The Importance of Memory Traces of Motor Efferent Discharges for Learning Skilled Movements

Develop. Med. Child Neurol. 1914, 16, 620-628

The Importance of Memory Traces of Motor Efferent Discharges for Learning

Skilled Movements Bill Jones

Introduction There is some evidence that voluntary

movements serve to structure perceptual judgements of spatial position. For example. judgements of the position of a sound by spastic children may be disrupted bk failure of eye-movement control: movement of the eyes in the direction of the sound helps to stabilize auditory memory (Jones et al. 1974). Adequate techniques for teaching movement patterns to the cerebral palsied are essential, not only for motor control itself but also for the child’s perceptual abilities. The purpose of the present paper is to show that the model of motor-skill acquisition, which i s at present almost exclusively used as the basis of physiotherapy-and which I shall call the proprioceptive inflow theory-is inadequate for the purpose, and that the evidence favours an alternative ‘motor outflow theory’ of skilled performance.

Theories of Timing The simplest voluntary movement in-

volves the temporal co-ordination of at least two muscle groups coupled at a

joint. A complex skill necessarily involves the ability to integrate a pattern of movements in the correct temporal sequence, which, in turn, depends upon knowledge of the direction and extent of previous movements. Such an ability will be called ‘timing’. Typically smooth timing breaks down in cerebral palsy. Hand waving, for example, requires the alternate contraction and relaxation of flexors and extensors, but flexion and extension may overlap in the cerebral palsied child (Holt 1965).

Traditionally there have been two general accounts of timing. In the first, information from peripheral receptors is assumed to calibrate movement error. Since in many skills the performer does not look at the movement of his limbs, or cannot look because visual attention is taken up with other demands of the task (as in touch-typing), it is commonly argued that proprioceptive inputs from muscles, tendons and joints provide error calibration (for example see Gibbs 1954, Bahrick et 01. 1955, Annett 1971).

We can contrast the proprioceptive inflow account with the motor outflow

_ _ _ ~. -~ - ~-

Vistt~ng Assistant Professor, Department of Psychology, University of Waterloo, Waterloo. Ontario. frc,senr uddrcw. Department of Psychology, University of Queensland, St. Lucia 4067, Queensland,

Awtialia

620

BILL JONES

theory, which assumes in its various forms (van Holst 1954, Sperry 1960, Jones 1972a) that the central nervous system (CNS) has knowledge of the direction and extent of voluntary movement through monitoring its own efferent signals to the muscles and retaining some ‘efferent copy’ (van Holst 1954). Physiologically, such a mechanism could depend upon a cortical-to-cerebellar loop around which efferent impulses are shunted at the time of transmission to the muscles (Ruch 1965). It is worth noticing that some such mechanism is required by the proprioceptive theory, since, if the peripheral input is to calibrate error, it must be compared against some record of the intended movement.

In practical terms, if proprioceptive inputs are in themselves necessary and sufficient for motor control, then passive movements of the limbs might be thought as effective for learning as the patients’ own movements. If central monitoring of efference is necessary and perhaps sufficient, it would follow that only voluntary movement could effectively teach motor control, since only voluntary movement and reflex postural motor responses are based upon efferent outflow.

Some Physiotherapy Programmes Phelp‘s Muscle Re-education

In all probability many clinics throughout the world still follow the Phelp’s method (Crickmay 1966), which is based upon a detailed analysis of muscle function. Individual muscles are tested and classified as spastic, rigid, and so on. Treatment is intended to improve individual muscle function. A fairly obvious criticism of Phelp’s method is that muscles do not work in isolation. It probably makes little sense to describe individual muscles as ‘spastic’. The typical spastic movement involves a failure to co-ordinate muscle groups. There is no doubt that assessment of muscle function is a part of

, ,

62 1

the assessment of cerebral palsy and may be particularly important in early preven- tion of deformities (Holt 1965). However, emphasis on individual muscle function simply avoids the problem of how movements are patterned in sequence.

