Pre-landing muscle timing and post-landing effects of falling with continuous vision and in blindfold conditions

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Abstract

The present study examined the effect of continuous vision and its occlusion in timing of pre-landing actions during free falls. When vision is occluded, muscle activation is hypothesized to start relative to onset of the fall. However, when continuous vision is available onset of action is hypothesized to be relative to the moment of touchdown.

Six subjects performed 6 randomized sets of 6 trials after becoming familiar with the task. The 36 trials were divided in 2 visual conditions (vision and blindfold) and 3 heights of fall (15, 45 and 75 cm). EMG activity was recorded from the gastrocnemius and rectus femoris muscles during the falls. The latency of onset (Lo) and the lapse from EMG onset to touchdown (Tc) were obtained from these muscles. Vertical forces were recorded to assess the effects of pre-landing activity on the impacts at collision with and without continuous vision. Peak amplitude (Fmax), time to peak (Tmax) and peak impulse normalized to momentum (Inorm) were used as outcome measures.

Within flight time ranges of ∼50–400 ms, the results showed that Lo and Tc follow a similar linear trend whether continuous vision was available or occluded. However, the variability of Tc for each of the muscles was larger in the vision occluded condition. Analyses of variance showed that the rectus femoris muscle started consistently earlier in no vision trials. Finally, impact forces were not different in vision or blindfold conditions, and thus, they were not affected by minor differences in the timing of muscles prior to landing.

Thus, it appears that knowing the surroundings before falling may help to reduce the need for a continuous visual input. The relevance of such input cannot be ruled out for falls from high landing heights, but cognitive factors (e.g., attention to specific cues and anticipation of a fall) may play a dominant role in timing actions during short duration falls encountered daily.

Introduction

The free fall paradigm has been used to study the role of different sensory inputs in triggering and modulating reflexive and voluntary preparatory responses to sudden vertical descents. The use of such a paradigm has been justified in part by the fact that landings are shared by several tasks encountered daily. Visual and vestibular information have been assumed to participate in landings during running over irregular terrains (Warren et al., 1986), in sudden falls (Greenwood and Hopkins, 1976a, Greenwood and Hopkins, 1976b, Melvill Jones and Watt, 1971), in stepping downstairs or in jumping down (Greenwood and Hopkins, 1980). In the present study, we assessed the contribution of ongoing visual input in the preparation to land from self-released free falls. The timing of the landing preparatory actions when continuous vision is available is expected to be different from the preparatory actions in blindfolded free falls.

Visual control of motion is reviewed within different two different theoretical perspectives that are suitable for the present study. The first perspective emphasizes a strategy based on ongoing perceptual inputs. The other puts an emphasis on the use of cognitive factors regardless of the availability of continuous perception. The possibility that prior knowledge of the surroundings may actually override the use of continuous vision of the landing surface is used as an alternative hypothesis. In such case, prospective motor control based only on optic information may not dominate the modulation of landing actions. That is, cognitive mediators such as internal representations of the landing conditions may also be used.

A major concern with respect to the preparation for landing is the reduction of forces at impact. Preparatory landing responses during the flight are intended to prevent hard impacts with the ground and have been often identified by measures of muscular activity. For example, at different times during an unexpected fall, both reflexive and voluntary responses may be observed. Based on such response timing, it has been suggested that low height falls (<100 ms) do not allow preparation time for the vestibular-otolith reflexes to build up and generate the muscle force necessary to reduce landing jolts (Melvill Jones and Watt, 1971). In contrast, when fall time is longer, the initial reflexive burst is often followed by a secondary voluntary burst of activity that starts within 40–140 ms before the moment of touchdown (Greenwood and Hopkins, 1976a, Greenwood and Hopkins, 1976b). It has been argued that the onset of this second phase depends on vision of the landing surface (Greenwood and Hopkins, 1976a, Greenwood and Hopkins, 1976b).

