Ontogenetic Development Of Sensorimotor Control In Manipulation

The ability to grasp using a precision grip involving the tips of the thumb and index finger first emerges in humans at approximately 8-10 months of age. However, fully mature patterns of grasping, lifting, and holding objects are not observed until about 8 years of age. During this period, there is gradual improvement in grasping behavior as well as qualitative improvements in the capacity to produce independent finger movements. These changes parallel the gradual maturation of the ascending and descending neural pathways that link the hand with the cerebral cortex. These observations strongly suggest that the control of the skilled precision lifting and manipulation relies to a large extent on cerebral processes.

As noted previously, when adults lift objects, they increase grip force and load force in phase such that the two forces increase and decrease together. As a consequence, a linear relationship between these forces is observed (Figs. 3B, 3C, and 7B). The motor system adapts the slope of this relationship to factors such as the frictional conditions and the shape of the contact surfaces but robustly maintains this force synergy (Figs. 3B and 3C). However, before 18 months of age, children do not exhibit such parallel control of grip and load forces (Fig. 7). Instead, they tend to increase grip force in advance of the load force in a sequential fashion. The transition from sequential force coordination to the mature parallel coordination is not completed until several years later. Young children also produce comparably slow increases in fingertip force before liftoff and these increases are discontinuous, featuring multiple peaks in force rate (Fig. 7A). In contrast, adults smoothly increase grip force and load force with a single peak in force rate. The discontinuous or start-and-stop force increases observed in young children suggest that they employ a feedback control strategy rather than feedforward control. That is, they continue to increase force in small increments until liftoff occurs. It is not until they receive somatosensory information that liftoff has occurred that they stop these increases. This feedback strategy is similar to that observed when adults underestimate the weight of an object and then have to increase force again until liftoff occurs (Fig. 6B, solid lines). These observations suggest that young children may not have the cognitive resources for accurate feedforward control.

In addition, very young children appear to be relatively inefficient at integrating sensory information into sensorimotor programs. In precision lifting, people start to increase grip force and load force soon after the digits contact the object. Signals from tactile afferents related to object contact trigger the next phase of the lift. In very young children, there is a

Figure 7 Ontogenetic development of the coordination of grip and load forces during precision lifting. (A) Grip force, load force, and grip force rate as a function of time during several consecutive trials (superimposed) for individual children of various ages and an adult. Note the large variability and excessive grip forces used by young children compared to the adults. (B) Relationship between grip force and load force during the initial parts of lifting trials by children of various ages and an adult. Note the nonparallel increase in grip and load forces for young children compared to adults. (A and B) Surface material and object's weight are constant (adapted with permission from Forssberg, H., Eliasson, A. C., Kinoshita, H., Johansson, R. S., and Westling, G., Exp. Brain Res. 85,451-457, 1991. Copyright © 1991 by Springer-Verlag).

Figure 7 Ontogenetic development of the coordination of grip and load forces during precision lifting. (A) Grip force, load force, and grip force rate as a function of time during several consecutive trials (superimposed) for individual children of various ages and an adult. Note the large variability and excessive grip forces used by young children compared to the adults. (B) Relationship between grip force and load force during the initial parts of lifting trials by children of various ages and an adult. Note the nonparallel increase in grip and load forces for young children compared to adults. (A and B) Surface material and object's weight are constant (adapted with permission from Forssberg, H., Eliasson, A. C., Kinoshita, H., Johansson, R. S., and Westling, G., Exp. Brain Res. 85,451-457, 1991. Copyright © 1991 by Springer-Verlag).

relatively long delay between initial contact and the onset of increases in grip and load force. This long delay indicates immature control of hand closure and inefficient triggering of the motor commands by cutaneous afferents. The decrease in this delay during subsequent years parallels a maturation of cutaneous reflexes of the hand as assessed by electrophysiological methods.

During the latter part of the second year, children begin to use sensorimotor memory, obtained from previous lifts, for scaling forces in anticipation of object weight. However, adult-like lifting performance with precise control of the load force for smooth object acceleration does not appear until 6-8 years of age. At about 3 years of age, children start to use vision for weight estimation through size-weight associations for classes of related objects. Thus, additional cognitive development is apparently required before the necessary associative size-weight mapping can take place. Unlike adults, once children begin to use visual size cues, they are unable to suppress adequately their influence when the cues are misleading (i.e., in situations in which weight and size do not reliably covary). This observation is consistent with the view that vision has a particularly strong influence on motor coordination in children. Thus, the context-related selective suppression of visual cues appears to require even further cognitive development.

Young children display a limited capacity to adapt the ratio of grip force and load force to frictional conditions. These children use unnecessarily high grip forces in trials with high friction (or low slipperiness) and their behavior is reminiscent of that of adults with impaired digital sensibility. This increased grip force may be a strategy to compensate for immature tactile control of precision grip because overgripping will prevent slips when handling slippery objects. Nevertheless, even the youngest children (1-2 years) show some capacity to adjust grip force to friction if the frictional conditions are kept constant over several consecutive precision grip lifts. The need for repetitive lifts suggests a poor capacity to form sensorimotor memory related to friction and/or to use this memory to control force output. Older children require fewer lifts to update effectively their force coordination to new frictional conditions, and adults require only one lift.

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