D. E. Marple-Horvat

Visually guided stepping under conditions of step cycle-related denial of visual information

We recently reported that subjects performing a task that requires visual guidance of each step onto irregularly placed “stepping stones” usually fixate the next target of footfall just before they lift the foot to be repositioned, i.e. towards the end of that limbs stance phase. When negotiating the same walkway without ambient lighting, and with each stones location indicated by a central light spot (LED), stepping and eye movements were unchanged. Under conditions of intermittent visual denial, in which all LEDs (the only visual cues) were temporarily extinguished at irregular intervals, temporal changes in the normal stepping pattern were sometimes observed, but stepping was not always affected. The primary effect of visual denial was on the leg that was in stance (foot in place on a stepping stone) at the moment of LED extinction, rather than on the leg that was in swing, and was an increase in stance duration, suggesting an effect on planning during this stance of the next swing towards the next target rather than on execution of the ongoing swing of the other leg. Subjects rarely failed to step onto the targets. Prolongations of stance under visual denial lasting 400 or 500 ms were less than 200 ms, much less than the duration of denial; subjects did not simply wait for the footfall target to reappear. There was no effect for denial lasting 300 ms; subjects performed as well as with a constantly visible target. Under 400 and 500 ms denial, there was no effect when the targets disappeared in the first 100 ms of stance (of the foot to be repositioned); stance durations were indistinguishable from control. This suggests that there is no crucial visuomotor processing by the control system(s) for eye and limb guidance until the target reappeared near the usual end of stance, when feedforward planning of the next saccade and/or swing to a target reaches a crucial stage, and is affected by intrusion of the period of visual denial. With longer (800 ms) denial there was an effect regardless of when in stance it began. A smaller effect of 800 ms denial sometimes visible in swing duration is attributable to interlimb coordination. Accurate saccades, followed by accurate steps, to the next target are almost always made, even when the target is invisible. Our results demonstrate that uninterrupted on-line visual information is not necessary for accurate stepping even when (as here) each step requires visual guidance. Also, since stance prolongations did not always result, and they were always much shorter than the periods of denial, we conclude that the visuomotor control mechanism(s) are robust in the face of substantial denial of all visual information including normally preferred inputs (foveal or peripheral images) at the normally preferred times. The fact that a saccade is still made to an invisible target location implies that this is useful in itself, since it does not result in a visible foveal image. We propose that skilled, visually guided stepping onto irregularly placed targets is executed under predominantly feedforward visuomotor control mechanisms, and suggest that the ability to function effectively in this way is dependent upon the integrity of the lateral cerebellum.

An internal model of a moving visual target in the lateral cerebellum

In order to overcome the relatively long delay in processing visual feedback information when pursuing a moving visual target, it is necessary to predict the future trajectory of the target if it is to be tracked with accuracy. Predictive behaviour can be achieved through internal models, and the cerebellum has been implicated as a site for their operation. Purkinje cells in the lateral cerebellum (D zones) respond to visual inputs during visually guided tracking and it has been proposed that their neural activity reflects the operation of an internal model of target motion. Here we provide direct evidence for the existence of such a model in the cerebellum by demonstrating an internal model of a moving external target. Single unit recordings of Purkinje cells in lateral cerebellum (D2 zone) were made in cats trained to perform a predictable visually guided reaching task. For all Purkinje cells that showed tonic simple spike activity during target movement, this tonic activity was maintained during the transient disappearance of the target. Since simple spike activity could not be correlated to eye or limb movements, and the target was familiar and moved in a predictable fashion, we conclude that the Purkinje cell activity reflects the operation of an internal model based on memory of its previous motion. Such a model of the targets motion, reflected in the maintained modulation during the targets absence, could be used in a predictive capacity in the interception of a moving object.

Mechanisms of synchronous activity in cerebellar Purkinje cells

Complex spike synchrony is thought to be a key feature of how inferior olive climbing fibre afferents make their vital contribution to cerebellar function. However, little is known about whether the other major cerebellar input, the mossy fibres (which generate simple spikes within Purkinje cells, PCs), exhibit a similar synchrony in impulse timing. We have used a multi‐microelectrode system to record simultaneously from two or more PCs in the posterior lobe of the ketamine/xylazine‐anaesthetized rat to examine the relationship between complex spike and simple spike synchrony in PC pairs located mainly in the A2 and C1 zones in crus II and the paramedian lobule. PC pairs displaying correlations in the occurrence of their complex spikes (coupled PCs) were usually located in the same zone and were also more likely to exhibit correlations in the timing of their spontaneous simple spikes and associated pauses in activity. In coupled PCs, synchrony in both complex spike and simple spike activity was enhanced and the relative timing in the occurrence of complex spikes could be altered by peripheral stimulation. We conclude that the functional coupling between PC pairs in their complex spike and simple spike activity can be significantly modified by sensory inputs, and that mechanisms besides electrotonic coupling are involved in generating PC synchrony. Synchronous activity in multiple PCs converging onto the same cerebellar nuclear cells is likely to have a significant impact on cerebellar output that could form important timing signals to orchestrate coordinated movements.

