Developmental Psychobiology
Brief Report Marianne Barbu-Roth1 David I. Anderson2,3 Adeline Despre`s1 Ryan J. Streeter2 Dominique Cabrol4 Michael Trujillo2 Joseph J. Campos3 Joe¨lle Provasi5 1
Laboratoire Psychologie de la Perception Universite´ Paris Descartes—UMR 8158 CNRS 45 Rue des Saints Pe`res, 75006 Paris, France E-mail: marianne. [email protected] 2 Department of Kinesiology San Francisco State University San Francisco, California 3
Institute of Human Development University of California Berkeley, California 4
Maternite´ Port-Royal Assistance Publique—Hoˆpitaux de Paris Universite´ Paris Descartes Paris, France
Air Stepping in Response to Optic Flows That Move Toward and Away From the Neonate ABSTRACT: To shed further light on the perceptual regulation of newborn stepping, we compared neonatal air stepping in response to optic flows simulating forward or backward displacement with stepping forward on a surface. Twenty-two 3-day-olds performed four 60 s trials in which they stepped forward on a table (Tactile) or in the air in response to a pattern that moved toward (Toward) or away (Away) from them or was static (Static). Significantly more steps were taken in the Tactile and Toward conditions than the Static condition. The Away condition was intermediate to the other conditions. The knee joint activity across the entire trial was significantly greater in the Toward than the Away condition. Within-limb kinematics and between-limb coordination were very similar for steps taken in the air and on the table, particularly in the Toward and Tactile conditions. These findings highlight that visual and tactile stimulation can equally elicit neonatal stepping. ß 2013 Wiley Periodicals, Inc. Dev Psychobiol 56: 1142–1149, 2014. Keywords: infant; locomotion; neonate; optic flow; stepping; vision
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Laboratoire CHArt Ecole Pratique des Hautes Etudes Paris, France
INTRODUCTION Although the stepping pattern is one of the most extensively studied movements in the human infant’s repertoire, its perceptual regulation remains poorly understood. Clinicians have long known that stepping Manuscript Received: 21 February 2013 Manuscript Accepted: 16 September 2013 Correspondence to: Marianne Barbu-Roth Contract grant sponsor: France-Berkeley Fund Contract grant sponsor: NICHD Contract grant number: HD050638 Contract grant sponsor: The National Center on Minority Health and Health Disparities Contract grant number: P20MD00262 Contract grant sponsor: Re´gion Ile-de-France Contract grant sponsor: Agence Nationale de la Recherche Contract grant number: ANR-11-BSH2-007 01 Article first published online in Wiley Online Library (wileyonlinelibrary.com): 5 November 2013 DOI 10.1002/dev.21174 ß 2013 Wiley Periodicals, Inc.
can be elicited by tactile stimulation. Neonates will typically take several steps when supported in a standing position on a solid surface and tilted forward; a test that is standard in neurological assessments (Andre´-Thomas & Autgaerden, 1966; Fiorentino, 1981; Peiper, 1963). The stepping pattern is difficult to elicit in the traditional standing position from 8 weeks of age onward (McGraw, 1932); however, it reappears when the infant is exposed to tactile and mechanical stimulation from a moving treadmill belt (Thelen, 1986; Thelen & Ulrich, 1991). Infant treadmill stepping is surprisingly adaptable to a range of tactile inputs (Yang et al., 2004). A recent study has shown that neonatal stepping is also responsive to visual stimulation (Barbu-Roth et al., 2009). Three-day-old infants were held in the air, to prevent tactile stimulation from a surface, and exposed to a rotating pinwheel or a projected checkerboard pattern that was static or moved toward them,
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Developmental Psychobiology
simulating forward displacement. The infants took significantly more air steps when the checkerboard moved toward them than when exposed to the other conditions. The number of air steps in the “visual treadmill” condition was equivalent to the number tactilely-elicited steps taken when the feet were allowed to contact a surface. This surprisingly precocious responsiveness to visual stimulation is consistent with the visually triggered stepping that has been observed in primitive species like lobsters (Davis & Ayers, 1972) as well as the head retraction documented in human neonates in response to optic flows that move linearly past each side of the face (Jouen, Lepecq, Gapenne, & Bertenthal, 2000) and in slightly older infants in response to looming optic flows that expand centrally toward the face (Nanez & Yonas, 1994). Visually triggered neonatal stepping challenges the idea that the stepping pattern is relatively immune from descending brain control during the first year of life (Yang et al., 2004). Even if the neonates in Barbu-Roth et al.’s (2009) study processed the approaching optic flow at a subcortical level, the subcortical visual system is higher in the nervous system than the brainstem and spinal circuits that are presumed to exert near-exclusive control over the stepping pattern (Dominici et al., 2011; Forssberg, 1985; Yang et al., 2004). Nevertheless, it is important to replicate the findings reported by Barbu-Roth et al. (2009) before accepting that higher brain centers can exert control over neonatal stepping. Moreover, it is important to determine whether air stepping and stepping on a surface are similar behaviors to know whether the visual control of air stepping likely generalizes to the traditional tactilely-elicited steps that are presumed to be the precursors to independent upright locomotion (Thelen & Ulrich, 1991; Yang et al., 2004; Zelazo, Zelazo, & Kolb, 1972). Although air stepping has been documented previously (Lamb & Yang, 2000; Thelen & Fisher, 1982; Zelazo et al., 1972), we know relatively little about it. Our primary objective in the current study was to build on Barbu-Roth et al.’s (2009) initial study and focus on two questions: (1) do neonates step in a different way to optic flows that move toward or away from them, and (2) are steps taken in the air kinematically similar to steps taken on a surface? Davis and Ayers (1972) have reported that lobsters and other species will walk forward or backward when exposed to optic flows that move toward or away from them and Lamb and Yang (2000) have demonstrated that infants are capable of stepping backward on a treadmill at 2 months of age. Differential step kinematics to approaching and receding optic flows would provide compelling evidence that the coupling between vision
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and stepping is quite sophisticated; perhaps as sophisticated as the coupling between stepping and tactile input. We hypothesized that the neonates would take more air steps when the optic flows moved toward them than away from them based on Lamb and Yang’s (2000) finding that only 69% of infants who stepped forward on a treadmill were also capable of stepping backward. However, we expected more air stepping in the two optic flow conditions than the static condition. Given the reported differences between forward and backward walking in adults (e.g., Grasso, Bianchi, & Lacquaniti, 1998) and 2-month-old infants (Lamb & Yang, 2000), we speculated that any differences in the air stepping kinematics between the two optic flow conditions would be localized at the knee joint. We hypothesized that the kinematics would be very similar when the neonates stepped in the air and on a surface. Finally, we expected to see similar step counts when infants stepped in the air to the approaching optic flow and when they stepped on the surface, replicating BarbuRoth et al.’s (2009) findings.
