Relationship of Proximal and Distal Function in Motor Development

Transcription

1 Relationship of Proximal and Distal Function in Motor Development CAROL LORIA, MS This study questions the validity of the principle of a proximo-distal direction of motor development and the idea that distal skill emerges out of and is dependent upon proximal control. To determine the relationship between proximal and distal motor function, normal infants (9 girls, boys), -weeks of age, were recorded on videotape while reaching for a one-inch red cube contained in a specially designed form board. Their visually guided reaching (proximal) ability and prehensile (distal) skills were rated on nonstandardized scales. No significant linear relationship was found between proximal and distal motor behavior. The conclusion that distal development does not necessarily follow proximal motor development is offered. The possibility that two different motor-control systems governing proximal and distal function is considered. Reconsideration of the proximo-distal sequences currently used in treating motor-system dysfunction is recommended. Key Words: Child development, Motor skills. The treatment of motor system dysfunction is often guided by the principle that distal motor development depends on proximal motor development. This principle, based on early phylogenetic, embryologic, and ontogenetic observations, -5 was generated in the 9s and 9s in support of the argument that behavior is refined from the whole rather than built up from its parts. The data upon which the proximodistal principle was formulated, however, were controversial and often scant. 6 Furthermore, observations from phylogenetic and embryologic studies of lower phyla were used to suggest the probability of a proximo-distal progression in man; yet man's increased encephalization and greater skilled hand function makes the validity of comparison to lower phyla questionable. Despite the lack of research support, this principle has mandated a treatment sequence that has been employed in many therapeutic procedures. For example, Ayres charts treatment sequences to suggest a Ms. Loria was a graduate student, Sargent College of Allied Health Professions, Division of Physical Therapy at Boston University, when this study was conducted. She is currently Education Coordinator, Department of Physical Therapy, Kennedy Memorial Hospital for Children, Warren St, Brighton, MA 5. This study was supported by an Allied Health Professions Traineeship from the Public Health Service, Department of Health, Education, and Welfare. This article was submitted August, 978, and accepted August 7, 979. relative emphasis and order of progression of the treatment program for improving upper extremity function follow the proximo-distal progression: first, control of head and eye musculature, then control of trunk, shoulder girdle, arm, and so on. 7 The sequence culminates with emphasis on distal motor skill. Rood, according to Stockmeyer, uses proximo-distal sequences when facilitating responses of mobility, stability, and mobility superimposed upon stability, as well as when promoting skill acquisition. 8 Bobath proposes control of key points according to a proximo-distal direction. 9 Recently, the validity of the rationale and hence the treatment sequences themselves has been challenged as new evidence on the neurological substrata of movement emerges. Kuypers has advanced a concept of motor control that departs from the classical concepts of pyramidal and extrapyramidal systems. In their place, he postulates ) a medial system that exerts control over axial and proximal limb musculature and ) a lateral system chiefly responsible for distal limb movements. This theory of dual motor control mechanisms is based on anatomical evidence in the cat and monkey, and on functional evidence in monkeys with lesions selectively placed in descending motor pathways. Recent studies, which further confirm the concept of two kinds of motor control mediated by two distinct systems, have considered the motor control exerted by one-half of the brain over Volume 6 / Number, February 98 67

2 contralateral and ipsilateral extremities in monkeys that have had commissurotomies., Does Kuypers' concept of dual mechanisms of motor control apply to man? Evidence in split-brain humans (who have undergone surgical disconnection of the corpus callosum to prevent interhemispheric spread of seizure activity) points to the likelihood of such a duality. The possibility of a dual motor control system in man raises important questions about the proximo-distal principle. First, if there are indeed two motor control systems with different functions, do they develop independently? If so, does their development overlap in time or does one system (proximal) develop first? Is development of one system (distal) dependent upon the development of the other (proximal)? A literature search revealed only one study that examined this proximo-distal relationship. That study found a