Proprioceptive Facilitation Techniques There are several methods explicitly de-

signed to augment supposed proprioceptive input. The Rood (1954) method makes use of brushing or stroking the skin sur- rounding the joints in an attempt to provide tactile-proprioceptive stimuli. The various techniques described by Kabat and Knott (1953) aim at developing normal movements in the cerebral-palsied child and they assume that proprioceptive stimuli maximally activate motor path- ways. Such stimuli, manually applied by the therapist, include passive stretch, resistance, and pressure. For example, if flexors and extensors are weak, both groups are given heavy resistance, particularly the weaker of the two.

The Bobath Technique In my view the Bobath technique

(Bobath and Bobath 1952, 1954; Bobath 1971, Bobath 1971), was a considerable conceptual advance on previous physio- therapies. They argue that all cases of cerebral palsy involve some failure of adequate inhibitory control, rather than seeing cerebral palsy as a problem of weak or paralyzed muscles. Since they concentrate on muscular co-ordination. the Bobaths almost inevitably emphasize control over a pattern of movements in a sequence rather than individual muscle contractions. There are three basic stages in their programme: (1) released postural reflexes are inhibited; (2) normal auto- matic righting and cquilibrium movements are taught; and (3) everyday movement skills such as feeding and dressing can be acquired.

DEVELOPMENTAL MEDICINE AND CHILD NEUROLOGY. 1974, 16

As is well known, the Bobath technique makes use of what are called ‘reflex-inhibiting postures’, in which abnormal postures are broken up and the patient is helped to adjust to normal postures. Fundamental to the treatment is the assumption that normal postures provide the cerebral-palsied child with normal proprioceptive sensa- tions for the first time: ‘The proprioceptive system serves to mediate at every moment the knowledge of our position in space, of the position of the parts of the body in relation to each other, and of the quality and range of movement. All our movements occur in response to sensory stimulation and they are guided by the constant current of information transmitted from the proprioceptors in the muscles and joints as well as from the eyes. Therefore, normal movements cannot be expected as long as muscle tone is abnormal, and with it the proprioceptive information which guides our movements (Bobath and Bobath 1954, p. 96).’ Since abnormal movements are explicitly tied to abnormal proprioceptive inflow rather than to abnormal patterns of efference, it follows that Bobath therdpy relies heavily on passive movement of the patient. Severe cases are not simply held within the reflex-inhibiting posture but are moved within the posture by the therapist.

These brief descriptions may suffice to show that widely-practised techniques of physiotherapy rely almost exclusively on the proprioceptive inflow model of voluntary control. I now wish to show that this model is not as well supported as we tend to :issume and that the alternative motor outflow theory of timing is more likely to be useful.

Evidence for the Two Theories of Timing I s Proprioception a Necessary Condition for Motor Control .?

If proprioceptive inputs were essential to

movement learning and control, the motor outflow account could not suffice. The work of Taub and his associates with monkeys has clearly shown that peripheral inflow from receptors in the limbs is not required for the performance of a complex pattern of movements (Taub and Berman 1968). Taub’s technique involves bilateral spinal deafferentation, mainly of the fore- limbs, and he has demonstrated that adult blindfolded monkeys so treated can re- acquire such complex skills as running up the wire mesh of a cage. Moreover, monkeys deafferented neonatally can acquire skilled movements (Taub e? al. 1972). The classical studies of Mott and Sherring- ton (1895) on the effects of unilateral deafferentation have been used to argue for the sensory control of voluntary movements (Twitchell 1954). Taub and Berman (1968) argue that the movements of one arm have an inhibitory effect on the movements of the other, an effect which is normally held in check by the ipsilateral segmental afferent inflow. Such a mechanism would be abolished by unilateral deafferentation, and co-ordinated movements of the deafferented limb rendered impossible.

Though proprioception is not a necessary condition for controlled movement, it is often taken for granted that proprioception is always involved in movement. For example, as a test of proprioception, Holt (1965) describes a situation in which the child reaches to a target without vision except for an initial sight of the target. In fact, proprioception may not be involved in guided reaching movements. The visual target initially determines the direction of movement. Movement to the target may be entirely ‘ballistic’ or monitored through central recording of efferent signals.

Limb Movements Proprioceptive inflow from the limbs

could conceivably come from the muscle

622

BILL JONES

spindles, the joint receptors, or the Golgi tendon organs. The tendon receptors fire in phase with the joints (Patton 1965) so that we must consider joint and muscle receptors. Since muscles change in length and joints change in angle, the one receptor must signal changes in length and the other changes in angle if the CNS is to have knowledge of the direction and extent of movement. The work of Boyd and Roberts (1953), confirmed many times (e.g. Skog- lund 1956, Burgess and Clarke 1969), has shown that rate of firing of the joint receptor following passive stretch is related to joint angle, whereas muscle- spindle firing is not related to changes in muscle length.