Such a suggestion is compatible with the Tau (τ) model proposed by Lee et al., 1999, Lee, 1976, Lee, 1980, which argues that perceptuo-motor coordination relies on time to contact (the time left before touchdown in the present case). Such a model allows for associating the timing of EMG onset with the time to contact with the ground (Tc) as perceived by the subject. This model found support from observations in animals such as gannets (Lee and Reddish, 1981) and pigeons (Lee et al., 1993), and has been tested in the past in human landing performances as well. For example, Sidaway and colleagues adopted Lee’s model as applied to the study of wing folding actions of gannets before entering the water (Lee and Reddish, 1981), and hypothesized also that continuous visual input may be used to trigger landing EMG responses at τ margin values (Sidaway et al., 1989). Their findings suggested that preparatory muscle activity was related to vision of the heights of fall and the landing surface, although their evidence regarding the use of an optic τ heuristic was less conclusive. In fact, Goodman and Liebermann (1992) calculated τ values from preliminary landing data in humans, but also took into consideration the height of the eyes and not only the height of fall from the feet to the ground (humans land on their feet and not on their heads as gannets do). They concluded that for landings from heights of fall of <1 m there was no evidence for a pre-landing muscle timing based on τ optics. However, they did not exclude the use of such a strategy for other tasks or conditions (higher, unrealistic heights for safe falls).

Santello (2005) reviewed the free fall literature with regard to these issues. From drop jump landing data, this author argued that EMG timing is not different with or without vision. At first glance, this is not surprising since such observations were also reported previously (Goodman and Liebermann, 1992, Greenwood and Hopkins, 1980). However, the finding that preparatory actions in visual and blindfold landings are similar is only descriptive. In fact, as far as preparatory timing strategies are concerned, they open further controversy because the importance of visual strategies in the preparation to land is questioned. For instance, Santello and McDonagh (1998) suggested that instead of vision, vestibular information might play a role in modulating the timing and amplitude of the EMG activity during the pre-landing period. However, it should be noted that studies that measure pre-landing responses as a function of heights of fall (Santello and McDonagh, 1998, Santello et al., 2001, Sidaway et al., 1989) cannot lead to comparable results and interpretations with studies that use actual flight times to assess time-related strategies of control (Goodman and Liebermann, 1992, Greenwood and Hopkins, 1976a, Greenwood and Hopkins, 1976b, Lee and Reddish, 1981). Liebermann and Hoffman (2005) carried out an analysis of pre-landing actions using drop jumps from heights of fall adjusted for actual flight durations. In that study, pre-landing responses of highly experienced subjects were also assessed by measuring EMG onsets, but the results suggested the use of a timing strategy that was insensitive to changes in optic flow. This stemmed from the finding that EMG onset in conditions that enabled maximal optic flow was not different from EMG timing in conditions that minimized the optic flow during landing from heights of fall below one meter. Liebermann and Hoffman (2005) argued that a feedforward mode of control may be implemented with experience, and further concluded that the fact that vision is available during a motor performance does not necessarily imply that visual input is always used.

The interaction between a moving performer and its immediate environment has often been conceived as a lawfully modulated relationship based on the assumption that ‘moving around’ depends on the availability of continuous perceptual inputs. The “direct perception” approach, first formulated by Gibson, 1966, Gibson, 1979, suggests that the control of movement is closely related to perception of features of the environment that remain invariant in spite of the continuous changes of an observer relative to the objects in the surroundings and⧹or vice versa. Thus, in order to perceive subjects must move and in order to move subjects must perceive (see Michaels and Carello, 1981 for comprehensive material). Empirical evidence in support for such a conjecture was provided by Held (1965), who showed in animals and humans that active movement under voluntary control modifies the visual perception of the surroundings.

Gibson’s approach emphasized the role of information arriving from continuous vision (the optic flow), which is deemed essential for modulating motor actions in anticipatory or interceptive events (Lee et al., 1999). Lee formally expressed the relationship between an observer in motion and the static surroundings by suggesting that timing movement is related to a constant τ optic ratio (Lee, 1976, Lee, 1980, Lee, 1974). Tau may provide information about the rate of closure to an approaching surface and is defined as the inverse of the rate of dilation of an external image moving away or towards the eye projected onto its retina. Under conditions of constant velocity, τ enables the perception of the time to contact, which can be used in the control of avoidant and anticipatory behavior (Lee, 1980). Time to contact information may be useful, for example, in actions that involve catching an approaching ball (Savelsbergh et al., 1991), in intercepting and hitting a volleyball (Lee et al., 1983), in driving maneuvers in a collision course (Lee, 1976, van der Horst, 1991), during walking (Lee, 1974) or in regulating the steps during the run up in the long jump (Lee et al., 1982).

