Visuomotor coordination in locomotion Trevor Drew Universit~ de M o n t r e a l , Q u e b e c , C a n a d a This article reviews the recent literature concerning the role of visual information in the control of locomotion with an emphasis on the neurophysiological mechanisms that underlie visually triggered, voluntary, gait modifications. Data are presented to show how these gait modifications may be encoded by the motor cortex, and how they may interact with the basic locomotor rhythm. Current Opinion in Neurobiology 1991, 1:652-657
Introduction In recent years, major advances have been made in the understanding of the spinal and brainstem mechanisms that underlie the production of the basic rhythmicity of the locomotor pattem. The neural pathways underlying visuomotor coordination in the intact animal, which are necessary for anticipatory changes of locomotion, are only now beginning to be studied, however. The present review will consider recent experiments that have looked at the role of the motor cortex in mediating visually initiated gait modifications, and will discuss the way in which these gait modifications may be incorporated into the underlying locomotor rhythm. In keeping with the style of this publication, emphasis is placed on recent findings and the reader is directed towards reviews by Armstrong [1] and GriUner [2] for more information concerning the neuronal control of locomotion, and to Patla [3 °°] for the importance of visual information.
shorten or lengthen his stride to attain the required location. Trials were carried out in full light, in complete obscurity, or when a brief pulse of light (300 ms duration) was given in each step cycle. The results showed that the intermittent visual information supplied by the pulses of light was quite sufficient to always permit the subject to accurately attain the target. In a similar type of study, Assaiente et al. [5] have shown that stroboscopic or intermittent illumination provides sufficient visual information to subjects required to walk along unevenly spaced rungs of a horizontal ladder. These two experiments demonstrate that intermittent visual information is sufficient to allow a subject to judge distance and to modify step length in order to attain a target. They do not, unfortunately, address the important questions of how frequently, and when, subjects would normally sample the environment in similar situations, although experiments by Patla (A Patla, personal communication) suggest that visual information is sampled more frequently when the degree of difficulty of the task to be undertaken increases.
Visual control of locomotion The importance of vision in controlling locomotion is seE-evident. In the absence of visual information it is impossible for an animal to make the anticipatory modifications of the locomotor rhythm that are taken for granted in everyday life. If artificial aids are unavailable, crossing a street or stepping on or off a curb all become difficult or impossible without vision. That is not to say, however, that there is a need for continuous visual input. Experiments in recent years have demonstrated that intermittent sampling of the immediate environment is both adequate, and probably the normal method employed, for extracting the visual information necessary for goal-directed locomotion. For example, taurent and Thomson [4] have recently examined the effects of intermittent visual sampling on the ability of subjects to step onto a stationary target. In their experiments, the position of the target was changed on each trial so that the subject had to either
Single-unit recordings Whereas such behavioural approaches in human subjects are well advanced and are giving important information about the way in which relevant visual information is extracted, parallel studies in awake animals have only just begun to examine the neurophysiological bases for such visually triggered gait modifications. Indeed, despite the fact that many different cortical (and sub-cortical) areas are probably engaged in processing and transforming the visual information into an accurate and appropriate motor response, the only structure that has been subjected to detailed study at the present time is the primary motor cortex (area 4). The body of this review will therefore examine the role that this region has to play in producing voluntary gait modifications.
Abbreviations CPG--central pattern generator; EDC---extensorcligitomm comrnunis; PTN--pyramidal tract neurone.
652
(~ Current Biology Ltd ISSN 0959-4388
Visuomotor coordination in locomotion Drew 653 Electrophysiological experiments in behaving cats have unequivocally demonstrated that the performance of locomotor tasks requiring visuomotor coordination is associated with an increased discharge in motor cortical units over and above that seen during normal overground or treadmill locomotion. Armstrong and his collaborators [6°°], for example, have reported that 50% of their sample of neurones (n = 16) showed a change in their discharge frequency in a task in which cats were required to walk along a horizontally positioned ladder (therefore placing a constraint on stride length and foot placement) with most of these neurones (six out of eight) showing an increase in discharge frequency. Similar results have been reported by Beloozerova and Sirota [7] in a parallel study in which 81% (88 out of 108) of their larger sample of motor cortical neurones demonstrated a change in their discharge rate during locomotion on a ladder. A substantial increase in the discharge rate of 83% of these task-related neurones (77 out of 88) was shown, while the other 11 task-related neurones decreased their discharge rate. Whereas these two studies examined motor cortical discharge when the principal consideration was the accuracy of foot placement, other studies have looked at neuronal discharge patterns in cats that were required to change the trajectory of their limbs in order to step over obstacles in their path. Beloozerova and Sirota [7], for example, have reported that a substantial number of neurones (79%) also changed their discharge frequency during this activity. In other studies [8,9oo], similar large changes in the discharge frequency of identified pyramidal tract neurones (PTNs) have been reported when animals stepped over obstacles fixed to a moving belt. Further analyses of these results have shown that a total of 73 out of 91 PTNs (80%), recorded from the forelimb region of area 4, showed changes in discharge frequency during steps over obstacles. The discharge rate of 48 out of 91 of these neurones was at least 20% larger during such steps than those observed during ordinary treadmill locomotion (T Drew, unpublished data). In all of these situations the increase in discharge frequency was best related to the swing phase of the forelimb contralateral to the recording site. It is important to note that these changes in cell discharge do not reflect a simple tonic increase or decrease in the amplitude of the discharge of the output neurones, but rather seem to precisely code specific aspects of the step cycle. This is particularly evident when neuronal discharge is examined while cats step over obstacles of different sizes and shapes. This task requires the production of different patterns of muscle activity for each situation, and results in a dissociation of the activity of muscles which are close synergists during ordinary locomotion over a flat surface [8]. Examination of the temporal relationships between the cell discharge and that of each of the forelimb muscles recorded during locomotion (normally eight to ten) demonstrates that the discharge of many of the PTNs which increased their firing frequency during the steps over the obstacles, often co-
varies with the activity of a single muscle, or small group of synergistic muscles acting around a single joint. A large number of the cells that demonstrated an increase in discharge rate during a gait modification could be subdivided into two groups according to the time of their peak discharge (T Drew, unpublished data). The larger group (n = 22) discharged maximally during the initial and middle parts of the swing phase, while the other group (n = 12) showed a preferential increase in discharge just prior to foot contact. It is suggested that cells in the former group are involved in controlling the activity of muscles involved in lifting the limb above and over the obstacle, while the latter group appear to be more specifically involved in regulating wrist dorsitlexor muscle activity prior to foot contact. An example of a PTN belonging to the latter group of neurones is shown in Fig.1 where the temporal correlation between the cell discharge and the period of activity in the extensor digitorum communis (EDC) muscle is shown in the raster displays of Fig.ld. In this example, the PTN discharged infrequently during ordinary treadmill locomotion (control), even though the receptive field of the cell included the ventral surface of the paw (Fig.la). The cell discharged relatively weakly when the cat stepped over a small high obstacle, more strongly when it had to extend its stride to step over a wide obstacle, and most strongly when the foot had to be placed between two moving obstacles. As can be seen from the averaged traces of Fig.lc, these tasks did not require an increase in the amplitude of the EDC muscle activity, but rather a temporal resequencing of the relative time in the step cycle at which the muscle was active. As suggested by Armstrong [ 1 ], who reported a similar pattern of discharge in a sample of neurones recorded during ladder walking, such neurones may be specifically involved in preparing and stabilizing the foot prior to foot contact.