METHOD Participants The final sample consisted of 22 3-day-old infants (9 girls and 13 boys, mean age of 107.9 hr, SD ¼ 38.9) with uncomplicated deliveries, mean weight of 3,394 g (SD ¼ 432.6), minimum Apgar score of 7 at 5 min after birth and mean term of 39.6 weeks (SD ¼ 1.5). The participants were predominantly middle class and 90% were Caucasian. The other 10% were of North or Central African descent. The mothers provided written informed consent prior to their infants’ participation in the study. All infants were tested just after feeding when awake and alert and were rated in stage 3 (eyes open, no movements) on Prechtl’s (1974) scale just prior to testing. Infants’ data were not used if they cried more than a total of 30 s across the four experimental conditions, fell asleep, or did not look at the table surface for more than 30 s during any of the trials. Twelve additional infants were excluded from the final sample—five for excessive crying, two for falling asleep, one for eye closure, and four because they did not step in any of the conditions—leaving the final sample of 22.
Materials and Apparatus The primary piece of apparatus was a 1 m 1 m .46 m (h l w) table with a solid rear projection screen
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as a surface. The visual stimuli were created using Pascal software and run on a PC computer connected to a video projector placed on the floor 2 m from a mirror (tilted at 45 degrees) that reflected the images onto the surface. The visual stimulus was a pattern of black circles of .10 m projected size (approximate spatial frequency of .06 cycle/degree relative to the infants’ eyes) on a white background. This pattern was either static or moved toward or away from the infant at 23 degrees/s (17 cm/s, approximate temporal frequency of .7 Hz relative to a stationary point). The circles were spaced .08 m apart in a uniform grid, such that there were six rows of three circles extending from the table edge closest to the infant to the edge farthest away in the static condition. The circle size did not change when the pattern moved. Two digital video cameras (Sony DCR-HC38) were positioned at 45 degrees relative to the infant’s midsagittal plane and at 90 degrees relative to each other to capture stepping behavior. In other words, the cameras and infant formed an isosceles triangle, with the infant at the vertex angle (90 degrees). The height of each camera was 1.2 m and each camera was 2 m away from the infant.
Procedure Upon arrival at the laboratory, the infants were undressed down to an undergarment and 20 mm diameter reflective markers were attached to each lateral malleolus of the ankles and each lateral epicondyle of the knees using black and white striped elastic bands to aid in digitizing the joint centers. Markers attached above the anterior inferior iliac spine and the acromion processes were digitized directly as approximations of the hip and shoulder joints respectively. The infants were tested in four randomly ordered 1-min conditions (with a 1 min break between conditions): (1) air stepping while held above the translating pattern of circles that moved toward them (Toward), (2) air stepping while held above the translating pattern of circles that moved away from them (Away), (3) air stepping while held above the static pattern of circles (Static) and, (4) stepping forward on a white table surface (Tactile). One experimenter held the neonate by placing one hand on the infant’s chest and supporting the infant’s chin with her index fingers while using the other hand to provide light support to the infant’s bottom when necessary. Another experimenter monitored the infant for alertness and gaze direction. The infant’s trunk was inclined forward approximately 35 degrees from the vertical in the air stepping conditions to facilitate viewing of the visual stimulus. The trunk angle in the tactile condition was approximately 30
Developmental Psychobiology
degrees forward. In the Tactile condition, initiation of stepping was facilitated by first stimulating the “placing” response (i.e., by dragging the dorsal surface of the infant’s foot across the edge of the table).
Data Reduction Kinematic Analysis. The video data were digitized and analyzed using custom Kinematic Analysis software (Schleihauf, 2004). The 60 s video trials from each camera were initially split into 60 fields/s from the 30 frames/s captured by the cameras. The fields were then manually digitized to generate two dimensional (x, y) coordinates for the ankle, knee, hip, and shoulder. Due to the enormous amount of video data that were captured, we digitized every tenth field, for an effective sampling rate of 6 Hz. Perspective corrected three dimensional position data were computed with the similar triangle approach (Black & Sprigings, 1979; Schleihauf, 2004, p 137–140). Kinematic measures were computed with the Kinematic Analysis software (Schleihauf, 2012) and followed analysis procedures defined in Schleihauf (2004). Defining a Step and Calculating Inter-Limb Coordination. A two-step process was used to define an air step. First, two experienced coders independently counted the number of steps taken in the Tactile stepping condition. A tactile step was defined as a cycle of flexion–extension of the hip (independent of the time between flexion and extension) that included the foot leaving and then returning to the surface of the table. The first coding led to 95% agreement on what constituted a tactile step. Disagreements were then resolved via discussion. The second step involved generating a series of algorithms in Matlab based on the vertical displacement and velocity of the knee or ankle marker to match the qualitative step counts. The algorithm that best matched the qualitative step counts was one in which the knee marker had to exceed a 50 mm/s1 velocity threshold in the ascending (flexion) direction followed by a 25 mm/s1 velocity threshold in the descending (extension) direction. The algorithm yielded 94% agreement with the qualitative step counts. The criterion is almost identical to one used by Domello¨f, Ro¨nnqvist, and Hopkins (2007) to identify the onsets of newborn steps, though Domello¨f and coworkers did not use a descending criterion. The algorithm was then used to identify steps in the air stepping conditions. A separate Matlab program was written to locate the beginning and end of each step (the first zero velocity values prior to the 50 mm/s1 threshold and after the 25 mm/s1 threshold).
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Developmental Psychobiology
Inter-limb coordination was determined using criteria that were similar to those developed by Groenen, Kruijsen, Mulvey, and Ulrich (2010). Parallel steps were defined as steps initiated between the beginning and 20% of a step cycle on the opposite leg. Alternating steps were defined as steps initiated within 20–80% of a step cycle on the opposite leg. Serial steps (a new category) were defined as steps initiated after 80% of a step cycle on the opposite leg and up to 1 s after the end of the step cycle on the opposite leg. Finally, isolated steps were steps that occurred with more than 1 s of separation from another step (on the same or opposite leg).