Yet although the joint receptor signals passive movement, joint receptor firing is not necessary for the perception of voluntary movements. Browne et al. (1954) showed that anaesthetizing the joint capsule abolished the ability to duplicate or even detect passive movements, without affecting the ability to duplicate voluntary movements. These workers, and Paillard and Brouchon (1968), have hypothesized, therefore, that muscle-spindle activity may be tied in with voluntary movement. I tested this hypothesis by comparing the duplication of two types of active movements, one purely voluntary and the other to a stop set by the experimenter, against the duplication of passive movements. The argument was that only the purely voluntary movement would allow efferent monitoring, because in the other two conditions the subject could not know in advance the end-point of the movement. He would have to maintain muscle tone in both active conditions, so that there should have been no difference in the behaviour of the muscle spindles. In fact, duplication of voluntary movement was significantly more accurate than either of the other two types of movement. I argued therefore that central monitoring of motor outflow rather

8 ,

623

than muscle spindle firing is a necessary condition for accurate retention of voluntary movement (Jones 1972~).

Boyd and Roberts (1953) assumed that the muscle spindles were a priori unlikely to specify direction and extent of passive movement since the CNS would have to integrate the firing of different groups at the same joint. This argument applies with equal force to voluntary movement. Muscle receptors are unlikely to provide precise error signals about the voluntary movement of a limb since their output reflects both intrafusal and extrafusal tension (see Brooks and Stoney 1971). The probability of the muscle spindles signal- ling displacement information is further weakened by the fact of so-called ‘iso- metric contractions’, i.e. contractions which take place without change in the length of the muscles involved. At very low rates of sinusoidal stretch, discharge by some spindle afferents is a linear function of muscle length (Matthews and Stein 1969), but while ‘. . . the results throw light on the internal working of the spindle . . . they are unlikely to be relevant to its normal functioning in the body’ (Matthews and Stein 1969, p. 741). Of course I am not implying that spindle receptors have no functional utility in voluntary movement. Matthews (1964), for example, argues that alpha and fusimotor neurons may operate so to maintain muscle spindle discharge at something like the same level throughout the course of a movement planned by the CNS. Any deviation from the central ‘programme’ could therefore be corrected reflexively. Such a mechanism could certainly be disrupted in, for example, ataxias of tabes dorsalis. However, the key point is that movement is centrally initiated. The CNS must have the ability to ‘pre-programme’ a set of motor commands.

To summarise, proprioceptive inflow from the limbs could conceivably arise from the joint or muscle receptors-or both


624

in combination. The evidence is that only the joints are involved in passive movement (Boyd and Roberts 1953) and that joint receptor activity is not required for accurate duplication of voluntary movements (Browne et al. 1954). The hypothesis that the muscle-spindle activity may be a necessary condition for the retention of voluntary movement has not been confirmed (Jones 1972a, 1974). Arguing by exclusion, therefore, central monitoring of efference is a necessary condition for timing voluntary movements of the limbs.

Eye Movements Proprioceptive data on eye movements

can only conceivably be signalled by muscle receptors. Brindley and Merton (1960) have shown that discharge from proprioceptors following passive stretch of the extraocular muscles in normal adult subjects does not allow the subject to perceive the movement of his eyes. Skaven- ski (1972) did report detection of passive- eye-movements by two highly practised subjects without visual or cutaneous cues when degree of movement was quite extreme, but it is doubtful whether this work is relevant to ordinary function and Skavenski himself put forward an outflow model of movement control (Skavenski e f a(. 1972; see also Martin et al. 1969).

Studies of eye-tracking also suggest that outflow rather than feed-back mechanisms are operating during voluntary movement of the eyes. Festinger and Canon (1965) have shown that a subject with head fixed can locate a moving spot of light more accurately using saccades than smooth- pursuit eye movements. In other words, he has more idea where he has sent his eyes than where they have been taken.