lack of significant relationship between the times of onset of goal-directed motility of the arms and the type of grasping, suggesting that the two functions develop differently with respect to time. The purpose of this study was to investigate the relationship between proximal and distal behavior, which should be demonstrable if the proximo-distal principle is correct. Failure to demonstrate this relationship could have far-reaching implications for reconsideration, and perhaps replacement, of the proximo-distal sequences currently employed in the treatment of motor impairment. The assumption in the study reported here was that the proximo-distal principle should predict a positive linear correlation between the rated quality of reaching and prehension in -week-old human infants. The second purpose was to examine the qualitative aspects of proximal and distal motor development by depicting the characteristics of visually guided reaching and the prehensile skill in these infants. METHOD The sample consisted of full-term infants (9 girls, boys) between the ages of 9 and days, recruited from personal acquaintances. All infants had normal gestational periods and health records. Pregnancy and delivery were satisfactory. All infants were white and came from similar socioeconomic backgrounds. Proximal-Function Assessment Scale For the purpose of this study, proximal function was tested by assessing visually guided reaching ability, because this movement involves a spatial aiming skill. To assess the infants' reaching ability, a proxi Visual Orientation Closes eyes Looks at hand Looks at object Form of Approach Circuitous Moderately circuitous Slightly circuitous Direct Number of Lateral Deviations or more or less Aim of Approach Pronated In some aspect of forearm rotation Forearm rotation definitely directed at cube Vertical Approach Slide Loop-slide Plane-slide Plane-loop Plane Accuracy of Approach Off-target; needs more than adjustment Off-target; needs only adjustment On target Coarse Tremor Moderate-severe Mild Absent Possible Points Subject's Total Score Infant Behavior ( ) Fig.. Proximal-Development Assessment Scale for scoring visually guided reaching in the -week-old infant. mal-development assessment scale was devised (Fig. ) that combines findings from the observational studies of Halverson, 5 the developmental norms of Gesell and Amatruda, 6 and the scale devised by Kopp. 7 This scale attempts to define the quality of reaching for a one-inch cube by a -week-old infant. Operational definitions for the seven criteria measured on the proximal-development assessment scale, adapted from the studies just mentioned, are as follows:. VISUAL ORIENTATION: Visual regard upon presentation of the cube. Closes eyes: infant closes eyes or looks away from the stimulus. Looks at hand: infant's initial response is to look at his hand. 68 PHYSICAL THERAPY

3 Looks at stimulus: infant's initial response is to look at the cube.. DIRECTION OF APPROACH: Aim of the hand along a horizontal plane. Circuitous: the hand, in advancing, moves laterally during the first part of the approach and medially during the latter part, thus describing an arc. Moderately circuitous: same as the circuitous approach except that a curvilinear figure rather than a full arc is described. Slightly circuitous: the forefinger fails to point definitely at the cube throughout the approach but swings out slightly laterally during the initial phase of the reach Aim of Thumb During Approach Down or out Down-in In At Final Thumb Angle Down or out Down-in In First Finger Position on Cube Fingers and thumb contact asynchronous Fingers and thumb contact synchronous Accuracy of Grasp Precarious grasp on cube; drops or aims and misses Precarious grasp on cube; does not drop Grasps top and side of cube and maintains accuracy Finger Spread on Cube Fingers are spread apart Fingers are not spread apart Type of Grasp Contact Hand Palm Superior-palm Inferior-forefinger Number of Contacts Prior to Securing Cube Does not secure or more Fine Tremor Moderate-severe Mild Absent Possible Points Infant Behavior ( ) Direct: the path of the forefinger approximates a straight line.. NUMBER OF LATERAL DEVIATONS: The number of changes in direction of the hand during the approach time.. AIM OF APPROACH: Aim of the forearm upon completion of the approach. Pronated: the forearm is pronated so that the hand is perfectly parallel to the horizontal plane and pointed directly at or above the cube. Some aspect of rotation: the hand is rotated slightly and oriented toward the cube. Forearm rotation definitely directed at the cube: the forearm is rotated around the sagittal axis more than degrees and oriented toward the cube. 5. VERTICAL APPROACH: Profile of the infant's route of approach when viewed laterally. Slide: the infant slides his hand along the tabletop. Loop-slide: a combination of the loop (the infant first raises his hand and then directs it toward the cube; at the end of the motion, the hand is pulled back instead of advancing forward) and the slide. Plane-slide: differs from loop-slide only in that in place of the loop, the infant uses a short planing movement (the infant raises and projects the hand forward simultaneously so that the hand just skims the top surface of the cube; at the end of the approach, the hand is still moving forward as it settles on the cube). Plane-loop: combination of the plane and the loop approaches. Plane: see definition under plane-slide. 