Data Analysis The data were analyzed with Mixed-Model ANOVAs with Leg and Condition as fixed factors and Subject as a random factor. Data from the left and right legs were collapsed for all variables because preliminary analyses found no differences between the two legs. Tukey’s post hoc tests were used to follow up on significant main effects. The following dependent variables were analyzed: (1) number of steps per condition, (2) latency to initiate a step, (3) knee linear flexion/extension duration, (4) maximum knee linear flexion/extension displacement, (5) maximum knee linear flexion/extension velocity, (6) maximum knee angular flexion/ extension displacement, (7) maximum knee angular flexion/extension velocity, (8) inter-limb coordination, (9) RMS of knee angular displacement across the entire trial (used as an index of the total knee joint motion regardless of whether steps were taken), and (10) duration of crying in each trial. Note that variables 1–5 were based on the vertical motion of the marker on each knee joint. For example, knee linear flexion displacement and velocity refer to vertical displacement of the knee marker in the upward direction and the rate of change of that displacement (note, the maker essentially serves as an index of the motion of the thigh segment and hip joint).
RESULTS The means and standard deviations for each of the dependent variables are presented in Table 1. For simplicity, we present only the significant findings in this section.
Total Number of Steps The ANOVA revealed significant differences among conditions, F (3, 63) ¼ 3.38, p < .05, h2 ¼ .07. Significantly more steps were taken in the Toward and Tactile
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conditions than in the Static condition, The Toward and Tactile conditions were not significantly different from each other and the Away condition was intermediate between the other conditions and not significantly different from any of them.
Inter-Limb Coordination (Step Types) The number of Isolated, Parallel, Alternating, and Serial steps were compared within each condition (see Fig. 1). (Note; we did not compare step types across conditions because the total number of steps was significantly lower in the Static condition than the other conditions.) Because the data were not normally distributed in the Static condition, the data were square-root transformed prior to analysis in each of the conditions. In the Static condition, the ANOVA was significant, F (3, 50) ¼ 21.95, p < .05, h2 ¼ .40. Significantly more Isolated steps were taken than the other three step types, which did not differ in number from each other. In the Toward condition, the ANOVA was significant, F (3, 50) ¼ 12.08, p < .05, h2 ¼ .22. Significantly more Alternating and Isolated steps were taken than Parallel and Serial steps, which did not differ from each other. In the Away condition, the ANOVA was significant, F (3, 50) ¼ 8.24, p < .05, h2 ¼ .19. Significantly more Isolated steps were taken than Parallel and Serial steps, but not Alternating steps; the number of Alternating, Parallel, and Serial steps was not significantly different. In the Tactile condition, the ANOVA was also significant, F (3, 50) ¼ 14.48, p < .05, h2 ¼ .28. Similar to what was found in the Toward condition, significantly more Alternating and Isolated steps were taken than Parallel and Serial steps; the number of Isolated and Alternating steps was not different and the number of Parallel and Serial steps was not different.
RMS of Knee Angle for the Entire Trial Only the air stepping conditions were included in this analysis because repositioning of the infants in the Tactile stepping condition after they had taken a few steps increased the overall activity in each leg. The ANOVA was significant, F (2, 42) ¼ 3.68, p < .05, h2 ¼ .05. The RMS value was significantly higher (i.e., the knee was more active) in the Toward condition than in the Away and Static conditions, which were not significantly different from each other.
DISCUSSION The significantly higher step numbers in the Toward and Tactile conditions than the Static air stepping
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Developmental Psychobiology
Table 1. Means and Standard Deviations (SD) for the Step Counts, Step Latency, Stepping Kinematic Variables, and Crying Durations Variable
Static
Steps (per min)
4.36 (4.6)
Latency (s) Step duration (s) Linear knee flexion duration (s) Linear knee extension duration (s) Linear knee flexion displacement (mm) Linear knee extension displacement (mm) Linear knee flexion velocity (mm/s1) Linear knee extension velocity (mm/s1) Knee angular flexion displacement (degree) Knee angular extension displacement (degree) Knee angular flexion velocity (degree/s1) Knee angular extension velocity (degree/s1) Crying (s) RMS of knee angular displacement
13.93 1.10 .51 .58 26.83 18.64 93.29 61.75 21.63
(14.2) (.3) (.1) (.2) (10.3) (9.6) (38.4) (34.8) (9.6)
Toward 10.05 (12.1) 11.24 1.10 .58 .51 29.72 20.55 106.14 70.43 26.5
Tactile
8.68 (9.5)
10.36 (8.2)
(14.3) 11.98 (13.8) (.3) 1.06 (.4) (.2) .47 (.2) (.2) .58 (.2) (8.1) 25.2 (10.9) (9.5) 20.22 (8.7) (36.22) 99.51 (35.93) (31.7) 67.08 (31.8) (8.7) 22.14 (9.8)
15.31 (9.2)
18.04 (7.9)
79.37 54.34 .04 35.38
107.53 69.73 .83 41.37
(33.6) (22.3) (.2) (10.2)
Away
(43.2) (34.8) (2.8) (13.4)
17.4 (7.6) 93.05 59.67 .54 35.77
(44.1) (30.8) (2.2) (13.6)
12.53 1.05 .48 .55 32.36 23.94 119.14 75.7 24.45
(11.7) (.3) (.2) (.2) (14.0) (11.8) (48.56) (35.2) (13.8)
p-Value p ¼ .02 To and Ta > St p ¼ .86 p ¼ .98 p ¼ .84 p ¼ .72 p ¼ .10 p ¼ .12 p ¼ .06 p ¼ .27 p ¼ .36
18.29 (8.4)
p ¼ .37
105.9 (52.5) 66.14 (29.6) 2.48 (6.6)
p ¼ .06 p ¼ .32 p ¼ .21 p ¼ .03 To > St and Aw
The p values represent the values for the omnibus ANOVAs and the abbreviations St, To, Aw, and Ta refer to the Static, Toward, Away, and Tactile conditions respectively. The number of infants for whom the step latency and the stepping kinematic means and SDs were calculated were 16, 19, 18, and 22 for the Static, Toward, Away, and Tactile conditions respectively. The steps, crying durations, and RMS of the knee angle were based on all 22 infants. The step velocities represent the maximum velocities.
condition provide further evidence that visual and tactile inputs are equally effective at eliciting stepping movements in neonates and that visual input alone can elicit air stepping without the need of tactile stimula-
tion (Barbu-Roth et al., 2009). Moreover, the effectiveness of the visual stimulation provides further confirmation that the stepping pattern is likely more open to modification from higher brain input than
FIGURE 1 The number (and standard deviation) of isolated, parallel, alternating, and serial steps taken in each condition. Note that the standard deviation bars are only plotted in the positive direction to remove visual clutter. The omission of the bars below the means creates an illusion that there should be more differences within each condition than were reported in the results.