When the head is left free, Fleming et al. (1969) found that eye-tracking is always saccadic and that at the end of each saccade there is a return eye-movement, the speed of which exactly matches the forward

velocity of the head. Since this returns eye- movement is initiated in a period of around 10 milliseconds before the head begins to move, co-ordination of head and eye movements can be understood as a feed- forward system in which efferent signals to the cephalomotor system are used to monitor eye movements prior to whatever feed-back signals there may be. Steinbach and Held (1968) have shown that central monitoring of efferent signals to the limbs can provide anticipatory information for control of eye movements. They found eye- tracking of a target fixed to one of the fingers to be more accurate when the subject made voluntary movements of his arm than when the arm was passively moved by the experimenter.

Accuracy of Voluntary Movement There is surprisingly little evidence for

the widely-held belief that accuracy of movement control depends upon proprioception. In the first place, most studies which claim to manipulate inflow also manipulate outflow. I have pointed out (Jones 1973) that many experiments which have claimed to demonstrate the necessity of proprioceptive feed-back for movement control tell us nothing about the rale of proprioception per se, since the procedures used involved either visual or verbal feed- back and conceivably also outflow mechanisms.

Many psychologists have claimed that accuracy of lever positioning can be im- proved by increasing the tension or resistance to movement of the lever which is held to augment proprioceptive inflow (e.g. Bahrick et al. 1955, Burke and Gibbs 1965). However, such studies have gener- ally given verbal or visual knowledge of results in addition to varying lever tension. Stelmach (1968) forced subjects to rely entirely on tension discriminability and found no significant differences in accuracy of lever positioning when tensions of 0 lb,

BILL JONES

5 lbs, and 10 lbs were used, i.e. augmenting whatever proprioceptive input there may be has little effect on accuracy of movement control (see also Jones 1974).

Laszlo (1966) initially indicated that proprioceptive feed-back may be important in the normal human subject even in such a simple task as tapping. She eliminated all feed-back from the limb, using a nerve compression block, and found that tapping rates declined sharply. However, when subjects were given a series of practice trials under nerve compression conditions they recovered to very nearly pre-test performance (Laszlo 1966). The initial decline may perhaps be due to the ‘queer feelings’ sometimes induced by Laszlo’s technique.

The early experiments of Woodworth (1899) clearly show that inflow from the limbs does not of itself lead to increases in accuracy of positioning. Woodworth showed that voluntary movements to a target have two phases: (1) an initial movement entirely under ‘pre-test’ control ; and (2) corrective adjustments to the required degree of accuracy. Movements of short duration (400 milliseconds for the non-preferred limb) were guided by initial impulse alone and were not influenced by visual or proprioceptive feed-back. Accur- acy of movements of longer durations in- creased only when the subject has his eyes open. When he had his eyes shut, and was consequently dependent upon whatever inflow there may have been from the joints, performance did not improve. All of which suggests that the corrective adjustments were a matter of visuaZ detection of dis- crepancies between the hand and the target and that the proprioceptors are not involved in fine discrimination. The more recent work of Beggs et al. (1972) and Beggs and Howarth (1972) on aiming at a target has shown that a visual feed-back theory of movement control accurately pre- dicts performance in the dark. Accuracy of movement in the dark is unaffected by

movement speed, but is linearly related to distance.

Conclusions To summarize the arguments against the

proprioceptive theory of motor control : (1) proprioception is not a necessary condition for motor control (Taub and Berman 1968) ; (2) joint receptors, but not muscle receptors, mediate knowledge of passive movements (Boyd and Roberts 1953, Browne et al. 1954); (3) joint receptors are not necessary for the perception of voluntary movements (Browne et al. 1954); (4) 1 to 3 imply that central monitoring of efference is involved in the execution and retention of voluntary movements; (5) studies of eye-movement further sup- port the outflow model; (6) there is no evidence from studies of human skilled performance that a CNS- proprioceptor loop is essential for learning the direction and extent of voluntary movement.

It must be emphasized that criticising the proprioceptive feed-back theory does not imply that feed-back or knowledge of results through other modalities is not involved in at least the acquisition of skills. The early and classic work of Woodworth (1899) and the more recent studies of Beggs et al. (1972) and Beggs and Howarth (1972) emphasize the importance of visual feed-back in the acquisition of guided reaching movements. Block (1969) reports some success in training movement control in the cerebral palsied, using augmented visual and auditory feed-back.