Microstimulation of the motor cortex during locomotion The results reviewed above strongly suggest that the motor cortex is involved in mediating visually initiated changes in gait, and that it exerts a quite precise control over specific aspects of the gait modification. The discharge of the PTNs must therefore be considered as a specific signal that descends to the spinal cord in order to effectuate the appropriate changes in muscle activity needed to modify limb trajectory for avoidance or for precise foot placement. It has to be emphasized, however, that these gait modifications must also be incorporated into the locomotor rhythm so that the animal may continue its forward progression with minimal disruption. As such, it is pertinent to ask how the descending signal from the motor cortex is integrated into the locomotor rhythm. Does the descending signal act within the constraints imposed by the oscillating spinal cord networks responsible for generating the basic locomotor
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Fig. 1. An example of a pyramidal tract neurone that increases its discharge when the cat makes visually triggered steps over different types of obstacles attached to a moving treadmill belt. (a) Shows the cutaneous receptive field of the neurone on the distal forelimb and ventral surface of the foot. (b} Shows antidromic activation of the neurone following stimulation of the medullary pyramidal tract (conduction velocity = 40 ms-1). (c) Shows an averaged activity of the cell discharge and the extensor digitorum communis (EDC) activity (c'ontralateral to recording site) when the cat steps over a wide obstacle (n = 13, thicker line). The data are shown together with the averaged activity from 44 control step cycles (thinner line) and are normalized to the duration of the average control step cycle. The average is synchronized with the onset of the cleidobrachialis muscle activity which corresponds approximately to the onset of swing. (d} (i) The figurines of the cat shown are representative tracings taken from video which give a true indication of the scale of the obstacles with respect to the cat. (ii) The post event histograms show the averaged cell activity in each condition. (iii) Raster displays of the cell activity aligned with the onset of activity in the EDC (contralateral to recording site). Note that in the steps over the obstacle, the activity is aligned with the second period of muscle activity (see Fig. lc). In each raster, the first series of vertical ticks indicate the onset of activity in the muscle, the second series indicate the cessation of muscle activity, and the third series indicate the onset of activity in the next step cycle. For further information see text.
rhythm, or does it override these networks and/or act independently of them? One approach that has helped to answer this question has involved the production of artificial descending volleys by microstimulation of the motor cortex, followed by an examination of how such volleys interact with the locomotor pattern. In the initial experiments of this type in the decerebrate cat, Orlovsky [10] showed that weak stimulation of the pyramidal tract in decerebrate cats activated either flexor or extensor muscles, depending on the time in the step cycle in which such a stimulation was applied, but did not change the time of onset and offset of muscle activity. Stronger stimulation, however, evoked
a phase advancement of the swing phase of locomotion by activatinga premature period of flexor muscle activity. These results have been confirmed in the intact animal by Armstrong and myself [ 11 ] by stimulating different regions of the motor cortex, and have recently been extended [9°°]. In these latter experiments, long trains of stimuli (200 ms trains of 0.2 ms pulses at 300 Hz, 25 pA) were systematically applied during different phases of the step cycle to sites in which task-related cell activity was recorded. The results extended those of previous experiments by showing a consistent and powerful resetting of the locomotor rhythm from certain areas of the motor cortex. Stimulation while the leg contralateral to the
Visuomotor coordination in locomotion Drew stimulation site was in the air prolonged the swing phase, whereas stimulation while the leg was on the ground curtailed stance and initiated a new phase of .swing. Shorter trains of stimuli from the same site gave phase-dependent effects which were integrated into the locomotor rhythm. In answer to the question posed above, it therefore seems that the descending signal is normally integrated into the locomotor rhythm, but may override it depending on the strength and/or the duration of the descending volley. With small volleys, it is likely that the descending signal is distributed through interneuronal networks that are influenced by, or may even form part of, the central pattern generator (CPG) for locomotion, in the same way that has recently been suggested for the effects evoked by stimulation of the medullary reticular formation [12-]. The fact that the resetting of the locomotor rhythm normally involves a curtailment of stance and a premature onset of swing, further suggests that the corticospinal system may have a privileged input into the flexor part of the network which, upon reaching a threshold level, curtails extension and resets flexion. At first sight these results may seem paradoxical in that some cells appear to encode parameters of muscle activity at a single joint, whereas stimulation at a single locus often evokes a coordinated response in muscles acting around several joints. Consideration of the physiology of the corticospinal tract, however, suggests that this is in fact quite a logical result of the organization of the system. First, other electrophysiological and anatomical studies have shown that there is a widespread branching of corticospinal axons at the spinal cord so that any de-
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scending volley will almost certainly facilitate a number of motor neurone pools, including those of muscles acting around different joints (see [13] for references). Second, the CPG should perhaps not be viewed as a single entity controlling muscle activity in the whole limb, but rather, as suggested by GriUner [14], as a collection of inter-related unit pattern generators, each of which principally regulates muscle activity around a single joint. In such a scenario a specific signal to muscles acting around a single joint, for example the wrist, would ensure the correct orientation of the paw for placement, while the axon collateralization and the connections between the unit pattern generators (amongst other factors) would ensure the correct coordination between the different joints. A conceptual model of this is shown in Fig. 2.