Developmental Psychobiology
previously suspected (Dominici et al., 2011; Forssberg, 1985; Yang et al., 2004). What remains unclear is whether the rudimentary couplings between vision and stepping are precursors to the more sophisticated regulation seen in older children and adults. Several researchers have noted that movement patterns in various species can be elicited by a wide range of stimuli early in development, with the neural circuits underlying perception becoming increasingly selective in their responsiveness toward a narrower range of stimuli as development continues (Fentress, 1987; Johnson, 2000; Nelson, 1993). Consequently, evidence of early couplings between perception and action may simply highlight the undifferentiated nature of the perceptual and motor systems. Further longitudinal research is needed to confirm whether the perceptualmotor coupling demonstrated here is a transient phenomenon or an indication of a very precocious biological preparedness to perceptually regulate actions. The differences between the Toward and Away air stepping conditions were subtle and difficult to interpret. We expected that differences in the stepping kinematics between the two conditions, potentially indicating forward stepping in response to an approaching optic flow and backward stepping in response to a receding optic flow, would provide evidence for specificity in the coupling between vision and stepping. Though we were confident our neonates could differentiate the different directions of optic flow, given that the subcortical visual pathways at birth can produce directionally specific eye movements in response to large optic flows at high velocities (Braddick, Atkinson, & Wattam-Bell, 2003), our neonates may have been unable to express forward and backward air stepping because of the tight synchrony between the movements of the ankle, knee, and hips during stepping. Consistent with previous research on infant stepping (e.g., Forssberg, 1985; Thelen, Bradshaw, & Ward, 1981; Thelen & Fisher, 1982), the tight synchrony between the joints was readily observable in all of the conditions we tested—all of the joints flexed together and extended together during each step in a pumping-type motion. Alternately, stepping backward may be more difficult than stepping forward, particularly when the infant is tilted forward; recall that only 69% of Lamb and Yang’s (2000) 2-month-olds who stepped forward on a treadmill were also able to step backward. The clearest difference between the Toward and Away conditions was in the RMS measure, an index of how much the knee joint flexed and extended throughout the entire 60 s trial, including stepping and nonstepping movements. We expected any differences between the Toward and Away conditions would be localized at the knee, however, the RMS measure
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suggests that the knee joints were simply more active in the Toward condition than the Away condition rather than engaged in a qualitatively different type of movement. At the very least, this difference in overall activity, combined with the extremely low and similar levels of crying in each of the conditions (see Tab. 1), helps to rule out arousal as an explanation for the significantly higher step numbers in the Toward condition than the Static condition. If the optic flows were simply arousing, we would expect identical RMS performance in the Toward and Away conditions. It is possible that additional differences between the Toward and Away conditions would be picked up with a higher data sampling rate than the one used in the current study. More research is clearly warranted to clarify the effects of approaching and receding optic flows on air stepping. Intra-limb and inter-limb similarities between the steps taken in the air and the steps taken on the table provide preliminary evidence that air stepping and tactile stepping are the same behaviors expressed in different perceptual contexts. Based on similarities in intra-limb kinematics and muscle activation patterns, Thelen and coworkers have claimed that supine kicking in the air and upright stepping on a surface are the same behaviors expressed in different postural contexts (e.g., Thelen et al., 1981; Thelen & Fisher, 1982; Thelen, Fisher, & Ridley-Johnson, 1984). The current findings lead us to suspect that kicking, stepping in the air, and stepping on a surface might all emerge from the same neuromuscular substrate. The current findings have important clinical implications. Researchers have already shown that typically developing infants and infants with spina bifida will take more steps and more mature steps on a treadmill when exposed to a patterned (checkerboard) treadmill belt compared to a plain one (Moerchen & Saeed, 2012; Pantall, Teulier, Smith, Moerchen, & Ulrich, 2011; Pantall, Teulier, & Ulrich, 2012). These findings raise the exciting possibility that treadmill interventions for infants with disabilities could be made even more effective if they were started earlier in development, perhaps as early as the neonatal period, and included exposure to optic flows (Teulier, Anderson, & BarbuRoth, 2013 and see Ulrich, 2010 for a convincing case for the need to start interventions as early as possible). The visual air stepping paradigm could be highly appropriate in its own right for stimulating leg movements in young infants with disabilities, particularly when there is concern that early weight bearing might lead to further musculoskeletal complications. It could also be a highly effective technique for stimulating alternating stepping in older infants who have difficulty supporting their own weight and/or pushing their legs
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against a surface. Air stepping practice might yield positive transfer to independent walking, though probably not the same degree of transfer that has been shown from supported stepping practice on a stationary surface or a moving treadmill belt. Ultimately, the efficacy of early locomotor interventions for children with disabilities will improve markedly as our understanding of the perceptual control of primitive movement patterns increases.
NOTES This work was supported by the France-Berkeley Fund, NICHD grant HD050638, grant P20MD00262 from the National Center on Minority Health and Health Disparities, grant from Re´gion Ile-de-France and grant ANR-11-BSH2-007 01 from the Agence Nationale de la Recherche. We would like to thank Viviane Huet and Brooke Schultz for their help with supplementary data analyses and we would like to thank all of the parents (and their newborns) who generously gave their time to participate in the experiment.