As suggested earlier in the manuscript, the τ ratio has been deemed relevant for timing the pre-landing actions during free falls. In such events, changes in perceived Tc are a function of the duration of the flight Ft, which depends on gravity acceleration g = 9.81 m/s2. The relationship between the variables Tc and Ft can be expressed as a constant of proportionality τ(t)=(Ft2-[Ft-Tc]2)/2·Lo (adapted from Lee and Reddish, 1981), where Lo is the time from release until the start of the EMG activity. Ft can be measured directly or can be estimated (assuming constant acceleration due to g alone) from Netwon’s formula Ft(s)=2·Height(m)/9.81(m/s2) for different heights of fall. Accordingly, Tc should increase at a negatively accelerated rate with increases in Ft until it reaches an asymptote. That is, under conditions of constant acceleration, as in vertical descents of gannets (Lee and Reddish, 1981), τ provides only an estimate of Tc. In such circumstances, timing of motor action is controlled based on a strategy that uses threshold values of time to contact. At a certain point in time, τ reaches a critical value as perceived by the subject. This is called the ‘τ margin strategy’ that provides the basis for an internal ‘perceptual trigger’ that informs the individual when to start a response (i.e., the moment during the flight when the muscles should be voluntarily contracted). Prospective use of visual information geared by τ is presumably more efficient (it is anticipatory), and does not require brain computations (it is immediate). According to a direct approach to action-perception control, timing of movement is reduced only to a perception of critical values provided by relative changes in optic inputs from invariant features of the environment. That is, perception is based on a continuous extraction of structured environmental information and not a result of computations based on internal representations of the environment.

An alternative approach that disputes the previous approach of Gibson is the constructivist approach (Fodor and Pylyshyn, 1981). From this vantage point, visual perception builds up from elementary bits of sensory information. In such a process of construction, cognitive components play an important role. The gist of the involvement of cognition in visual perception is evident in visual illusions (Gregory, 1998). Based on the assumption that visual information per se is ambiguous, it is hypothesized that the brain first integrates visual inputs and then interprets the information based on previous conjectures about their meaning. Consequently, perception cannot be dissociated from cognitive processes such as memory, information analysis and the ability to recognize events based on previous experience.

Furthermore, transformations from seeing (at the eye level) to perceiving (in the brain), and from perceiving to motor action (planning and execution levels) must involve neuro-cognitive factors (Churchland, 1989). This is because vision (the perceptual domain) deals with a metric in terms of visual (retinal or other) coordinates, while movement (the motor domain) involves another metric in terms of end-effector coordinates (Andersen, 1995, Bizzi and Mussa-Ivaldi, 1995, Georgopoulos, 1995). Thus, from a computational perspective, direct perception of Tc without further interpretation of the optic information cannot result in the control of action. Indeed, some would argue (Maunsell and Gibson, 1992) that a continuous flow of information at the retinal level is simply not useful in anticipating events since the visual delays in the neural transmission within the retina are so long that visual perception lags behind the motion of real physical objects in space and time (Schlag et al., 2000). Even though research suggests that such a gap of information may be compensated partially with an early neuronal pre-processing at the retinal level (Berry et al., 1999), some information might still be missing from the conscious perception of motion. Yet, our perception of a whole event (between start and end) seems to be complete. Therefore, researchers have assumed that missing perceptual inputs must be filled via brain process such as a cognitive extrapolation of the ‘where’ and ‘when’ an object will be. Evidence suggests that time to contact with a ball, for example, may be obtained from computation without relaying on continuous vision. Baseball fielders appear to use estimates of the initial velocity of a ball in flight to extrapolate its future location in space (McLeod et al., 2003). Changes in gaze angle may allow obtaining an optic equivalent of linear distance. Having estimated their actual distance from the ball together with the estimates of the initial ball velocity, baseball fielders are able to accurately adjust their running speed (McLeod et al., 2003). This process does not require a continuous visual input of the ball. Intermittent vision at specific times during an ongoing performance may be enough (Elliott, 1990). Finally, it should be mentioned that there is evidence suggesting that time to contact may also be computed even without a need for continuous vision, simply from a ratio between estimates of distance and velocity of approach (Smeets et al., 1996, Tresilian, 1991, Tresilian, 1993).