At present we are experimenting with prismatic shifts of the visual field which visually exaggerate error of movement and largely force the child to rely upon voluntary movement to achieve adaptation. There is evidence from two studies of Held and his associates, though neither is well

625


controlled, that absence of opportunity to associate voluntary movement with visual feed-back degrades both visual abilities and movement control (Held and Hein 1963, Held and Bauer 1967). I have also emphasized the relationship between vision and voluntary movement by showing that voluntary but not passive movement ex- ploration of shape and extent facilitates visual recognition (Jones 19726).

It may be objected that a model of normal movement control has no relevance to abnormal conditions. I believe that this objection is mistaken. The aim of modern physiotherapy is to train the cerebral- palsied child to the level of normal movement control of which he is individually

capable. In any case, as I have suggested, many methods of physiotherapy at present in use are based upon one model of normal skilled performance. The Bobath’s argument that normal control cannot be built upon abnormal muscle tone is almost certainly correct, and a technique for inhibiting reflex release is clearly essential. The Bobaths have consistently emphasized that the reflex-inhibiting posture results in normal appearance, normal muscle-tone and the possibility of normal movement- control. If they are right, and if this stage of their technique is useful, a valid theory of timing would be essential the for development of further voluntary control.

SUMMARY The evidence is reviewed to show that proprioception may not be as important in the

acquisition of patterns of movement as is commonly believed. Instead, the central nervous system may control the temporal sequence of muscular contraction through monitoring its own efferent outflow. It is argued that many methods of physiotherapy currently employed to improve movement control may be ineffective because they are based upon the proprioceptive feedback theory of skilled performance. New methods of physiotherapy may need to be developed which concentrate on teaching a child to monitor his own voluntary movements through visual means.

RCSUME

1 ’upprentissage gestuel L’auteur montre que la proprioception ne semble pas avoir l’importance qu’on h i

accorde gknkralement dans l’acquisition des patterns de mouvement. En revanche, le systeme nerveux central peut contrder les stquences temporelles de contraction musculaire par la surveillance de ses propres influx efferents. De ce fait, de nombreuses mdthodes kinksithkrapiques couramment utiliskes pour amdliorer le contrale des mouvements peuvent stre inefficaces du fait qu’elles sont basees sur une theorie de feed-back proprioceptif des performances gestuelles. De nouvelles mkthodes de physiotherapie peuvent demander 2 Etre dkveloppees pour apprendre B l’enfant a contr8ler ses propres mouvements volontaires au travers du contr6le visuel.

Importance des traces riinisiques des dkcltarges motrices effirentes dans

ZUSAMMENFASSUNG Die Bedeutung der Buhtiutig motorisclier eferenter Entladungen beim Erlernen

gez ielt er Be) regungsniust er Es herden die Befunde zusammengetragen, die darauf hinweisen, daI3 die Proprioception

fur den Erwerb von Bewegungsmustern nicht so bedeutsem ist wie gemeinhin angenommen wird. Stattdessen kann das Zentralnervensystem die zeitliche Aufeinanderfolge von Muskel-

626

BILL JONES

kontraktionen kontrollieren durch die Steuerung der eigenen efferenten Entladungen. Es wird gezeigt, daB viele Methoden der Physiotherapie, die zur Verbesserung der Bewegungs- kontrolle angewandt werden, moglicherweise deshalb nicht wirksam sind, weil sie auf der Theorie des proprioceptiven Feed-back Mechanismus gelernter Bewegungsmuster beruhen. Es sollten neue Methoden der Physiotherapie entwickelt werden, die ein Kind lehren, seine willkiirlichen Bewegungen mit Hilfe visueller Wahrnehmungen zu steuern.

RESUMEN La importancia de la impresidn en la memoria de las descargas motoras eferentes para

el aprendizaje de movimientos habiles Se revisa la evidencia que muestra que lo propioceptivo puede no ser tan importante en la

adquisici6n de esquemas de movimiento como corrientemente se Cree. En vez de ello, el SNC puede controlar la secuencia temporal de la contracci6n muscular a base de monitorizar su propia salida eferente. Se arguye que muchos mCtodos de fisioterapia empleados corrientemente para majorar el control del movimiento pueden ser ineficaces por estar basados en la teoria del feedback propioceptivo de la ejecuci6n hibil. Puede ser necesario desarrollar nuevos mCtodos de fisioterapia que se concentren en enseiiar a1 nifio a monitorizar sus propios movimientos voluntarios a travts de medios visuales.