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Thelen E., & Ulrich, B. D. (1991). Hidden skills: A dynamic systems analysis of treadmill stepping during the first year. Monographs of the Society for Research in Child Development, 56(1), 1–98; discussion 99–104. Ulrich, B. D. (2010). Opportunities for early intervention based on theory, basic neuroscience, and clinical science. Physical Therapy, 90(12), 1868–1880. Yang, J. F., Lam, T., Pang, M. Y., Lamont, E., Musselman, K., & Seinen, E. (2004). Infant stepping a window to the behaviour of the human pattern generator for walking. Canadian Journal of Physiology, Pharmacology, 82(8– 9):662–674. Zelazo, P. R., Zelazo, N. A., & Kolb, S. (1972). “Walking” in the newborn. Science, 176(32), 314–315.
Brief Report Marianne Barbu-Roth1 David I. Anderson2,3 Adeline Despre`s1 Ryan J. Streeter2 Dominique Cabrol4 Michael Trujillo2 Joseph J. Campos3 Joe¨lle Provasi5 1
Laboratoire Psychologie de la Perception Universite´ Paris Descartes—UMR 8158 CNRS 45 Rue des Saints Pe`res, 75006 Paris, France E-mail: marianne. [email protected] 2 Department of Kinesiology San Francisco State University San Francisco, California 3
Institute of Human Development University of California Berkeley, California 4
Maternite´ Port-Royal Assistance Publique—Hoˆpitaux de Paris Universite´ Paris Descartes Paris, France
Air Stepping in Response to Optic Flows That Move Toward and Away From the Neonate ABSTRACT: To shed further light on the perceptual regulation of newborn stepping, we compared neonatal air stepping in response to optic flows simulating forward or backward displacement with stepping forward on a surface. Twenty-two 3-day-olds performed four 60 s trials in which they stepped forward on a table (Tactile) or in the air in response to a pattern that moved toward (Toward) or away (Away) from them or was static (Static). Significantly more steps were taken in the Tactile and Toward conditions than the Static condition. The Away condition was intermediate to the other conditions. The knee joint activity across the entire trial was significantly greater in the Toward than the Away condition. Within-limb kinematics and between-limb coordination were very similar for steps taken in the air and on the table, particularly in the Toward and Tactile conditions. These findings highlight that visual and tactile stimulation can equally elicit neonatal stepping. ß 2013 Wiley Periodicals, Inc. Dev Psychobiol 56: 1142–1149, 2014. Keywords: infant; locomotion; neonate; optic flow; stepping; vision
5
Laboratoire CHArt Ecole Pratique des Hautes Etudes Paris, France
INTRODUCTION Although the stepping pattern is one of the most extensively studied movements in the human infant’s repertoire, its perceptual regulation remains poorly understood. Clinicians have long known that stepping Manuscript Received: 21 February 2013 Manuscript Accepted: 16 September 2013 Correspondence to: Marianne Barbu-Roth Contract grant sponsor: France-Berkeley Fund Contract grant sponsor: NICHD Contract grant number: HD050638 Contract grant sponsor: The National Center on Minority Health and Health Disparities Contract grant number: P20MD00262 Contract grant sponsor: Re´gion Ile-de-France Contract grant sponsor: Agence Nationale de la Recherche Contract grant number: ANR-11-BSH2-007 01 Article first published online in Wiley Online Library (wileyonlinelibrary.com): 5 November 2013 DOI 10.1002/dev.21174 ß 2013 Wiley Periodicals, Inc.
can be elicited by tactile stimulation. Neonates will typically take several steps when supported in a standing position on a solid surface and tilted forward; a test that is standard in neurological assessments (Andre´-Thomas & Autgaerden, 1966; Fiorentino, 1981; Peiper, 1963). The stepping pattern is difficult to elicit in the traditional standing position from 8 weeks of age onward (McGraw, 1932); however, it reappears when the infant is exposed to tactile and mechanical stimulation from a moving treadmill belt (Thelen, 1986; Thelen & Ulrich, 1991). Infant treadmill stepping is surprisingly adaptable to a range of tactile inputs (Yang et al., 2004). A recent study has shown that neonatal stepping is also responsive to visual stimulation (Barbu-Roth et al., 2009). Three-day-old infants were held in the air, to prevent tactile stimulation from a surface, and exposed to a rotating pinwheel or a projected checkerboard pattern that was static or moved toward them,
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simulating forward displacement. The infants took significantly more air steps when the checkerboard moved toward them than when exposed to the other conditions. The number of air steps in the “visual treadmill” condition was equivalent to the number tactilely-elicited steps taken when the feet were allowed to contact a surface. This surprisingly precocious responsiveness to visual stimulation is consistent with the visually triggered stepping that has been observed in primitive species like lobsters (Davis & Ayers, 1972) as well as the head retraction documented in human neonates in response to optic flows that move linearly past each side of the face (Jouen, Lepecq, Gapenne, & Bertenthal, 2000) and in slightly older infants in response to looming optic flows that expand centrally toward the face (Nanez & Yonas, 1994). Visually triggered neonatal stepping challenges the idea that the stepping pattern is relatively immune from descending brain control during the first year of life (Yang et al., 2004). Even if the neonates in Barbu-Roth et al.’s (2009) study processed the approaching optic flow at a subcortical level, the subcortical visual system is higher in the nervous system than the brainstem and spinal circuits that are presumed to exert near-exclusive control over the stepping pattern (Dominici et al., 2011; Forssberg, 1985; Yang et al., 2004). Nevertheless, it is important to replicate the findings reported by Barbu-Roth et al. (2009) before accepting that higher brain centers can exert control over neonatal stepping. Moreover, it is important to determine whether air stepping and stepping on a surface are similar behaviors to know whether the visual control of air stepping likely generalizes to the traditional tactilely-elicited steps that are presumed to be the precursors to independent upright locomotion (Thelen & Ulrich, 1991; Yang et al., 2004; Zelazo, Zelazo, & Kolb, 1972). Although air stepping has been documented previously (Lamb & Yang, 2000; Thelen & Fisher, 1982; Zelazo et al., 1972), we know relatively little about it. Our primary objective in the current study was to build on Barbu-Roth et al.’s (2009) initial study and focus on two questions: (1) do neonates step in a different way to optic flows that move toward or away from them, and (2) are steps taken in the air kinematically similar to steps taken on a surface? Davis and Ayers (1972) have reported that lobsters and other species will walk forward or backward when exposed to optic flows that move toward or away from them and Lamb and Yang (2000) have demonstrated that infants are capable of stepping backward on a treadmill at 2 months of age. Differential step kinematics to approaching and receding optic flows would provide compelling evidence that the coupling between vision
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and stepping is quite sophisticated; perhaps as sophisticated as the coupling between stepping and tactile input. We hypothesized that the neonates would take more air steps when the optic flows moved toward them than away from them based on Lamb and Yang’s (2000) finding that only 69% of infants who stepped forward on a treadmill were also capable of stepping backward. However, we expected more air stepping in the two optic flow conditions than the static condition. Given the reported differences between forward and backward walking in adults (e.g., Grasso, Bianchi, & Lacquaniti, 1998) and 2-month-old infants (Lamb & Yang, 2000), we speculated that any differences in the air stepping kinematics between the two optic flow conditions would be localized at the knee joint. We hypothesized that the kinematics would be very similar when the neonates stepped in the air and on a surface. Finally, we expected to see similar step counts when infants stepped in the air to the approaching optic flow and when they stepped on the surface, replicating BarbuRoth et al.’s (2009) findings.
