps’ contact with food/plate. Timing of hand movement and gaze-shift was correlated (red open circles in Fig. 2; Y = 0.744X 59.9, r = 0.69, p < 0.01).
The process of the learning was similar in the other monkey. The transient phase was from day 8 (early gaze-shift to food in 10% of trials) through day 11 (78%). Finally, gazeshift preceded forceps-contact with the food/plate in all trials on day 12. When they failed to pick up food in the first attempt, they tried again by making small reaches to the food. If, then, the first reach was made without or with vision, the second reach was also without or with vision, respectively (Fig. 3A or B). Progress in performance without the visual guide is exemplified in Fig. 3C1 and C2, where forceps placement in the first 20 trials on days 5 and 6 is schematically illustrated for the second monkey (transient phase on 8–11 days). Accuracy (bias from the center of food to the tip of the forceps in the yaxis) was significantly improved from 17.7 10.3 mm on day 5 to 11.6 7.6 mm on day 6 (t-test; p < 0.05). With further practice, reaching without vision became more accurate ( 4.8 5.2 mm; Fig. 3C3) on day 10 and progressed in performance up to picking food (also see below). The effect of vision is shown in Fig. 3D where the accuracy of reaching is compared between trials with and without using vision, both of which occurred on the same day of the transient phase. The accuracy was rated into three classes (top three panels of Fig. 3D: 0, food outside of the forceps; 1, one arm of the forceps on food; 2, food just in-between forceps). Food was just in between the forceps in 12 out of 15 reaches with gazeshift (red column) and, by contrast, in only 4 out of 18 trials without gaze-shift (gray column). Thus, occurrence frequency of the top rank trial was significantly higher under visual guidance (Fischer’s exact test, p < 0.01). The whole task is completed by picking food that follows reaching. Processes of transition from reaching to gripping and of manipulating the forceps to pick are two main aspects to be analyzed for elucidating the learning process of forceps-use, which are now being studied. Reaching is achieved by integration of many sensory and motor systems. Eye and hand movements are temporarily well coordinated during goal-directed reaching, and it is generally accepted that the gaze directs to the target earlier, so that a cue for precise guidance of the hand can be provided (e.g., Biguer et al., 1982). This was the case with our monkeys when they took food by hand, but not when they were learning to take food with forceps. The present study revealed that a novel movement of food-taking with forceps was acquired through a few steps of characteristic processes. Initially, monkeys either quickly took food with the hand after seeing it or suppressed the action by not seeing the food. In the next stage, they performed and learned the task movement (forceps-reaching) which, however, did not accompany gaze-shift to the target, and finally gaze-shift occurred with hand movement as in reaching with hand. An interesting finding in the present study was that monkeys did not take advantage of using vision at the early stages of learning. In the beginning, there was a tendency to keep their eyes away from the food, but made a quick action of taking food with fingers once they looked at it. For monkeys, seeing and then taking food with hand had been the ordinary and automatic action in their everyday life. When taking with hand was not
S. Sasaki et al. / Neuroscience Research 60 (2008) 452–456
455
Fig. 3. Relationship between gaze and hand movements during correction reaches (A and B), and accuracy of forceps placement (C and D). The vertical lines in A and B indicate the timing of downward movement of the hand. When the monkey failed to reach food in the first attempt, he tried again by making small reaches to the food. (A) The first reach was made without gaze-shift toward food (thick dashed line) and failed to pick food. After forceps-contact with floor, gaze was directed toward the food. When the monkey was lifting up forceps off the table to make a small correction reach, gaze remained still on the food, but just before he brought the forceps down to the food (vertical line), gaze was released from the food; gaze returned on the food after forceps touched down to the table. In this case, another correction was made following a similar procedure. (B) When the first reach was accompanied with gaze-shift on food (thick dashed line) and failed to take food, gaze remained on food throughout the correction reach. (C) Improvement of forceps placement by practice without visual guidance. Results of first 20 trials without vision of day 5 (1), day 6 (2), and day 10 (3) are schematically illustrated from top views as shown in D. The arrowhead represents the center of the tips of the forceps. Square in orange represents food. (D) Influence of vision on performance. Accuracy was rated into three grades: 0 (food outside of the forceps); 1 (one arm of the forceps on food); 2 (food just in-between forceps). Graph shows the score of 33 consecutive trials. Red or gray column indicates trial with or without gaze-shift accompanying hand movement. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of the article.)