Processing of the visual i n p u t It seems clear that although the motor cortex is involved in the execution of the motor command, it also lies quite close to the final end-point of the processes involved in the visuomotor transformation. The neuronal discharges recorded from PTNs within area 4 appear, at least in most cases, to be strictly related to the motor task to be undertaken. In my own experimental paradigm, although the cat was able to see &e obstacle two or three cycles before stepping over it, the earliest changes in discharge in most PTNs were seen during the stance phase of the step cycle, prior to the step, whilst most of these cells only showed changes in their discharge frequency just
Fig.2. A schematic representation of the way in which different regions of the motor cortex may interact with the neuronal networks controlling the locomotor rhythm. As in the paper by Grillner [14], the central pattern generator is represented as a series of tightly coupled unit pattern generators, each of which projects to the motor neurone pools controlling a single joint. Areas of the cortex regulating elbow musculature, for example, would project most strongly to the elbow unit pattern generator, although they would also send collateral branches to other unit generators. Areas of cortex controlling the wrist musculature would send their main projection to the interneuronal networks controlling the wrist, etc. It is suggested that both areas would have connections to interneuronal networks which regulate the overall rhythmicity of the locomotor pattern (here represented by the symbol for an oscillator). Such an organization would permit control over muscle activity at individual joints while also ensuring that modifications were coordinated and integrated into the overall locomotor activity. E, extensor. F, flexor.
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Neuralcontrol prior to, or during the swing phase of the cycle over the obstacle (unpublished data). At the moment, information concerning the route and processes by which the visuomotor transformation is performed is not readily available. Data from experiments in primates suggest that the visual signal passes from primary visual cortical areas to parietal and temporal cortex, from where it passes progressively to premotor cortex and finally to the primary motor cortex (for recent reviews, see [15.,16-]). In the cat, where there may be direct pathways from area 7 to the motor cortex [17], it is possible that the route may be even more direct, and that the suprasylvian gyms may play an important role in the process of transforming the visual signal into a motor command. For example, Fabre and Buser [18] have shown that lesions of the anterior suprasylvian gyms (including parts of areas 5 and 7) disrupt the cat's ability to make a visually guided movement to a moving target, even though reaching movements to stationary targets are readily made. Slightly caudal to the area studied by Fabre and Buser, Rauschecker et al. [19] have described neurones which have binocular receptive fields, as well as both direction and velocity preferences. They have suggested that such cells may be important in processing visual information during locomotion. Their suggestion that this region may be functionally analogous to the primate medial temporal cortex would also be in accord with the suggestion of Duffy and Wurtz [20-] that this region is involved in analyzing optic flow patterns. These results suggest that the suprasytvian gyms may play an important role in processing the visual information received during locomotion. While these pathways are certainly the most direct, it must also be realized that other pathways, via routes including the superior colliculus, basal ganglia, and cerebellum also exist and probably function, at least partially, in a parallel rather than in a completely hierarchical fashion (for a review, see [16"]).
Final comments and conclusions It has to be emphasized that the present review has concentrated on results obtained from studies on the motor cortex for the simple reason that this is the only structure that has been specifically studied with respect to visually-controlled locomotor movements. It is unlikely, however, that these movements are under the sole control of the motor cortex. The recent results of Martin and Ghez [21 ], for example, serve to demonstrate the marked similarities in the properties of rubral and cortical pathways in controlling multi-articulate reaching movements. In addition, visuomotor control of locomotion requires not only fine control over the movement of a single limb, but also appropriate postural responses to maintain equilibrium and to redistribute the centre of mass of the animal. These latter functions are almost certainly subserved by brainstem pathways that have to be activated in concert with the cortical and rubral systems to provide a smooth coordinated gait adjustment.
Acknowledgements I would like to thank M Bourdeau, R Bouchoux, S Doucet and R St-Jacques for technical aid during the experiments described in this review, as well as G Filosi for the design of Fig. 2. The comments of CE Chapman, JF Kalaska and S Rossignol on earlier versions of this review are gratefully acknowledged. Supported by the Canadian MRC and the Fonds de Recherche en Sant/~ de Qu6bec (FRSQ).
References and recommended reading Papers of special interest, published within the annual peri(xt have been highlighted as: • of interest • , of outstanding interest
of
review,
1.
ARMSTRONGDM: Supraspinal Contributions to t h e Initiation and Control of L o c o m o t i o n in t h e Cat. Prog Neurobio11986, 26:273-361.
2.
GRII.I.NERS: Control of L o c o m o t i o n in Bipeds, T e t r a p o d s and Fish. In tiana~ook of Physiology.. Motor Control, edited by Brookhart JM, Mountcastle VB [book]. Bethesda: Am Physiol Soc 1981, vol 3, pp 1179-1236.
3. ..