6. ACCURACY OF APPROACH: Precision of approach measured when the infant's hand is within two inches of the recessed portion of the board. Adjustments: changes in the infant's hand direction when within two inches of the recess. 7. COARSE TREMOR: Involuntary muscle contractions in the arm manifested as rhythmical alternating movements. Moderate-severe: oscillates 8 to times per second. Mild: oscillates to 5 times per second. Distal-Function Assessment Scale Distal function was tested by evaluating prehensile skill in grasping and retrieving the one-inch cube, as this involves fine motor ability. The distal-development assessment scale (Fig. ) and the operationally 8. defined criteria (below) for assessing hand orientation and grasping and releasing abilities were based on the Subject's Total Score findings in studies cited for the proximal-development assessment scale. Fig.. Distal-Development Assessment Scale for scoring. AIM OF THUMB DURING APPROACH: Aim quality of grasping by the -week-old infant. of the thumb-forefinger angle. Volume 6 / Number, February 98 69

4 Down or out: angle faces vertically downward or outward away from the cube. Down-in: angle faces partly downward and partly inward toward the cube. In: angle faces inward toward the cube; the thumb consistently points toward the cube. At: angle subtends the area occupied by the cube.. FINAL THUMB ANGLE: The direction of the thumb at the moment of contact with the cube. Down or out: the thumb is pointing downward toward the board, with very little, if any, thumb opposition. Down-in: the thumb is pointing toward the cube. In: the thumb is pointing above and toward the cube.. FIRST FINGER POSITION ON CUBE: Timing of thumb and finger contact on the cube. Asynchronous contact: two or more fingers touch the cube and then the thumb is brought to the cube or the thumb touches the cube and then the fingers are brought to it. Synchronous contact: fingers and thumb simultaneously contact the cube.. ACCURACY OF GRASP: Precision of hand orientation and finger fractionation as measured in the ability to grasp the cube securely. Precarious grasp: an undue amount of finger or hand maneuvers to maintain the cube securely. Secure grasp: the infant maintains the cube securely when he is able to lift the cube out of the recess without dropping it or appearing to be about to drop it. 5. FINGER SPREAD: The spread of the digits after contact with the cube. Fingers are apart: distance between digits is greater than ¼ inch. Fingers are not apart: distance between digits is less than or equal to ¼ inch. 6. TYPE OF GRASP: Relative position of palm and digits to the cube. Contact: infant succeeds in touching but not securing the cube. Hand: infant brings the pronated hand down upon the cube and presses it firmly against the heel of the palm. All fingers appear to be of equal importance. The cube is in the middle of the palm. Palm: infant sets the pronated hand down on the cube and opposes the thumb and fingers to force the cube against the palm. The cube is off-center and toward the radial aspect of the palm. Superior-palm: infant sets only the radial side of the palm down on the cube; the thumb opposes the first two fingers to press the cube against the thumb and palm. Inferior-forefinger: similar to the superior-palm except the digits at the end of the approach point more medialward than downward and the cube is no longer pressed against the palm. 7. NUMBER OF CONTACTS BEFORE SECUR ING CUBE: Number of times the infant contacts the cube, measured from the initial contact until the child retrieves it out of the recessed area. 8. FINE TREMOR: Involuntary muscle contractions in the hand manifested as rhythmical alternating movements. Moderate-severe: oscillates 8 to times per second. Mild: oscillates to 5 times per second. Equipment The criteria for both scales assess the quality of movements demonstrated when the infant reaches for a red one-inch cube contained in the recessed area of the Kuypers-like form board. This board is a modification of the apparatus used to minimize tactile "cuing" and to distinguish proximal and distal function in split-brain monkeys attempting to retrieve food pellets. However, compared to the original model, the board used in this study was very simple, in accordance with the expected achievement for the age group under study. Specifically, the apparatus used was a yellow board measuring in. by 6 in. by in. (.8 cm.6 cm 5.8 cm), with one centered recess with a diameter of in. (7.6 cm) and a depth of in. (.5 cm). In addition, the