allowed, therefore, they seemed to have restrained themselves from doing so by not seeing food. After this period, when monkeys started learning the task, they still continued to avoid seeing food during reaching but this was for other reasons as discussed below. Based on the present findings, the process of motor learning may be considered, as followed. Monkeys could not exert the novel task movement (forceps-reaching) in the beginning, while repeated non-vision trials improved the movement progressively, until reaching out the hand-held forceps for the target became nearly accurate (Fig. 3C). This indicates that motor learning did occur with practice but monkeys did not use, or even avoided vision in the initial stage (Figs. 1F1 and 3C). We assume that the learning in this stage is a process of organizing many efferent and afferent movement-related signals to make-and-memorize a new motor program, where proprioceptive and various internal feedback (Oscarsson, 1973; Baldissera et al., 1981; Andersen et al., 1997) as well as knowledge of results play important roles (Kitazawa and Yin, 2002). The learning is concerned with the body movement itself, hence may be referred to as ‘learning of movement per se’. We postulate that the first step of learning a new movement is this ‘learning of movement per se’, and that on-line visual control can come after this step is achieved. The latter is
suggested by the finding that monkeys began to see food during the movement, just when forceps-reaching became almost accurate by non-vision learning. Next, concerning the role of vision in motor learning, an important question is why monkeys did not use vision during movement at the initial stage. One reason may be related to the nature of the reach movement that its main part is executed in one step following a program, either to an imagery (pre-seen) or to a real target, and does not necessarily need on-line visual information for control. Further, vision is possibly disadvantageous to the learning of reach-movement itself, as suggested by the reports showing that performance of target-reach produced by the practice under the vision is considerably degraded once vision is no longer available (Getz et al., 1995; Bernier et al., 2005). Our monkeys even avoided using vision actively, and it was remarkable that they did so even in short-distance reaching for correction (Fig. 3A). Presumably, there are some strong reasons for monkeys to have to avoid vision, such that vision disturbs monkey’s attention and concentration which may be paid to execution of the task, or they cannot accept and incorporate visual information into on-going CNS processes of producing movements. After the forceps-reaching is learned (program established), on the other hand, the
456
S. Sasaki et al. / Neuroscience Research 60 (2008) 452–456
movement can proceed automatically following the program, like in locomotion, and vision can come at any phase of the movement. Addition of visual information, at this stage, makes forceps-reach to food more accurate (Fig. 3D). We suggest that the learning of forceps-use at the initial stage without vision was a process of incorporating the grasped-forceps into the scheme of the body (cf. Maravita and Iriki, 2004), thus enabling reaching with the extension (forceps) to a certain place in space. Using vision at the final stage was to precisely reach and to pick up food with the extension. References Andersen, R.A., Snyder, L.H., Bradley, D.C., Xing, J., 1997. Multimodal representation of space in the posterior parietal cortex and its use in planning movements. Annu. Rev. Neurosci. 20, 303–330. Baldissera, F., Hultborn, H., Illert, M., 1981. Integration in spinal neuronal systems. In: Brooks, V.B. (Ed.), Handbook of Physiology. Section 1, vol. II. Motor Control. American Physiological Society, Washington, D.C., pp. 509–595. Bernier, P.-M., Chua, R., Franks, I.M., 2005. Is proprioception calibrated during visually guided movements? Exp. Brain Res. 167, 292–296.
Biguer, B., Jeannerod, M., Prablanc, C., 1982. The coordination of eye, head, and arm movements during reaching at a single visual target. Exp. Brain Res. 46, 301–304. Ducoing, A.M., Thierry, B., 2005. Tool-use learning in Tonkean macaques (Macaca tonkeana). Anim. Cogn. 8, 103–113. Getz, C.J., Gordon, J., Ghilardi, M.F., 1995. Impairments of reaching movements in patients without proprioception. II. Effects of visual information on accuracy. J. Neurophysiol. 73, 361–372. Iriki, A., Tanaka, M., Iwamura, Y., 1996. Coding of modified body schema during tool use by macaque postcentral neurons. Neuroreport 7, 2325–2330. Ishibashi, H., Hihara, S., Iriki, A., 2000. Acquisition and development of monkey tool-use: behavioral and kinematic analyses. Can. J. Physiol. Pharmacol. 78, 958–966. Johnson-Frey, S.H., 2003. Cortical presentations of human tool use. In: Johnson-Frey, S.H. (Ed.), Taking Action. The MIT Press, Massachusetts, pp. 185–217. Kitazawa, S., Yin, P.-B., 2002. Prism adaptation with delayed visual error signals in the monkey. Exp. Brain Res. 144, 258–261. Ko¨hler, W., 1917. Intelligenzpru¨fungen an Menschenaffen. Springer, Berlin/Iwanami-Shoten, Tokyo, 1962, 328 pp. (translated into Japanese by Miya, K.). Maravita, A., Iriki, A., 2004. Tools for the body (schema). Trends Cogn. Sci. 8, 79–86. Oscarsson, O., 1973. Functional organization of spinocerebellar paths. In: Iggo, A. (Ed.), Handbook of Sensory Physiology, vol. II. Somatosensory System. Springer-Verlag, Berlin, pp. 339–380.