The response of the walking human to specific, transient sensory disturbances is well documented (reviewed in Dietz 1986; Stein, Yang, Edamura & Capaday, 1991). Many of these responses in the human resemble those found in other mammals, such as the cat (reviewed in Rossignol, 1996). Interestingly, however, there are certain responses typically seen in reduced preparations of cats that are very weak in the adult human. For example, unloading the extensor muscles of the limb in the late stance phase is necessary for the initiation of the subsequent swing phase in the spinal or decerebrate cat (e.g. Duysens & Pearson, 1980; Conway, Hultborn & Kiehn, 1987; Gossard, Brownstone, Barajon & Hultborn, 1994). The magnitude of such responses was extremely weak in the intact human (Stephens & Yang, 1996a,b). Other conditions such as the importance of hip extension for the initiation of the swing phase (Grillner & Rossignol, 1978) are clearly not functioning in the same way in the intact human as in cat preparations, since humans can easily walk with large degrees of hip flexion such as are needed when walking in a crouched position through a low tunnel. The question remains, however, whether the underlying mechanisms for controlling walking are fundamentally different between these species, or whether the preparations studied (i.e. intact human versus spinal or decerebrate cats) can account for the differences. There is certainly some suggestion that the preparation can have a profound influence. The responses of load-sensitive receptors in the muscle, in particular, differ depending on whether the animal is spinalized, decerebrated (McCrea, Shefchyk, Stephens & Pearson, 1995) or intact (Whelan & Pearson, 1998). The reflex responses to force changes are clearest in immobilized spinal or decerebrate cats (Conway et al. 1987; Gossard et al. 1994; Guertin, Angel, Perreault & McCrea, 1995), less strong in walking decerebrate cats (Whelan, Hiebert & Pearson, 1995), and weakest in intact cats (Whelan & Pearson, 1998).
One of the ways to address the above question is to study walking in humans, in states comparable to the decerebrate or spinal cat. Adult humans are sometimes in such states, but when in those states, stepping behaviour is extremely rare (Calancie, Needham-Shropshire, Jacobs, Willer, Zych & Green, 1994; Hanna & Frank, 1995; Dietz, Colombo, Jensen & Baumgartner, 1995). Infants, on the other hand, exhibit a stepping response at birth (Peiper, 1929), and indeed much earlier in utero (de Vries, Visser & Prechtl, 1984). This stepping behaviour appears to be controlled largely by the spinal and brainstem circuitry, since anencephalic infants exhibit similar responses (Peiper, 1961). Thus, infants offer the opportunity for studying the response of humans to similar transient disturbances in sensory input during stepping, before the cerebrum exerts its full control. The response of infants to such disturbances may offer a glimpse at the underlying mechanisms for controlling human walking. This paper presents the development of feasible procedures to study the role of sensory input in stepping in the human infant.
In order to study how sensory input is controlled during infant stepping, regular, sustained stepping is needed. Minor perturbations can then be applied during a sequence of steps to determine the response to the disturbance (reviewed in Rossignol, 1996). Stepping can be elicited in infants at birth through to about 2 months of age. Ideally, this would be the best age to study stepping, because cerebral influences on stepping are presumably smallest at this time. In reality, infants at this age are rarely in an awake and alert state, optimal for eliciting stepping. After 2 months of age, stepping is difficult to obtain for a duration of about 4–6 months (McGraw, 1940). The ability to study stepping during this time (i.e. between 2 and 7 months of age) is clearly advantageous, because the infant is alert for longer periods of time in the day, and the cerebral influences probably remain small. Daily practice in stepping is known to prevent the disappearance of the stepping response and increase the number of steps obtained in the laboratory (Zelazo, Zelazo & Kolb, 1972). Thus, the first issue addressed in this paper is the effect of such practice. It is not clear whether daily practice would produce a sufficiently regular pattern of walking, and whether it would induce changes in the locomotor pattern itself. Thus, the walking patterns of two groups of infants were compared, those with practice and those without.
The second issue addressed is whether the muscle activation patterns of infant stepping are regular and reproducible. Most earlier studies on supported stepping in infants reported that co-contraction was common (Forssberg & Wallberg, 1980; Berger, Altenmueller & Dietz, 1984; Forssberg, 1985, 1986; Thelen & Cooke, 1987), and that clear alternation of flexors and extensors was not present until much later in development, well after independent walking has been established (Berger et al. 1984; Leonard, Hirchfeld & Forssberg, 1991). Only one study reported clear reciprocally alternating contractions in supported walking (Okamoto & Goto, 1985). In re-examining this issue, our results agree with Okamoto & Goto (1985), in which alternation of flexor and extensor contraction was the norm in infants of all ages during supported stepping.
Finally, the responses to changes in sensory input induced by changes in treadmill speed or ground support were determined. Infants responded to changes in speed by modifying the extensor burst duration without much change in the flexor burst, as is the case in intact cats (Halbertsma, 1983) and adult humans (Grillner, Halbertsma, Nilsson & Thorstensson, 1979). When airstepping could be induced, the cycle durations were short, and the co-ordination of the two limbs less rigid than treadmill walking, as in spinal cats (Bradley & Smith, 1988).