board was stabilized on adjustable legs to allow for height adjustment for each subject. Assessment Procedure All infants were seen at home. They were seated on their mothers' laps and the Kuypers-like board was placed in front of them and adjusted to waist level. A videotape camera with a zoom lens was used to record the infants' behavior. All infants were examined when awake, cooperative, and anticipating. The infant was allowed a brief period to adapt to the situation and to the examiner, after which his attention was obtained by the mother's calling the child's name. The mother next placed the infant's hands on the near edge of the board and then deposited the one-inch cube into the recessed area of the board. This procedure was followed for four trials. Half of the subjects were videotaped with the camera facing directly in front of them for trials and and with the camera filming a lateral view during trials and. The other half of the subjects were videotaped from a lateral view on trials and and an anterior view for trials and. This counterbalancing was intended to compensate for the effects of fatigue and 7 PHYSICAL THERAPY

5 practice during the procedure. A two- to three-minute rest period was given after the first two trials and then the infant's attention was again obtained by the method described. For videotape analysis, the more successful of the two trials for each anterior view was scored. The same criterion was used in selecting the lateral view for scoring. Success was defined in terms of the infant's accomplishment in securing and retrieving the cube. The videotaped responses of three of the subjects were previewed by two unbiased raters (one physical therapist and one occupational therapist) to evaluate interrater reliability. The raters were in 96 percent agreement on the proximal-development assessment scale and in 88 percent agreement on the distal-development asssessment scale. RESULTS On both the proximal-development and distal-development scales, mean scores of boys were compared to mean scores of girls. A nondirectional t test revealed no statistically significant difference between the two groups on either scale (on both scales, t =., df =, NS). 8 Consequently, boys and girls were treated as one group for all subsequent analyses. To assess the relationship between proximal and distal function in the -week-old infant, the Pearson product-moment coefficient of correlation was used. Analysis of the data (Table) revealed no statistically significant correlation (r =.7) between visually guided reaching ability and prehensile skill (if df = on a one-tailed test, an r of.97 is required for p =.5). With the exception of two subjects, all subjects looked at the cube when it was first presented and throughout the majority of the test session. Most TABLE Individual Scores on Proximal and Distal Scales Subject Proximal Score ( = 7.58, s =.7) Distal Score ( =.75, s =.) infants used a slightly circuitous direction when approaching the cube and all subjects required two or less changes in direction to reach the cube. Some degree of forearm rotation was seen in nine infants upon initial entry of their hand into the recessed area. In their distal function, most infants maintained their thumbs in abduction with lack of opposition during the approach phase, although half of the infants did oppose the thumb to some extent upon initial contact with the cube. Seven subjects contacted the cube asynchronously with regard to fingers and thumb timing, whereas five infants did so synchronously. Half of the infants were able to grasp the cube securely, but the other half were not. The most common grasp, the superior-palm, was exhibited by eight younsters. These children set only the radial side of the palm down on the cube and used the thumb to oppose the first two fingers, which pressed the cube against the thumb and palm. Three infants did use the more advanced inferior-finger grasping pattern. Upon retrieving the cube, all infants brought it to their mouths and explored it orally. Manual tactual exploration was minimal. DISCUSSION The results of this study of -week-old human infants do not support the proximo-distal hypothesis of a relationship between reach and prehension. The lack of a statistically and clinically significant relationship between proximal and distal motor function suggests that proximal development is not a prerequisite for distal motor development. The theory that distal skill emerges out of and depends on proximal control is not confirmed by the findings of this study. Furthermore, these findings tend to support the theory of a dual motor control mechanism in the developing human infant. The existence of two motor systems operating during development that is, a proximal system controlling visually guided reaching ability and a distal system controlling prehensile skill is very possible in light of this data. Kuypers' model, which was formulated from animal experimentation, and applied to the human adult, now also appears to apply to the developing human infant. This study, in conjunction with the findings of research on animals and human adults cited above, raises legitimate doubts about the rationale behind proximo-distal treatment sequences. Clearly, the time has come to reexamine therapeutic approaches to motor impairment in light of the findings of these studies. Perhaps we should no longer look at the proximal and distal systems as one mechanism, but rather seek new means of evaluating each function Volume 6 / Number, February 98 7