METHOD Participants The final sample consisted of 22 3-day-old infants (9 girls and 13 boys, mean age of 107.9 hr, SD ¼ 38.9) with uncomplicated deliveries, mean weight of 3,394 g (SD ¼ 432.6), minimum Apgar score of 7 at 5 min after birth and mean term of 39.6 weeks (SD ¼ 1.5). The participants were predominantly middle class and 90% were Caucasian. The other 10% were of North or Central African descent. The mothers provided written informed consent prior to their infants’ participation in the study. All infants were tested just after feeding when awake and alert and were rated in stage 3 (eyes open, no movements) on Prechtl’s (1974) scale just prior to testing. Infants’ data were not used if they cried more than a total of 30 s across the four experimental conditions, fell asleep, or did not look at the table surface for more than 30 s during any of the trials. Twelve additional infants were excluded from the final sample—five for excessive crying, two for falling asleep, one for eye closure, and four because they did not step in any of the conditions—leaving the final sample of 22.
Materials and Apparatus The primary piece of apparatus was a 1 m 1 m .46 m (h l w) table with a solid rear projection screen
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as a surface. The visual stimuli were created using Pascal software and run on a PC computer connected to a video projector placed on the floor 2 m from a mirror (tilted at 45 degrees) that reflected the images onto the surface. The visual stimulus was a pattern of black circles of .10 m projected size (approximate spatial frequency of .06 cycle/degree relative to the infants’ eyes) on a white background. This pattern was either static or moved toward or away from the infant at 23 degrees/s (17 cm/s, approximate temporal frequency of .7 Hz relative to a stationary point). The circles were spaced .08 m apart in a uniform grid, such that there were six rows of three circles extending from the table edge closest to the infant to the edge farthest away in the static condition. The circle size did not change when the pattern moved. Two digital video cameras (Sony DCR-HC38) were positioned at 45 degrees relative to the infant’s midsagittal plane and at 90 degrees relative to each other to capture stepping behavior. In other words, the cameras and infant formed an isosceles triangle, with the infant at the vertex angle (90 degrees). The height of each camera was 1.2 m and each camera was 2 m away from the infant.
Procedure Upon arrival at the laboratory, the infants were undressed down to an undergarment and 20 mm diameter reflective markers were attached to each lateral malleolus of the ankles and each lateral epicondyle of the knees using black and white striped elastic bands to aid in digitizing the joint centers. Markers attached above the anterior inferior iliac spine and the acromion processes were digitized directly as approximations of the hip and shoulder joints respectively. The infants were tested in four randomly ordered 1-min conditions (with a 1 min break between conditions): (1) air stepping while held above the translating pattern of circles that moved toward them (Toward), (2) air stepping while held above the translating pattern of circles that moved away from them (Away), (3) air stepping while held above the static pattern of circles (Static) and, (4) stepping forward on a white table surface (Tactile). One experimenter held the neonate by placing one hand on the infant’s chest and supporting the infant’s chin with her index fingers while using the other hand to provide light support to the infant’s bottom when necessary. Another experimenter monitored the infant for alertness and gaze direction. The infant’s trunk was inclined forward approximately 35 degrees from the vertical in the air stepping conditions to facilitate viewing of the visual stimulus. The trunk angle in the tactile condition was approximately 30
Developmental Psychobiology
degrees forward. In the Tactile condition, initiation of stepping was facilitated by first stimulating the “placing” response (i.e., by dragging the dorsal surface of the infant’s foot across the edge of the table).
Data Reduction Kinematic Analysis. The video data were digitized and analyzed using custom Kinematic Analysis software (Schleihauf, 2004). The 60 s video trials from each camera were initially split into 60 fields/s from the 30 frames/s captured by the cameras. The fields were then manually digitized to generate two dimensional (x, y) coordinates for the ankle, knee, hip, and shoulder. Due to the enormous amount of video data that were captured, we digitized every tenth field, for an effective sampling rate of 6 Hz. Perspective corrected three dimensional position data were computed with the similar triangle approach (Black & Sprigings, 1979; Schleihauf, 2004, p 137–140). Kinematic measures were computed with the Kinematic Analysis software (Schleihauf, 2012) and followed analysis procedures defined in Schleihauf (2004). Defining a Step and Calculating Inter-Limb Coordination. A two-step process was used to define an air step. First, two experienced coders independently counted the number of steps taken in the Tactile stepping condition. A tactile step was defined as a cycle of flexion–extension of the hip (independent of the time between flexion and extension) that included the foot leaving and then returning to the surface of the table. The first coding led to 95% agreement on what constituted a tactile step. Disagreements were then resolved via discussion. The second step involved generating a series of algorithms in Matlab based on the vertical displacement and velocity of the knee or ankle marker to match the qualitative step counts. The algorithm that best matched the qualitative step counts was one in which the knee marker had to exceed a 50 mm/s1 velocity threshold in the ascending (flexion) direction followed by a 25 mm/s1 velocity threshold in the descending (extension) direction. The algorithm yielded 94% agreement with the qualitative step counts. The criterion is almost identical to one used by Domello¨f, Ro¨nnqvist, and Hopkins (2007) to identify the onsets of newborn steps, though Domello¨f and coworkers did not use a descending criterion. The algorithm was then used to identify steps in the air stepping conditions. A separate Matlab program was written to locate the beginning and end of each step (the first zero velocity values prior to the 50 mm/s1 threshold and after the 25 mm/s1 threshold).