REFERENCES Annett, J. (1971) ‘Acquisition of skill.’ British Medical Bulletin, 27, 266. Bahrick, H. P., Fitts, W. F., Schneider, R. (1955) ‘Reproduction of simple movements as a function of

factors influencing proprioceptive feedback.’ Journal of Experimental Psychology, 49,445. Beggs, W. D. A., Howarth, C. I. (1972) ‘The movement of the hand towards a target.’ Quarterly Journal of

Experimental Psychology, 24,448. - Andrew, J. A., Baker, M. L., Dove, S. R., Farclough, I., Howarth, C. I. (1972) ‘The accuracy of non-

visual aiming.’ Quarterly Journal of Experimental Psychology, 24, 51 5. Block, J. D. (1969) ‘Operant conditioning with augmented feedback. New perspectives in motor rehabilita-

tion of the brain damaged.’ Invited address to the New York Society of Physical Medicine and Rehabili- tation.

Bobath, B. (1971) ‘Motor development, its effect on general development, and application to the treatment of cerebral palsy.’ Physiotherapy, 57, 526.

Bobath, K. (1971) ‘The normal postural reflex mechanism and its deterioration in children with cerebral palsy.’ Physiotherapy, 57, 515. - Bobath, B. (1952) ‘The treatment of cerebral palsy based on the analysis of the patient’s motor be-

haviour.’ British Juurnal of Physical Medicine, 15, 107. _ - (1954) ‘Treatment of cerebral palsy by the inhibition of abnormal reflex action.’ British Orthuptic Journal, 11, 88.

Boyd, I. A., Roberts, T. D. M. (1953) ‘Proprioceptive discharges from stretch-receptors in the knee joint of the cat.’ Journal of Physiology, 122, 38.

Brindley, G. S., Merton, P. A. (1960) ‘The absence of position sense in the human eye.’Journal OfPhysiolugy, 153, 127.

Brooks, V. B., Stoney, S. D. Jr. (1971) ‘Motor mechanisms: the role of the pyramidal system in motor control.’ Annual Review of Physiology, 33, 1065

Browne, K., Lee, J., Ring, P. A. (1954) ‘The sensation of passive movement at the metatarso-phalangeal joint of the great toe in man.’ Journal of Physiology, 126,448.

Burgess, P. R., Clark, F. J. (1969) ‘Characteristics of knee joint receptors in the cat.’ Journal ufPhysiulugy, 203, 317.

Burke, L., Gibbs, C. B. (1965) ‘A comparieon of free-moving and pressure levers in a positional control system.’ Ergunornics, 8, 23.

Crickmay, M. C. (1966) Speech Therapy and the Bobath Approach to CerebraZPalsy. Springfield, 111.: Charles C Thomas.

Festinger, L., Canon, L. K. (1965) ‘Information about spatial location based on knowledge about efference.’ Psychological Review, 72, 373.

Fleming, D. G., Vossius, G. W., Bowman, G., Johnson, E. L. (1969) ‘Adaptive properties of the eye- tracking system as revealed by moving-head and open-loop studies.’ Annals of the New York Academy of Sciences, 156, 825.

Gibbs, C. B. (1954) ‘The continuous regulation of skilled response by kinaesthetic feedback.’ British Journal of Psychology, 45,24.

Held, R., Hein, A. (1963) ‘Movement produced stimulation in the development of visually guided behavior. Journal of Comparative and Physiological Psychology, 56, 872.

E 627


--- Bauer, J. A. (1967) ’Visually guided reaching in infant monkeys after restricted rearing.’ Science, 155,

Hoist, E. van (1954) ‘Relations between the central nervous system and the peripheral organs.’ British

Holt, K. S. (1965) Assessment of Cerebral Palsy. London: Lloyd-Luke. Jones, B. (1972a) ‘Outflow and inflow in movement duplication.’ Perception and Psychophysics, 12, 95. -- (19726) ‘Facilitation of visual perception through voluntary movement in elementary school children.’