PATIA A: Visual Control of H u m a n Locomotion. In AdaptabiliO, of H u m a n Gait.. Advances in Ps3,chologv, edited by Patla A [book]. Elsevier 1991, vol 78, pp 55-97. A thorough review of the importance of visual information in the control of human locomotion. The article discusses critically current opinions on the way in which visual information is sampled and how it is used to modify gait. 4.
LAURENTM, THOMSON JA: T h e Role of Visual Information
in Control of a Constrained Locomotor Task. J Mot Bebat, 1988, 20:17-37. 5.
A.':,SAIENTEC, MARCHANDAR, A~mLCRDB: Discrete Visual Samples May Control Locomotor Equilibrium and Foot Positioning in Man. J Mot Behat, 1989, 21:72-91.
6. ..
AMOS A, ARMSTRONGDM, MARPLE-HORVATDE: C h a n g e s in t h e Discharge Patterns of Motor Cortical N e u r o n s Associated with Volitional C h a n g e s in Stepping in the Cat. Neurosci Lett 1990, 109:107-112. Describes results obtained from recordings of motor cortical neurones in unanaesthetized cats during locomotion on a horizontal ladder. The paper shows that the discharge frequency, in 50% of these neurones changed during locomotion on a ladder, as compared to locomotion over a flat surface. Most of these task-related neurones showed an increase in their discharge frequency. 7.
BEbOOZEROVAIN, SIROTA MG: Role of Motor Cortex in Control of Locomotion. In Stance a n d Motion: Facts a n d Concepts, edited by Gurfinkel VS, Ioffe ME, Massion J, Roll JP [book]. New York: Plenum Press 1988, pp 163-176.
8.
DRI:~' T: Motor Cortical Cell Discharge During Voluntary Gait Modification. Brain Res 1988, 457:181-187.
9. •.
DREW T: T h e Role of the Motor Cortex in t h e Control of Gait Modification in the Cat. In Neurobiological Basis of H u m a n Locomotion, edited by Shimamura M, Grillner S, Edgerton VR [book]. Tokyo: Japan Scientific Societies Press 1991, pp 201-212. Reports on the results of recording from identified PTNs in the motor cortex of cats trained to walk over obstacles attached to a moving belt. This review also provides data about the effects of microstimulation in sites in which task-related neuronal activity was recorded, and shows that the motor cortex is capable of effecting changes in the locomotor pattern of the type that would be required during anticipatory gait modifications. 10.
ORLOVSKYGN: T h e Effect of Different Descending Systems o n Flexor and Extensor Activity During Locomotion. Brain Res 1972, 40:359-371.
Visuomotor coordination in locomotion Drew 11.
ARMSTRONGDM, DREW T: Forelimb Electromyographic Res p o n s e s to Motor Cortex Stimulation During Locomotion in t h e Cat. J Physiol 1985, 367:327-351.
12. •
DREW T: Functional Organization within t h e Medullary Reticular Formation of t h e Intact Unanaesthetized Cat. III. Microstimulation During Locomotion. J Neurophysiol 1991, 66:919-938. This article shows that the responses evoked during locomotion by medullary reticular formation stimulation in the intact animal are organized into a functionally meaningful pattern. It is suggested that these effects are mediated by intemeuronal networks that either form part of, or are influenced by, the spinal CPGs for locomotion. 13.
LEMONRN: T h e O u t p u t Map of the Primate Motor Cortex. Trend.~ Neurosci 1988, 11:501-505.
14.
GRIU.NERS: Possible Analogies in t h e Control o f Innate Motor Acts and t h e Production of Sound in Speech. In Speech Motor Control, Wenner. Gren Center International Symposium Serie& edited by Grillner S [book]. Oxford: Pergamon Press 1982, vol 36, pp 217-229.
GEORGOPOULOSAP: Higher Order Motor Control. Annu Ret, Neur~ci 1991, 14:361-377. This article gives a brief overview of the planning processes involved in making a visually guided movement. The emphasis is placed on determining which parameters of movement are controlled, and h o w the coordinate transformation from visual signal to motor act may be brought about. 15.
•
16. •
PAIILARDJ: Development of Eye-Hand Coordination Across the Life Span. In Growth, Motor Development and Pl~sical ActiviO~ Across the Life Span, edited by Bard C, Fleury M, Hay L [book]. Columbia: University of South Carolina Press 1990, pp 26--74.
Examines the recent literature concerning the control of reaching movements. The emphasis is placed on the way that different supraspinal structures may be implicated in transforming a visual signal into a motor act. 17.
BABB RR, WATERS RS, ASANUMAH: Corticocortical C o n n e c tions to the Motor Cortex from the Posterior Parietal Lobe (Areas 5a, 5b, 7) in t h e Cat D e m o n s t r a t e d by t h e Retrograde Axonal Transport of Horseradish Peroxidase. Exp Brain Res 1984, 54:476-484.
18.
FABREM, BUSER P: Effects of Suprasylvian Lesions on Visually Guided Performances in Cats. Exp Brain Res 1981, 41:81-88.
19.
RAUSCHECKER JP, YON GRUNAU MW, POUUN C: Centrifugal Organization of Direction Preferences in t h e Cat's Lateral Suprasylvian Visual Cortex and its Relation to Flow Field Processing. J Neurosci 1987, 7:943-958.
20. •
DUFFYCJ, WUR'FZ RH: Sensitivity of MST N e u r o n s to Optic Flow Stimuli. I. A C o n t i n u u m o f Response Selectivity to Large.Field Stimuli. J Neurophysiol 1991, 65:1329-1345. Presents recent results on the properties of neurones recorded from the medial superior temporal (MST) cortex of monkeys. The results show that the response properties of neurones within this region are compatible with a role for the MST in the analysis of optic flow fields of the type which might be generated during locomotion. 21.
MAR'nNJH, GttEZ C: Red Nucleus and Motor Cortex: Parallel Motor Systems for the Initiation and Control of Skilled Movement. Behat, Brain Res 1988, 28:217-223.