The role of effort in moderating the anxiety – performance relationship: Testing the prediction of processing efficiency theory in simulated rally driving

Abstract We tested some of the key predictions of processing efficiency theory using a simulated rally driving task. Two groups of participants were classified as either dispositionally high or low anxious based on trait anxiety scores and trained on a simulated driving task. Participants then raced individually on two similar courses under counterbalanced experimental conditions designed to manipulate the level of anxiety experienced. The effort exerted on the driving tasks was assessed though self-report (RSME), psychophysiological measures (pupil dilation) and visual gaze data. Efficiency was measured in terms of efficiency of visual processing (search rate) and driving control (variability of wheel and accelerator pedal) indices. Driving performance was measured as the time taken to complete the course. As predicted, increased anxiety had a negative effect on processing efficiency as indexed by the self-report, pupillary response and variability of gaze data. Predicted differences due to dispositional levels of anxiety were also found in the driving control and effort data. Although both groups of drivers performed worse under the threatening condition, the performance of the high trait anxious individuals was affected to a greater extent by the anxiety manipulation than the performance of the low trait anxious drivers. The findings suggest that processing efficiency theory holds promise as a theoretical framework for examining the relationship between anxiety and performance in sport.

Neuronal activity in the lateral cerebellum of the cat related to visual stimuli at rest, visually guided step modification, and saccadic eye movements

1 The discharge patterns of 166 lateral cerebellar neurones were studied in cats at rest and during visually guided stepping on a horizontal circular ladder. A hundred and twelve cells were tested against one or both of two visual stimuli: a brief full‐field flash of light delivered during eating or rest, and a rung which moved up as the cat approached. Forty‐five cells (40 %) gave a short latency response to one or both of these stimuli. These visually responsive neurones were found in hemispheral cortex (rather than paravermal) and the lateral cerebellar nucleus (rather than nucleus interpositus). 2 Thirty‐seven cells (of 103 tested, 36 %) responded to flash. The cortical visual response (mean onset latency 38 ms) was usually an increase in Purkinje cell discharge rate, of around 50 impulses s−1 and representing 1 or 2 additional spikes per trial (1.6 on average). The nuclear response to flash (mean onset latency 27 ms) was usually an increased discharge rate which was shorter lived and converted rapidly to a depression of discharge or return to control levels, so that there were on average only an additional 0.6 spikes per trial. A straightforward explanation of the difference between the cortical and nuclear response would be that the increased inhibitory Purkinje cell output cuts short the nuclear response. 3 A higher proportion of cells responded to rung movement, sixteen of twenty‐five tested (64 %). Again most responded with increased discharge, which had longer latency than the flash response (first change in dentate output ca 60 ms after start of movement) and longer duration. Peak frequency changes were twice the size of those in response to flash, at 100 impulses s−1 on average and additional spikes per trial were correspondingly 3–4 times higher. Both cortical and nuclear responses were context dependent, being larger when the rung moved when the cat was closer than further away. 4 A quarter of cells (20 of 84 tested, 24 %) modulated their activity in advance of saccades, increasing their discharge rate. Four‐fifths of these were non‐reciprocally directionally selective. Saccade‐related neurones were usually susceptible to other influences, i.e. their activity was not wholly explicable in terms of saccade parameters. 5 Substantial numbers of visually responsive neurones also discharged in relation to stepping movements while other visually responsive neurones discharged in advance of saccadic eye movements. And more than half the cells tested were active in relation both to eye movements and to stepping movements. These combinations of properties qualify even individual cerebellar neurones to participate in the co‐ordination of visually guided eye and limb movements.

Evidence for interactive locomotor and oculomotor deficits in cerebellar patients during visually guided stepping

Abstract. Eight patients suffering from primary cerebellar degenerative diseases undertook a walkway task, demanding precise foot placement at each step, and a visual fixation task, requiring only eye movements. Step cycle and horizontal eye movements were recorded throughout the tasks and compared to those of healthy adults (including age- and sex-matched controls). Cerebellar patients displayed both locomotor and oculomotor deficits. Increases in duration of the stance, swing and double support phases of the step cycle were all shown to contribute to ataxic gait. Dysmetric saccades to fixate the footfall targets were seen more frequently in patients than in controls. These hypometric saccades were followed by one or more corrective saccades (patients: >45% accompanied by one or more corrective saccades; controls: <10% accompanied by a single corrective saccade). Similarities between the oculomotor deficits displayed by patients during the visual fixation task and when walking indicate that the latter are not merely a consequence of ataxic gait. The existence of several links between these locomotor and oculomotor deficits provides evidence for considerable interaction between the two control systems in the production of patterned eye and stepping movements. These results also suggest that the cerebellum plays an active role in the co-ordination of visually guided eye and limb movements during visually guided stepping.