(1973) ‘Is there any proprioceptive feedback ’?’ Psychological Bulletin, 79, 386. (1’974) ‘The role of central monitoring of elTerence in short-term memory for movements.’ Journal of

718.

Journal of Animal Behaviour, 2, 89.

Journal of Experimental Child PsychoIug.v, 14,408.

E.rperimental Psychology, 102, 37.

of s i~na l detection techniaues.’ Journal of Child Pspcholom and Child Psychiatry (In the press). -- Thompson, M., Kabanoff, B. (1974) ‘Judgements in auditory space by spastic chjldren: the application

Kabat,-H., Knott, M. (1953) ‘Propriocepiive facilitation technique for treatment of paralysis.’ Physical Therapy Review, 33, 53.

Laszlo. J. 1. (1966) ‘The Derformance of a simple motor task with kinaesthetic sense loss.’ Quarterly Journal of Experimental Psychblogy, 19, 344.

Martin, L., Matin, E., Pearce, D. (1969). ‘Visual perception of direction when voluntary saccades occur. Relation of visual direction of a fixation target to a flash presented during the saccade.’ Perception and Psyclwphysics, 5, 65.

Matthews, P. B. C. (1964) ‘Muscle spindles and their motor control.’ Physiological Reviews, 44, 219. -- Stein, R. B. (1969) ’The sensitivity of muscle spindle afferents to small sinusoidal changes of length.’

Journal OfPhysiology, 200,723. Mott, F. W., Sherrington, C . S. (1895) ‘Experiments upon the influence of sensory nerves upon movement

and nutrition of the limbs.’ Proceedings of the Royal Society, 57, 481. Paitlard, J., Brouchon, M. (1968) ‘Active and passive movement in the calibration of position sense.’ In:

Freedman, S. J. (Ed.) The Neuropsychology of Spatially Orienfed Behavior. Homewood, 111. : Dorsey Press.

Patton, H. D. (1965) ‘Reflex regulation of movement and position.’ In Ruch, T. C., Patton, H. D. (Eds.) Physialogy and Biophysics. Philadelphia : W. B. Saunders.

Rood, M. (1954) ‘Neurophysiological reactions as a basis for physical therapy.’ Physical Therapy Review, 34, 444.

Ruch, T. C. (1965) ‘Basal ganglia and cerebellum.’ In Ruch, T. C., Patton, H. D. (Eds.) Physiology and Biophysics. Philadelphia: W. B. Saunders.

Skavenski, A. A. (1972) ‘ W o w as a source of extra-retinal eye position information.’ Visual Research, 12, 221.

- Haddad, G., Steiman, R. M. (1972) ‘The extra-retinal signal for the visual perception of direction.’ Perception and Psychophysics, 11,287.

Skoglund, S . (1956) ‘Anatomical and physiological studies of knee joint innervation in the cat.’ ActaPhysio- Iogica Scandinavia, 36, Suppl. 124, 1.

Sperry, R. W. (1960) ‘Neural basis of the spontaneous optokinetic response produced by visual neural inversion.’ Journal of Comparative and Physiological Psychology, 43,482.

Steinbach, M. J., Held, R. (1968) ‘Eye tracking of observer gmerated target movements.’ Science, 161, 187. Stelmach, G. E. (1968) ‘The accuracy of reproducing target positions under various tensions.’ Psychonomic

Taub, E., Berman, A. J. (1968) ‘Movement learning in the absence of sensory feedback.’ In Freeman, S. J.

- Perella, P. N., Barro, G. (1972) ‘Behavioral development in monkeys following bilateral forelimb de-

Twitchell, T. E. (1954) ‘Sensory factors in purposive movement.’ Journal of Neurophysiology, 17, 239. Woodworth, R. S. (1899) ’The accuracy of voluntary movement.’ Psychological Review, Monograph Supple-

Science, 13, 287.

(Ed.) The Neuropsychology of Spatially Oriented Behariour. Homewood, Ill. : Dorsey Press.

afferentation on the first day of life.’ Transactions of the American Neurological Association.

ments, 3, No. 3.

628

Documents

The Importance of Memory Traces of Motor Efferent Discharges for Learning Skilled Movements