T Drew, D0partement de Physiologie, Facult0 de M&tecine, Universit~ de Momrhal, CP6128, Succ. A, Montr6al, Quebec, H3C 3J7, Canada.
657
Introduction In recent years, major advances have been made in the understanding of the spinal and brainstem mechanisms that underlie the production of the basic rhythmicity of the locomotor pattem. The neural pathways underlying visuomotor coordination in the intact animal, which are necessary for anticipatory changes of locomotion, are only now beginning to be studied, however. The present review will consider recent experiments that have looked at the role of the motor cortex in mediating visually initiated gait modifications, and will discuss the way in which these gait modifications may be incorporated into the underlying locomotor rhythm. In keeping with the style of this publication, emphasis is placed on recent findings and the reader is directed towards reviews by Armstrong [1] and GriUner [2] for more information concerning the neuronal control of locomotion, and to Patla [3 °°] for the importance of visual information.
shorten or lengthen his stride to attain the required location. Trials were carried out in full light, in complete obscurity, or when a brief pulse of light (300 ms duration) was given in each step cycle. The results showed that the intermittent visual information supplied by the pulses of light was quite sufficient to always permit the subject to accurately attain the target. In a similar type of study, Assaiente et al. [5] have shown that stroboscopic or intermittent illumination provides sufficient visual information to subjects required to walk along unevenly spaced rungs of a horizontal ladder. These two experiments demonstrate that intermittent visual information is sufficient to allow a subject to judge distance and to modify step length in order to attain a target. They do not, unfortunately, address the important questions of how frequently, and when, subjects would normally sample the environment in similar situations, although experiments by Patla (A Patla, personal communication) suggest that visual information is sampled more frequently when the degree of difficulty of the task to be undertaken increases.
Visual control of locomotion The importance of vision in controlling locomotion is seE-evident. In the absence of visual information it is impossible for an animal to make the anticipatory modifications of the locomotor rhythm that are taken for granted in everyday life. If artificial aids are unavailable, crossing a street or stepping on or off a curb all become difficult or impossible without vision. That is not to say, however, that there is a need for continuous visual input. Experiments in recent years have demonstrated that intermittent sampling of the immediate environment is both adequate, and probably the normal method employed, for extracting the visual information necessary for goal-directed locomotion. For example, taurent and Thomson [4] have recently examined the effects of intermittent visual sampling on the ability of subjects to step onto a stationary target. In their experiments, the position of the target was changed on each trial so that the subject had to either
Single-unit recordings Whereas such behavioural approaches in human subjects are well advanced and are giving important information about the way in which relevant visual information is extracted, parallel studies in awake animals have only just begun to examine the neurophysiological bases for such visually triggered gait modifications. Indeed, despite the fact that many different cortical (and sub-cortical) areas are probably engaged in processing and transforming the visual information into an accurate and appropriate motor response, the only structure that has been subjected to detailed study at the present time is the primary motor cortex (area 4). The body of this review will therefore examine the role that this region has to play in producing voluntary gait modifications.
Abbreviations CPG--central pattern generator; EDC---extensorcligitomm comrnunis; PTN--pyramidal tract neurone.
652
(~ Current Biology Ltd ISSN 0959-4388
Visuomotor coordination in locomotion Drew 653 Electrophysiological experiments in behaving cats have unequivocally demonstrated that the performance of locomotor tasks requiring visuomotor coordination is associated with an increased discharge in motor cortical units over and above that seen during normal overground or treadmill locomotion. Armstrong and his collaborators [6°°], for example, have reported that 50% of their sample of neurones (n = 16) showed a change in their discharge frequency in a task in which cats were required to walk along a horizontally positioned ladder (therefore placing a constraint on stride length and foot placement) with most of these neurones (six out of eight) showing an increase in discharge frequency. Similar results have been reported by Beloozerova and Sirota [7] in a parallel study in which 81% (88 out of 108) of their larger sample of motor cortical neurones demonstrated a change in their discharge rate during locomotion on a ladder. A substantial increase in the discharge rate of 83% of these task-related neurones (77 out of 88) was shown, while the other 11 task-related neurones decreased their discharge rate. Whereas these two studies examined motor cortical discharge when the principal consideration was the accuracy of foot placement, other studies have looked at neuronal discharge patterns in cats that were required to change the trajectory of their limbs in order to step over obstacles in their path. Beloozerova and Sirota [7], for example, have reported that a substantial number of neurones (79%) also changed their discharge frequency during this activity. In other studies [8,9oo], similar large changes in the discharge frequency of identified pyramidal tract neurones (PTNs) have been reported when animals stepped over obstacles fixed to a moving belt. Further analyses of these results have shown that a total of 73 out of 91 PTNs (80%), recorded from the forelimb region of area 4, showed changes in discharge frequency during steps over obstacles. The discharge rate of 48 out of 91 of these neurones was at least 20% larger during such steps than those observed during ordinary treadmill locomotion (T Drew, unpublished data). In all of these situations the increase in discharge frequency was best related to the swing phase of the forelimb contralateral to the recording site. It is important to note that these changes in cell discharge do not reflect a simple tonic increase or decrease in the amplitude of the discharge of the output neurones, but rather seem to precisely code specific aspects of the step cycle. This is particularly evident when neuronal discharge is examined while cats step over obstacles of different sizes and shapes. This task requires the production of different patterns of muscle activity for each situation, and results in a dissociation of the activity of muscles which are close synergists during ordinary locomotion over a flat surface [8]. Examination of the temporal relationships between the cell discharge and that of each of the forelimb muscles recorded during locomotion (normally eight to ten) demonstrates that the discharge of many of the PTNs which increased their firing frequency during the steps over the obstacles, often co-
varies with the activity of a single muscle, or small group of synergistic muscles acting around a single joint. A large number of the cells that demonstrated an increase in discharge rate during a gait modification could be subdivided into two groups according to the time of their peak discharge (T Drew, unpublished data). The larger group (n = 22) discharged maximally during the initial and middle parts of the swing phase, while the other group (n = 12) showed a preferential increase in discharge just prior to foot contact. It is suggested that cells in the former group are involved in controlling the activity of muscles involved in lifting the limb above and over the obstacle, while the latter group appear to be more specifically involved in regulating wrist dorsitlexor muscle activity prior to foot contact. An example of a PTN belonging to the latter group of neurones is shown in Fig.1 where the temporal correlation between the cell discharge and the period of activity in the extensor digitorum communis (EDC) muscle is shown in the raster displays of Fig.ld. In this example, the PTN discharged infrequently during ordinary treadmill locomotion (control), even though the receptive field of the cell included the ventral surface of the paw (Fig.la). The cell discharged relatively weakly when the cat stepped over a small high obstacle, more strongly when it had to extend its stride to step over a wide obstacle, and most strongly when the foot had to be placed between two moving obstacles. As can be seen from the averaged traces of Fig.lc, these tasks did not require an increase in the amplitude of the EDC muscle activity, but rather a temporal resequencing of the relative time in the step cycle at which the muscle was active. As suggested by Armstrong [ 1 ], who reported a similar pattern of discharge in a sample of neurones recorded during ladder walking, such neurones may be specifically involved in preparing and stabilizing the foot prior to foot contact.