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Inter-limb coordination was determined using criteria that were similar to those developed by Groenen, Kruijsen, Mulvey, and Ulrich (2010). Parallel steps were defined as steps initiated between the beginning and 20% of a step cycle on the opposite leg. Alternating steps were defined as steps initiated within 20–80% of a step cycle on the opposite leg. Serial steps (a new category) were defined as steps initiated after 80% of a step cycle on the opposite leg and up to 1 s after the end of the step cycle on the opposite leg. Finally, isolated steps were steps that occurred with more than 1 s of separation from another step (on the same or opposite leg).
Data Analysis The data were analyzed with Mixed-Model ANOVAs with Leg and Condition as fixed factors and Subject as a random factor. Data from the left and right legs were collapsed for all variables because preliminary analyses found no differences between the two legs. Tukey’s post hoc tests were used to follow up on significant main effects. The following dependent variables were analyzed: (1) number of steps per condition, (2) latency to initiate a step, (3) knee linear flexion/extension duration, (4) maximum knee linear flexion/extension displacement, (5) maximum knee linear flexion/extension velocity, (6) maximum knee angular flexion/ extension displacement, (7) maximum knee angular flexion/extension velocity, (8) inter-limb coordination, (9) RMS of knee angular displacement across the entire trial (used as an index of the total knee joint motion regardless of whether steps were taken), and (10) duration of crying in each trial. Note that variables 1–5 were based on the vertical motion of the marker on each knee joint. For example, knee linear flexion displacement and velocity refer to vertical displacement of the knee marker in the upward direction and the rate of change of that displacement (note, the maker essentially serves as an index of the motion of the thigh segment and hip joint).
RESULTS The means and standard deviations for each of the dependent variables are presented in Table 1. For simplicity, we present only the significant findings in this section.
Total Number of Steps The ANOVA revealed significant differences among conditions, F (3, 63) ¼ 3.38, p < .05, h2 ¼ .07. Significantly more steps were taken in the Toward and Tactile
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conditions than in the Static condition, The Toward and Tactile conditions were not significantly different from each other and the Away condition was intermediate between the other conditions and not significantly different from any of them.
Inter-Limb Coordination (Step Types) The number of Isolated, Parallel, Alternating, and Serial steps were compared within each condition (see Fig. 1). (Note; we did not compare step types across conditions because the total number of steps was significantly lower in the Static condition than the other conditions.) Because the data were not normally distributed in the Static condition, the data were square-root transformed prior to analysis in each of the conditions. In the Static condition, the ANOVA was significant, F (3, 50) ¼ 21.95, p < .05, h2 ¼ .40. Significantly more Isolated steps were taken than the other three step types, which did not differ in number from each other. In the Toward condition, the ANOVA was significant, F (3, 50) ¼ 12.08, p < .05, h2 ¼ .22. Significantly more Alternating and Isolated steps were taken than Parallel and Serial steps, which did not differ from each other. In the Away condition, the ANOVA was significant, F (3, 50) ¼ 8.24, p < .05, h2 ¼ .19. Significantly more Isolated steps were taken than Parallel and Serial steps, but not Alternating steps; the number of Alternating, Parallel, and Serial steps was not significantly different. In the Tactile condition, the ANOVA was also significant, F (3, 50) ¼ 14.48, p < .05, h2 ¼ .28. Similar to what was found in the Toward condition, significantly more Alternating and Isolated steps were taken than Parallel and Serial steps; the number of Isolated and Alternating steps was not different and the number of Parallel and Serial steps was not different.
RMS of Knee Angle for the Entire Trial Only the air stepping conditions were included in this analysis because repositioning of the infants in the Tactile stepping condition after they had taken a few steps increased the overall activity in each leg. The ANOVA was significant, F (2, 42) ¼ 3.68, p < .05, h2 ¼ .05. The RMS value was significantly higher (i.e., the knee was more active) in the Toward condition than in the Away and Static conditions, which were not significantly different from each other.
DISCUSSION The significantly higher step numbers in the Toward and Tactile conditions than the Static air stepping
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Table 1. Means and Standard Deviations (SD) for the Step Counts, Step Latency, Stepping Kinematic Variables, and Crying Durations Variable
Static
Steps (per min)
4.36 (4.6)
Latency (s) Step duration (s) Linear knee flexion duration (s) Linear knee extension duration (s) Linear knee flexion displacement (mm) Linear knee extension displacement (mm) Linear knee flexion velocity (mm/s1) Linear knee extension velocity (mm/s1) Knee angular flexion displacement (degree) Knee angular extension displacement (degree) Knee angular flexion velocity (degree/s1) Knee angular extension velocity (degree/s1) Crying (s) RMS of knee angular displacement
13.93 1.10 .51 .58 26.83 18.64 93.29 61.75 21.63
(14.2) (.3) (.1) (.2) (10.3) (9.6) (38.4) (34.8) (9.6)
Toward 10.05 (12.1) 11.24 1.10 .58 .51 29.72 20.55 106.14 70.43 26.5
Tactile
8.68 (9.5)
10.36 (8.2)
(14.3) 11.98 (13.8) (.3) 1.06 (.4) (.2) .47 (.2) (.2) .58 (.2) (8.1) 25.2 (10.9) (9.5) 20.22 (8.7) (36.22) 99.51 (35.93) (31.7) 67.08 (31.8) (8.7) 22.14 (9.8)
15.31 (9.2)
18.04 (7.9)
79.37 54.34 .04 35.38
107.53 69.73 .83 41.37
(33.6) (22.3) (.2) (10.2)
Away
(43.2) (34.8) (2.8) (13.4)
17.4 (7.6) 93.05 59.67 .54 35.77
(44.1) (30.8) (2.2) (13.6)
12.53 1.05 .48 .55 32.36 23.94 119.14 75.7 24.45
(11.7) (.3) (.2) (.2) (14.0) (11.8) (48.56) (35.2) (13.8)
p-Value p ¼ .02 To and Ta > St p ¼ .86 p ¼ .98 p ¼ .84 p ¼ .72 p ¼ .10 p ¼ .12 p ¼ .06 p ¼ .27 p ¼ .36
18.29 (8.4)
p ¼ .37
105.9 (52.5) 66.14 (29.6) 2.48 (6.6)
p ¼ .06 p ¼ .32 p ¼ .21 p ¼ .03 To > St and Aw
The p values represent the values for the omnibus ANOVAs and the abbreviations St, To, Aw, and Ta refer to the Static, Toward, Away, and Tactile conditions respectively. The number of infants for whom the step latency and the stepping kinematic means and SDs were calculated were 16, 19, 18, and 22 for the Static, Toward, Away, and Tactile conditions respectively. The steps, crying durations, and RMS of the knee angle were based on all 22 infants. The step velocities represent the maximum velocities.