Changes in the discharge patterns of motor cortical neurones associated with volitional changes in stepping in the cat

Extracellular recordings have been obtained from motor cortical neurones of cats walking along a horizontal ladder. We present responses obtained when the animal produced defined volitional changes in limb trajectory, and during different conditions of locomotion. Our results show substantial changes in discharge pattern of some cells under these different conditions. Encounters with displaced rungs produce marked changes in discharge pattern including some which precede foot contact and others graded to the magnitude and direction of displacement.

Rhythmic neuronal activity in the lateral cerebellum of the cat during visually guided stepping

1 The discharge patterns of 117 lateral cerebellar neurones were studied in cats during visually guided stepping on a horizontal circular ladder. Ninety per cent of both nuclear cells (53/59) and Purkinje cells (53/58) showed step‐related rhythmic modulations of their discharge frequency (one or more periods of ‘raised activity’ per step cycle of the ipsilateral forelimb). 2 For 31 % of nuclear cells (18/59) and 34 % of Purkinje cells (20/58) the difference between the highest and lowest discharge rates in different parts of the step cycle was > 50 impulses s−1. 3 Individual neurones differed widely in the phasing of their discharges relative to the step cycle. Nevertheless, for both Purkinje cells and nuclear cells population activity was significantly greater in swing than in stance; the difference was more marked for the nuclear population. 4 Some cells exhibited both step‐related rhythmicity and visual responsiveness (28 of 67 tested, 42 %), whilst others were rhythmically active during locomotion and increased their discharge rate ahead of saccadic eye movements (11 of 54 tested, 20 %). The rhythmicity of cells that were visually responsive was typical of the rhythmicity seen in the whole locomotor‐related population. The step‐related rhythmicity of cells that also discharged in relation to saccades was generally below average strength compared with the cortical and nuclear populations as a whole. 5 The possibility is discussed that the rhythmicity of dentate neurones acts as a powerful source of excitatory locomotor drive to motor cortex, and may thereby contribute to establishing the step‐related rhythmicity of motor cortical (including pyramidal tract) neurones. More generally, the activity patterns of lateral cerebellar neurones provide for a role in the production of visually guided, co‐ordinated eye and body movements.

Changes in the discharge patterns of cat motor cortex neurones during unexpected perturbations of on-going locomotion.

1. The impulse activity of single neurones in the forelimb part of the motor cortex was recorded extracellularly in unrestrained cats during self‐paced locomotion on a horizontal circular ladder. 2. Fifty‐one cells (forty‐nine of which discharged rhythmically in time with the step cycle) were recorded during encounters with a number of rungs that could be locked firmly in position or, alternatively, held in position by weak springs so that when stepped on they unexpectedly descended (under the weight of the animal) from 1 to 5 cm before contacting a mechanical stop. 3. In eleven cells (22%) including four fast‐axon pyramidal tract neurones (PTNs), an increase in discharge occurred when the contralateral forelimb descended unexpectedly. Onset latency relative to the start of rung movement ranged from ca 20 to ca 100 ms. In eight cells latency was such that most of the response preceded contact of the rung with the stop; averaged over a number of trials the altered discharge in five of these cells (including two PTNs) represented an accurate profile of the averaged velocity of rung (and foot) descent. The three remaining cells appeared to be responding largely to the cessation of rung movement. 4. Thirty‐six of the cells were also studied during unexpected descent of the ipsilateral forelimb and six (17%) displayed an increase in discharge (onset latency ca 35 to ca 80 ms); three of these were among those that also responded to contralateral descents. 5. These findings for skilled locomotion requiring a high degree of visuomotor coordination are discussed and it is concluded that the motor cortex is rapidly informed regarding unexpected perturbations delivered to the contralateral forelimb at the onset of stance and that changes are evoked in the pattern of impulse traffic descending via the pyramidal tract.

Prevention of coordinated eye movements and steering impairs driving performance

When approaching a bend in the road, a driver looks across to the inside kerb before turning the steering wheel. Eye movements and steering are tightly linked, with the eyes leading, which means that the oculomotor controller can assist the neural centres controlling steering. This optimum coordination is observed for all drivers; but despite being the preferred solution to the motor-control problem of successfully steering along a winding road, the question remains as to how crucial such coordinated eye and steering movements are for driving performance. Twenty subjects repeatedly drove a simulated stage of the World Rally Championship, aiming to complete the course in the fastest possible time. For the first six repetitions they used the usual coordination of eye movements and steering; for drives 7–12 they were instructed to fixate on a small spot in the centre of the screen (centre gaze). Prevention of coordination in this way impaired their performance (drives 6 and 7 compared), dramatically increasing their time taken to complete the course, equivalent to slipping 19 places down the leader board in the actual rally stage. This indicates that the usual pattern of eye movements correlated with steering is crucial for driving performance. Further experiments are suggested to reveal whether any attentional demand associated with keeping the eyes still contributes to the loss in performance.