Microstimulation of the motor cortex during locomotion The results reviewed above strongly suggest that the motor cortex is involved in mediating visually initiated changes in gait, and that it exerts a quite precise control over specific aspects of the gait modification. The discharge of the PTNs must therefore be considered as a specific signal that descends to the spinal cord in order to effectuate the appropriate changes in muscle activity needed to modify limb trajectory for avoidance or for precise foot placement. It has to be emphasized, however, that these gait modifications must also be incorporated into the locomotor rhythm so that the animal may continue its forward progression with minimal disruption. As such, it is pertinent to ask how the descending signal from the motor cortex is integrated into the locomotor rhythm. Does the descending signal act within the constraints imposed by the oscillating spinal cord networks responsible for generating the basic locomotor
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Fig. 1. An example of a pyramidal tract neurone that increases its discharge when the cat makes visually triggered steps over different types of obstacles attached to a moving treadmill belt. (a) Shows the cutaneous receptive field of the neurone on the distal forelimb and ventral surface of the foot. (b} Shows antidromic activation of the neurone following stimulation of the medullary pyramidal tract (conduction velocity = 40 ms-1). (c) Shows an averaged activity of the cell discharge and the extensor digitorum communis (EDC) activity (c'ontralateral to recording site) when the cat steps over a wide obstacle (n = 13, thicker line). The data are shown together with the averaged activity from 44 control step cycles (thinner line) and are normalized to the duration of the average control step cycle. The average is synchronized with the onset of the cleidobrachialis muscle activity which corresponds approximately to the onset of swing. (d} (i) The figurines of the cat shown are representative tracings taken from video which give a true indication of the scale of the obstacles with respect to the cat. (ii) The post event histograms show the averaged cell activity in each condition. (iii) Raster displays of the cell activity aligned with the onset of activity in the EDC (contralateral to recording site). Note that in the steps over the obstacle, the activity is aligned with the second period of muscle activity (see Fig. lc). In each raster, the first series of vertical ticks indicate the onset of activity in the muscle, the second series indicate the cessation of muscle activity, and the third series indicate the onset of activity in the next step cycle. For further information see text.
rhythm, or does it override these networks and/or act independently of them? One approach that has helped to answer this question has involved the production of artificial descending volleys by microstimulation of the motor cortex, followed by an examination of how such volleys interact with the locomotor pattern. In the initial experiments of this type in the decerebrate cat, Orlovsky [10] showed that weak stimulation of the pyramidal tract in decerebrate cats activated either flexor or extensor muscles, depending on the time in the step cycle in which such a stimulation was applied, but did not change the time of onset and offset of muscle activity. Stronger stimulation, however, evoked
a phase advancement of the swing phase of locomotion by activatinga premature period of flexor muscle activity. These results have been confirmed in the intact animal by Armstrong and myself [ 11 ] by stimulating different regions of the motor cortex, and have recently been extended [9°°]. In these latter experiments, long trains of stimuli (200 ms trains of 0.2 ms pulses at 300 Hz, 25 pA) were systematically applied during different phases of the step cycle to sites in which task-related cell activity was recorded. The results extended those of previous experiments by showing a consistent and powerful resetting of the locomotor rhythm from certain areas of the motor cortex. Stimulation while the leg contralateral to the
Visuomotor coordination in locomotion Drew stimulation site was in the air prolonged the swing phase, whereas stimulation while the leg was on the ground curtailed stance and initiated a new phase of .swing. Shorter trains of stimuli from the same site gave phase-dependent effects which were integrated into the locomotor rhythm. In answer to the question posed above, it therefore seems that the descending signal is normally integrated into the locomotor rhythm, but may override it depending on the strength and/or the duration of the descending volley. With small volleys, it is likely that the descending signal is distributed through interneuronal networks that are influenced by, or may even form part of, the central pattern generator (CPG) for locomotion, in the same way that has recently been suggested for the effects evoked by stimulation of the medullary reticular formation [12-]. The fact that the resetting of the locomotor rhythm normally involves a curtailment of stance and a premature onset of swing, further suggests that the corticospinal system may have a privileged input into the flexor part of the network which, upon reaching a threshold level, curtails extension and resets flexion. At first sight these results may seem paradoxical in that some cells appear to encode parameters of muscle activity at a single joint, whereas stimulation at a single locus often evokes a coordinated response in muscles acting around several joints. Consideration of the physiology of the corticospinal tract, however, suggests that this is in fact quite a logical result of the organization of the system. First, other electrophysiological and anatomical studies have shown that there is a widespread branching of corticospinal axons at the spinal cord so that any de-
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scending volley will almost certainly facilitate a number of motor neurone pools, including those of muscles acting around different joints (see [13] for references). Second, the CPG should perhaps not be viewed as a single entity controlling muscle activity in the whole limb, but rather, as suggested by GriUner [14], as a collection of inter-related unit pattern generators, each of which principally regulates muscle activity around a single joint. In such a scenario a specific signal to muscles acting around a single joint, for example the wrist, would ensure the correct orientation of the paw for placement, while the axon collateralization and the connections between the unit pattern generators (amongst other factors) would ensure the correct coordination between the different joints. A conceptual model of this is shown in Fig. 2.