condition provide further evidence that visual and tactile inputs are equally effective at eliciting stepping movements in neonates and that visual input alone can elicit air stepping without the need of tactile stimula-
tion (Barbu-Roth et al., 2009). Moreover, the effectiveness of the visual stimulation provides further confirmation that the stepping pattern is likely more open to modification from higher brain input than
FIGURE 1 The number (and standard deviation) of isolated, parallel, alternating, and serial steps taken in each condition. Note that the standard deviation bars are only plotted in the positive direction to remove visual clutter. The omission of the bars below the means creates an illusion that there should be more differences within each condition than were reported in the results.
Developmental Psychobiology
previously suspected (Dominici et al., 2011; Forssberg, 1985; Yang et al., 2004). What remains unclear is whether the rudimentary couplings between vision and stepping are precursors to the more sophisticated regulation seen in older children and adults. Several researchers have noted that movement patterns in various species can be elicited by a wide range of stimuli early in development, with the neural circuits underlying perception becoming increasingly selective in their responsiveness toward a narrower range of stimuli as development continues (Fentress, 1987; Johnson, 2000; Nelson, 1993). Consequently, evidence of early couplings between perception and action may simply highlight the undifferentiated nature of the perceptual and motor systems. Further longitudinal research is needed to confirm whether the perceptualmotor coupling demonstrated here is a transient phenomenon or an indication of a very precocious biological preparedness to perceptually regulate actions. The differences between the Toward and Away air stepping conditions were subtle and difficult to interpret. We expected that differences in the stepping kinematics between the two conditions, potentially indicating forward stepping in response to an approaching optic flow and backward stepping in response to a receding optic flow, would provide evidence for specificity in the coupling between vision and stepping. Though we were confident our neonates could differentiate the different directions of optic flow, given that the subcortical visual pathways at birth can produce directionally specific eye movements in response to large optic flows at high velocities (Braddick, Atkinson, & Wattam-Bell, 2003), our neonates may have been unable to express forward and backward air stepping because of the tight synchrony between the movements of the ankle, knee, and hips during stepping. Consistent with previous research on infant stepping (e.g., Forssberg, 1985; Thelen, Bradshaw, & Ward, 1981; Thelen & Fisher, 1982), the tight synchrony between the joints was readily observable in all of the conditions we tested—all of the joints flexed together and extended together during each step in a pumping-type motion. Alternately, stepping backward may be more difficult than stepping forward, particularly when the infant is tilted forward; recall that only 69% of Lamb and Yang’s (2000) 2-month-olds who stepped forward on a treadmill were also able to step backward. The clearest difference between the Toward and Away conditions was in the RMS measure, an index of how much the knee joint flexed and extended throughout the entire 60 s trial, including stepping and nonstepping movements. We expected any differences between the Toward and Away conditions would be localized at the knee, however, the RMS measure
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suggests that the knee joints were simply more active in the Toward condition than the Away condition rather than engaged in a qualitatively different type of movement. At the very least, this difference in overall activity, combined with the extremely low and similar levels of crying in each of the conditions (see Tab. 1), helps to rule out arousal as an explanation for the significantly higher step numbers in the Toward condition than the Static condition. If the optic flows were simply arousing, we would expect identical RMS performance in the Toward and Away conditions. It is possible that additional differences between the Toward and Away conditions would be picked up with a higher data sampling rate than the one used in the current study. More research is clearly warranted to clarify the effects of approaching and receding optic flows on air stepping. Intra-limb and inter-limb similarities between the steps taken in the air and the steps taken on the table provide preliminary evidence that air stepping and tactile stepping are the same behaviors expressed in different perceptual contexts. Based on similarities in intra-limb kinematics and muscle activation patterns, Thelen and coworkers have claimed that supine kicking in the air and upright stepping on a surface are the same behaviors expressed in different postural contexts (e.g., Thelen et al., 1981; Thelen & Fisher, 1982; Thelen, Fisher, & Ridley-Johnson, 1984). The current findings lead us to suspect that kicking, stepping in the air, and stepping on a surface might all emerge from the same neuromuscular substrate. The current findings have important clinical implications. Researchers have already shown that typically developing infants and infants with spina bifida will take more steps and more mature steps on a treadmill when exposed to a patterned (checkerboard) treadmill belt compared to a plain one (Moerchen & Saeed, 2012; Pantall, Teulier, Smith, Moerchen, & Ulrich, 2011; Pantall, Teulier, & Ulrich, 2012). These findings raise the exciting possibility that treadmill interventions for infants with disabilities could be made even more effective if they were started earlier in development, perhaps as early as the neonatal period, and included exposure to optic flows (Teulier, Anderson, & BarbuRoth, 2013 and see Ulrich, 2010 for a convincing case for the need to start interventions as early as possible). The visual air stepping paradigm could be highly appropriate in its own right for stimulating leg movements in young infants with disabilities, particularly when there is concern that early weight bearing might lead to further musculoskeletal complications. It could also be a highly effective technique for stimulating alternating stepping in older infants who have difficulty supporting their own weight and/or pushing their legs
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against a surface. Air stepping practice might yield positive transfer to independent walking, though probably not the same degree of transfer that has been shown from supported stepping practice on a stationary surface or a moving treadmill belt. Ultimately, the efficacy of early locomotor interventions for children with disabilities will improve markedly as our understanding of the perceptual control of primitive movement patterns increases.
NOTES This work was supported by the France-Berkeley Fund, NICHD grant HD050638, grant P20MD00262 from the National Center on Minority Health and Health Disparities, grant from Re´gion Ile-de-France and grant ANR-11-BSH2-007 01 from the Agence Nationale de la Recherche. We would like to thank Viviane Huet and Brooke Schultz for their help with supplementary data analyses and we would like to thank all of the parents (and their newborns) who generously gave their time to participate in the experiment.
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