6 separately. Treatment protocols should perhaps consider proximal and distal function individually with regard to goals and pace of progression. For example, in treating an individual with deficits in visually guided reaching and prehensile skills, a therapist would perhaps use facilitation techniques to enhance proximal and distal control simultaneously, adhering to the developmental sequence of each individual system rather than emphasizing proximal improvement as a necessary prerequisite for distal recovery. Obviously, at some point, therapy must work on the integration of these two functions. The dissociation of proximal and distal motor-control systems offers a possible explanation for several clinical observations. The adult with good recovery of hand function and little or no proximal recovery following a cerebral vascular accident has long been an enigma to the clinician. A similar pattern of return has been noted in the child recovering from diffuse head trauma and coma. The possibility of two motor control systems with different functions raises many further research concerns. For example, when and how do two systems become integrated? Can and do the systems ever operate independently? Also, can the systems be dissociated, as evidenced by damage to one, particularly with sparing of the more sophisticated and complex distal system? The behaviors noted in these -week-old infants confirm early developmental observations. For example, visual attention directed toward the stimulus object for long periods is a common behavior at this age, 5 as is the predominance of oral exploration. 6 In their proximal function, those infants who were comparatively advanced used economy of space and effort. With regard to distal function, a progressive differentiation of the thumb and index finger in grasp and a progressive use of the digits without involvement of the palm were observed in advanced, compared to less advanced, infants. Even the most advanced infants tended to abduct their thumbs during reach and did not use thumb rotation and opposition until the cube was contacted. Apparently, visual guidance is not sufficient in the -week-old to orient the thumb for grasp, and tactile input is required to call forth the thumb action. One would expect that, later in development, the sensory inputs become integrated and vision alone can program the thumb position. Acknowledgments. The author wishes to thank Jane Coryell, PhD, and Shirley Stockmeyer for their advice in the writing of this article. REFERENCES. Coghill GE: Early development of behavior in amblystoma and in man. Archives of Neurology and Psychiatry :989-9, 99. Irwin OC: Proximodistal differentiation of limbs in young organisms. Psychol Rev :67-77, 9. Castner BM: Development of fine prehension in infancy. Genet Psychol Monogr :5-9, 9. Gesell A: The Mental Growth of the Pre-school Child. New York, Macmillan Publishing Co, Inc, Halverson HM: Experimental study in prehension in infants by means of systematic cinema records. Genet Psychol Monogr :7-86, 9 6. McCraw M: Grasping in infants and the proximo-distal course of growth. Psychol Rev :-, 9 7. Ayres AJ: Ontogenetic principles in the development of arm and hand functions. Am J Occup Ther 8:95-99, Stockmeyer SA: An interpretation of the approach of Rood to the treatment of neuromuscular dysfunction. Am J Phys Med 6():9-956, Bobath B: Facilitation of normal postural reactions and movement in the treatment of cerebral palsy. Physiotherapy 5: 6-6, 96. Kuypers HGJM: Organization of the motor system. Int J Neurol :78-9, 96. Lawrence DG, Kuypers HGJM: Functional organization of the motor system in the monkey:. The effects of bilateral pyramidal lesions.. The effects of lesions of the descending brainstem pathways. Brain 9:-6, 968. Brinkman J, Kuypers HGJM: Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the splitbrain rhesus monkey. Brain 96:65-67, 97. Brinkman J, Kuypers HGJM: Motor control in split-brain monkeys. Brain 96:675-69, 97. Gazzaniga MS: The Bisected Brain. New York, Appleton- Century-Crofts, Touwen BCL: Neurological Development in Infancy. London, Spastics International Medical Publications, 976, pp Gesell A, Amatruda CS: Developmental Diagnosis: Normal and Abnormal Child Development. New York, Paul B. Hober Inc, 97, pp Kopp CB: Fine motor abilities in infants. Dev Med Child Neurol 6:69-66, McCall RB: Fundamental Statistics for Psychology. New York, Harcourt Brace Jovanovich, Inc, 975, pp 9, 5, - 7 PHYSICAL THERAPY