Processing of the visual i n p u t It seems clear that although the motor cortex is involved in the execution of the motor command, it also lies quite close to the final end-point of the processes involved in the visuomotor transformation. The neuronal discharges recorded from PTNs within area 4 appear, at least in most cases, to be strictly related to the motor task to be undertaken. In my own experimental paradigm, although the cat was able to see &e obstacle two or three cycles before stepping over it, the earliest changes in discharge in most PTNs were seen during the stance phase of the step cycle, prior to the step, whilst most of these cells only showed changes in their discharge frequency just
Fig.2. A schematic representation of the way in which different regions of the motor cortex may interact with the neuronal networks controlling the locomotor rhythm. As in the paper by Grillner [14], the central pattern generator is represented as a series of tightly coupled unit pattern generators, each of which projects to the motor neurone pools controlling a single joint. Areas of the cortex regulating elbow musculature, for example, would project most strongly to the elbow unit pattern generator, although they would also send collateral branches to other unit generators. Areas of cortex controlling the wrist musculature would send their main projection to the interneuronal networks controlling the wrist, etc. It is suggested that both areas would have connections to interneuronal networks which regulate the overall rhythmicity of the locomotor pattern (here represented by the symbol for an oscillator). Such an organization would permit control over muscle activity at individual joints while also ensuring that modifications were coordinated and integrated into the overall locomotor activity. E, extensor. F, flexor.
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Neuralcontrol prior to, or during the swing phase of the cycle over the obstacle (unpublished data). At the moment, information concerning the route and processes by which the visuomotor transformation is performed is not readily available. Data from experiments in primates suggest that the visual signal passes from primary visual cortical areas to parietal and temporal cortex, from where it passes progressively to premotor cortex and finally to the primary motor cortex (for recent reviews, see [15.,16-]). In the cat, where there may be direct pathways from area 7 to the motor cortex [17], it is possible that the route may be even more direct, and that the suprasylvian gyms may play an important role in the process of transforming the visual signal into a motor command. For example, Fabre and Buser [18] have shown that lesions of the anterior suprasylvian gyms (including parts of areas 5 and 7) disrupt the cat's ability to make a visually guided movement to a moving target, even though reaching movements to stationary targets are readily made. Slightly caudal to the area studied by Fabre and Buser, Rauschecker et al. [19] have described neurones which have binocular receptive fields, as well as both direction and velocity preferences. They have suggested that such cells may be important in processing visual information during locomotion. Their suggestion that this region may be functionally analogous to the primate medial temporal cortex would also be in accord with the suggestion of Duffy and Wurtz [20-] that this region is involved in analyzing optic flow patterns. These results suggest that the suprasytvian gyms may play an important role in processing the visual information received during locomotion. While these pathways are certainly the most direct, it must also be realized that other pathways, via routes including the superior colliculus, basal ganglia, and cerebellum also exist and probably function, at least partially, in a parallel rather than in a completely hierarchical fashion (for a review, see [16"]).
Final comments and conclusions It has to be emphasized that the present review has concentrated on results obtained from studies on the motor cortex for the simple reason that this is the only structure that has been specifically studied with respect to visually-controlled locomotor movements. It is unlikely, however, that these movements are under the sole control of the motor cortex. The recent results of Martin and Ghez [21 ], for example, serve to demonstrate the marked similarities in the properties of rubral and cortical pathways in controlling multi-articulate reaching movements. In addition, visuomotor control of locomotion requires not only fine control over the movement of a single limb, but also appropriate postural responses to maintain equilibrium and to redistribute the centre of mass of the animal. These latter functions are almost certainly subserved by brainstem pathways that have to be activated in concert with the cortical and rubral systems to provide a smooth coordinated gait adjustment.
Acknowledgements I would like to thank M Bourdeau, R Bouchoux, S Doucet and R St-Jacques for technical aid during the experiments described in this review, as well as G Filosi for the design of Fig. 2. The comments of CE Chapman, JF Kalaska and S Rossignol on earlier versions of this review are gratefully acknowledged. Supported by the Canadian MRC and the Fonds de Recherche en Sant/~ de Qu6bec (FRSQ).
References and recommended reading Papers of special interest, published within the annual peri(xt have been highlighted as: • of interest • , of outstanding interest
of
review,
1.
ARMSTRONGDM: Supraspinal Contributions to t h e Initiation and Control of L o c o m o t i o n in t h e Cat. Prog Neurobio11986, 26:273-361.
2.
GRII.I.NERS: Control of L o c o m o t i o n in Bipeds, T e t r a p o d s and Fish. In tiana~ook of Physiology.. Motor Control, edited by Brookhart JM, Mountcastle VB [book]. Bethesda: Am Physiol Soc 1981, vol 3, pp 1179-1236.
3. ..
PATIA A: Visual Control of H u m a n Locomotion. In AdaptabiliO, of H u m a n Gait.. Advances in Ps3,chologv, edited by Patla A [book]. Elsevier 1991, vol 78, pp 55-97. A thorough review of the importance of visual information in the control of human locomotion. The article discusses critically current opinions on the way in which visual information is sampled and how it is used to modify gait. 4.