The present study attempts to resolve the issue of whether continuous vision is used when previous knowledge of the surrounding is available. For this purpose, subjects were allowed to practice landings until becoming familiar with task and the experimental conditions. The heights of fall were known prior to performing the landing trials. In such conditions, the timing characteristics of the preparatory landing actions were assessed. Different strategies were hypothesized in the control of pre-landing actions under the constraint of visual occlusion as well as in normal visual conditions. The ability to dissipate the impacts at touchdown was assumed to depend on these preparatory actions.

Section snippets

Subjects and design

Six male volunteers (mean age = 27.2 ± 3.8 years; mean height = 177.3 ± 4.3 cm; mean body mass = 76.6 ± 7.5 kg) performed a series of vertical descents from an overhead bar by self-releasing the handgrip. A repeated measures (RM) design was used in which every subject completed 36 landings from each of three heights (15, 45 and 75 cm) in blocks of six trials, performed in vision and blindfold conditions in random order. Subjects were paid for their participation but they could withdraw from the experiment at

Preliminary analysis of EMG onsets

A one-way ANOVA (4 ‘Subjects’) was carried out using the difference between the computer detected onsets and those of the experts (432 observations per subject). It was hypothesized that there were no differences between experts themselves, and no differences between the experts and the computer detection. However, the results yielded a significant effect (F(3,1296) = 47.234; p < 0.001) suggesting that there were some differences. Post hoc comparisons showed that onsets visually detected by three

Discussion

The results from the present free-fall experiments suggested that landings from falls in the range of heights that may be encountered in daily activities (e.g., at home, in working environments or in sports) are not significantly affected by the absence of continuous visual input when the surroundings are previously known to the performer. Preparatory actions with or without continuous vision are similar, although unequivocal support for one or the other model of action hypothesized here was

Summary and conclusion

Our findings showed that the relationship between the latency of EMG onset of two landing extensor muscles and the flight times followed similar linear trends in vision and blindfold conditions (for falls ⩽80 cm). Impact forces elicited in vision and blindfold trials were not different regardless of the variables used to assess the collision impacts. That is, with or without vision landing preparatory actions may be modulated in a similar manner. Moreover, the ability to dissipate the forces

Dr. Dario G. Liebermann works with the Sacker Faculty of Medicine at the University of Tel Aviv since October 2000. He has received his MSc in Kinesiology (Simon Fraser University) and completed the PhD degree in Applied Mathematics and Computer Sciences (Weizmann Institute of Science) followed by post-doc research in Clinical Neurosciences and Kinesiology (University of Calgary). He worked in the motor control area in diverse topics such as arm kinematic modeling, visual control of motion and

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    Dr. Dario G. Liebermann works with the Sacker Faculty of Medicine at the University of Tel Aviv since October 2000. He has received his MSc in Kinesiology (Simon Fraser University) and completed the PhD degree in Applied Mathematics and Computer Sciences (Weizmann Institute of Science) followed by post-doc research in Clinical Neurosciences and Kinesiology (University of Calgary). He worked in the motor control area in diverse topics such as arm kinematic modeling, visual control of motion and formation of inter-muscular coordination patterns. He lectures on diverse movement science topics at the Physical Therapy Department of the Stanley Steyer School of Health Professions – Sackler Faculty of Medicine, University of Tel Aviv.

    Dr. David Goodman received his PhD at the University of Iowa in 1981. He is now a professor in the School of Kinesiology, Simon Fraser University, where he teaches and conducts research in the area of motor control and learning. His proudest accomplishments are the achievements of the many students that have graduated from his lab.

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