LAURENTM, THOMSON JA: T h e Role of Visual Information
in Control of a Constrained Locomotor Task. J Mot Bebat, 1988, 20:17-37. 5.
A.':,SAIENTEC, MARCHANDAR, A~mLCRDB: Discrete Visual Samples May Control Locomotor Equilibrium and Foot Positioning in Man. J Mot Behat, 1989, 21:72-91.
6. ..
AMOS A, ARMSTRONGDM, MARPLE-HORVATDE: C h a n g e s in t h e Discharge Patterns of Motor Cortical N e u r o n s Associated with Volitional C h a n g e s in Stepping in the Cat. Neurosci Lett 1990, 109:107-112. Describes results obtained from recordings of motor cortical neurones in unanaesthetized cats during locomotion on a horizontal ladder. The paper shows that the discharge frequency, in 50% of these neurones changed during locomotion on a ladder, as compared to locomotion over a flat surface. Most of these task-related neurones showed an increase in their discharge frequency. 7.
BEbOOZEROVAIN, SIROTA MG: Role of Motor Cortex in Control of Locomotion. In Stance a n d Motion: Facts a n d Concepts, edited by Gurfinkel VS, Ioffe ME, Massion J, Roll JP [book]. New York: Plenum Press 1988, pp 163-176.
8.
DRI:~' T: Motor Cortical Cell Discharge During Voluntary Gait Modification. Brain Res 1988, 457:181-187.
9. •.
DREW T: T h e Role of the Motor Cortex in t h e Control of Gait Modification in the Cat. In Neurobiological Basis of H u m a n Locomotion, edited by Shimamura M, Grillner S, Edgerton VR [book]. Tokyo: Japan Scientific Societies Press 1991, pp 201-212. Reports on the results of recording from identified PTNs in the motor cortex of cats trained to walk over obstacles attached to a moving belt. This review also provides data about the effects of microstimulation in sites in which task-related neuronal activity was recorded, and shows that the motor cortex is capable of effecting changes in the locomotor pattern of the type that would be required during anticipatory gait modifications. 10.
ORLOVSKYGN: T h e Effect of Different Descending Systems o n Flexor and Extensor Activity During Locomotion. Brain Res 1972, 40:359-371.
Visuomotor coordination in locomotion Drew 11.
ARMSTRONGDM, DREW T: Forelimb Electromyographic Res p o n s e s to Motor Cortex Stimulation During Locomotion in t h e Cat. J Physiol 1985, 367:327-351.
12. •
DREW T: Functional Organization within t h e Medullary Reticular Formation of t h e Intact Unanaesthetized Cat. III. Microstimulation During Locomotion. J Neurophysiol 1991, 66:919-938. This article shows that the responses evoked during locomotion by medullary reticular formation stimulation in the intact animal are organized into a functionally meaningful pattern. It is suggested that these effects are mediated by intemeuronal networks that either form part of, or are influenced by, the spinal CPGs for locomotion. 13.
LEMONRN: T h e O u t p u t Map of the Primate Motor Cortex. Trend.~ Neurosci 1988, 11:501-505.
14.
GRIU.NERS: Possible Analogies in t h e Control o f Innate Motor Acts and t h e Production of Sound in Speech. In Speech Motor Control, Wenner. Gren Center International Symposium Serie& edited by Grillner S [book]. Oxford: Pergamon Press 1982, vol 36, pp 217-229.
GEORGOPOULOSAP: Higher Order Motor Control. Annu Ret, Neur~ci 1991, 14:361-377. This article gives a brief overview of the planning processes involved in making a visually guided movement. The emphasis is placed on determining which parameters of movement are controlled, and h o w the coordinate transformation from visual signal to motor act may be brought about. 15.
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16. •
PAIILARDJ: Development of Eye-Hand Coordination Across the Life Span. In Growth, Motor Development and Pl~sical ActiviO~ Across the Life Span, edited by Bard C, Fleury M, Hay L [book]. Columbia: University of South Carolina Press 1990, pp 26--74.
Examines the recent literature concerning the control of reaching movements. The emphasis is placed on the way that different supraspinal structures may be implicated in transforming a visual signal into a motor act. 17.
BABB RR, WATERS RS, ASANUMAH: Corticocortical C o n n e c tions to the Motor Cortex from the Posterior Parietal Lobe (Areas 5a, 5b, 7) in t h e Cat D e m o n s t r a t e d by t h e Retrograde Axonal Transport of Horseradish Peroxidase. Exp Brain Res 1984, 54:476-484.
18.
FABREM, BUSER P: Effects of Suprasylvian Lesions on Visually Guided Performances in Cats. Exp Brain Res 1981, 41:81-88.
19.
RAUSCHECKER JP, YON GRUNAU MW, POUUN C: Centrifugal Organization of Direction Preferences in t h e Cat's Lateral Suprasylvian Visual Cortex and its Relation to Flow Field Processing. J Neurosci 1987, 7:943-958.
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DUFFYCJ, WUR'FZ RH: Sensitivity of MST N e u r o n s to Optic Flow Stimuli. I. A C o n t i n u u m o f Response Selectivity to Large.Field Stimuli. J Neurophysiol 1991, 65:1329-1345. Presents recent results on the properties of neurones recorded from the medial superior temporal (MST) cortex of monkeys. The results show that the response properties of neurones within this region are compatible with a role for the MST in the analysis of optic flow fields of the type which might be generated during locomotion. 21.
MAR'nNJH, GttEZ C: Red Nucleus and Motor Cortex: Parallel Motor Systems for the Initiation and Control of Skilled Movement. Behat, Brain Res 1988, 28:217-223.
T Drew, D0partement de Physiologie, Facult0 de M&tecine, Universit~ de Momrhal, CP6128, Succ. A, Montr6al, Quebec, H3C 3J7, Canada.
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