Abstract: To investigate neural mechanisms of movement, physiologists have analyzed the activity of task-related neurons in behaving animals. The relative onset latencies of neural activity have been scrutinized for evidence of a functional hierarchy of sequentially recruited centers, but experiments reveal that activity changes occur largely in parallel. Neurons whose activity covaries with movement parameters have been sought for evidence of explicit coding of parameters such as active force, limb displacement, and behavioral set. Neurons with recognizable relations to the task are typically selected from a larger population, ignoring those cells with complex relations to the task and unmodulated cells. Selective interpretations are also used to support the notion that different motor regions perform different motor functions; again, current evidence suggests that units with similar properties are distributed over widely different regions.

These coding issues are reexamined for premotoneuronal (PreM) cells, whose correlational links with motoneurons are revealed by spike-triggered averages. PreM cells are recruited over long times relative to their target muscles; they show diverse response patterns relative to the muscle force they produce; functionally disparate PreM cells such as afferent fibers and descending corticomotoneuronal and rubromotoneuronal cells can exhibit similar patterns. Neural mechanisms have been further elucidated by neural network simulations of sensorimotor behavior; the pre-output hidden units typically show diverse response patterns in relation to their target units.

Abstract: This target article draws together two groups of experimental studies on the control of human movement through peripheral feedback and centrally generated signals of motor commands. First, during natural movement, feedback from muscle, joint, and cutaneous afferents changes; in human subjects these changes have reflex and kinesthetic consequences. Recent psychophysical and microneurographic evidence suggests that joint and even cutaneous afferents may have a proprioceptive role. Second, the role of centrally generated motor commands in the control of normal movements and movements following acute and chronic deafferentation is reviewed. There is increasing evidence that subjects can perceive their motor commands under various conditions, but that this is inadequate for normal movement; deficits in motor performance arise when the reliance on proprioceptive feedback is abolished either experimentally or because of pathology. During natural movement, the CNS appears to have access to functionally useful input from a range of peripheral receptors as well as from internally generated command signals. The unanswered questions that remain suggest a number of avenues for further research.

Abstract: It is increasingly clear that spinal reflex systems cannot be described in terms of simple and constant reflex actions. The extensive convergence of segmental and descending systems onto spinal interneurons suggests that spinal interneurons are not relay systems but rather form a crucial component in determining which muscles are activated during voluntary and reflex movements. The notion that descending systems simply modulate the gain of spinal interneuronal pathways has been tempered by the observation that spinal interneurons gate and distribute descending control to specific motoneurons. Spinal reflex systems are complex but current approaches will continue to provide insight into motor systems. During movement, several neural mechanisms act to reduce the functional complexity of motor systems by inhibiting some of the parallel reflex pathways available to segmental afferents and descending systems. The flexion reflex system is discussed as an example of the flexibility of spinal interneuron systems and as a useful conceptual construct. Examples are provided of the kinds of experiments that can be developed using current approaches to spinal interneuronal systems.

Abstract: The premise explored in this target article is that the function of the cerebellum is best understood in terms of the operation it performs across its structurally homogeneous subdivisions. The functional heterogeneity sometimes ascribed to these different regions reflects the multiplicity of functions subserved by the central targets receiving the outputs of different cerebellar regions. Recent studies from our own laboratory and others suggest that the functional unit of the cerebellum is the sagittal zone. It is hypothesized that the climbing fiber system produces a short-lasting modification in the gain of Purkinje cell responses to its other principal afferent input, the mossy fiber-granule cell-parallel fiber system. Because the climbing fiber inputs to sagittally aligned Purkinje cells can be activated under functionally specific conditions, these afferents could select populations of Purkinje neurons that would be most highly modulated by mossy fiber inputs responding to the same conditions. These operations may be critical for the on-line integration of inputs characterizing external target space with features of the intended movement, proprioceptive and kinesthetic cues, and the body image.

Abstract: Engineers use neural networks to control systems too complex for conventional engineering solutions. To examine the behavior of individual hidden units would defeat the purpose of this approach because it would be largely uninterpretable. Yet neurophysiologists spend their careers doing just that! Hidden units contain bits and scraps of signals that yield only arcane hints about network function and no information about how its individual units process signals. Most literature on single-unit recordings attests to this grim fact. On the other hand, knowing a system's function and describing it with elegant mathematics tell one very little about what to expect of interneuronal behavior. Examples of simple networks based on neurophysiology are taken from the oculomotor literature to suggest how single-unit interpretability might decrease with increasing task complexity. It is argued that trying to explain how any real neural network works on a cell-by-cell, reductionist basis is futile and we may have to be content with trying to understand the brain at higher levels of organization.

Commentaries submitted by the qualified professional readership of this journal will be considered for publication in a later issue as Continuing Commentary on these articles. Integrative overviews and syntheses are especially encouraged.

How does the nervous system control the equilibrium trajectory?

[EB] The classical monkey limb perturbation experiments of Bizzi et al. (1982; 1984) greatly influenced motor control studies. Their findings, as well as those of Asatryan and Feldman (1965) on the unloading of the human forearm, were in good agreement with Feldman's hypothesis that the nervous system controls limb movements not by programming EMG bursts or force pulses for the limb acceleration and deceleration, but by defining a new equilibrium of the “limb/external load” system. In their target article, however, Bizzi et al. reject the concrete neurophysiological mechanism proposed by Feldman for how the system's equilibrium position is controlled.

Alpha-lambda controversy. It is suggested by Bizzi et al. that the X model is a subset of the a model, because the former uses a concrete form of the relationship between joint angle, central control parameters, and the level of a activity. They also reject the necessity of a muscle invariant characteristic for an equilibrium point (EP) model and argue that “the reflex apparatus contributes in a modest way to force generation” (see, however, Gandevia & Burke, this issue).

Introduction

The region of the primate brain which shows the greatest extent of postnatal development is the cerebral cortex, with detectable changes occurring within the region in humans until the teenage years. Not unrelatedly, the cerebral cortex is also the region of the mammalian brain most susceptible to the effects of postnatal experience. While the exact role of cerebral cortex in psychological processes is still unclear, several authors have argued that extent of the cerebral cortex may be correlated with ‘intelligence’ across species (e.g. MacPhail, 1982). Thus, the main evolutionary development within the brain across mammals is the relative expansion of the area of cerebral cortex. For example, the area of the cortex in the cat is about 100 cm, whereas that of the human is about 2400 cm (24 times the size). This suggests that the extra cortex possessed by primates, and especially humans, is related to the higher cognitive functions they possess. The aim of this chapter is to describe some of the progressive and regressive events which occur during the postnatal development of the primate cortex, and to discuss how these neural developments may relate to advances in perceptual, attentional, and memory abilities in human infants.

Until recently, the study of the development of cognitive abilities such as attention, language, and object recognition had proceeded largely independently of any considerations of their neural concomitants. This lack of interest in the brain by cognitive developmentalists may be due to an implicit assumption that identifiable neural developments which correspond in time or age to a cognitive change may allow the inference that the cognitive change was caused by the maturation of a neural structure (see discussion in Johnson & Morton, 1991).

The title of this book, Causal Mechanisms of Behavioural Development, comprises four substantive words, all of which are relatively common in English. They are words that most speakers of the language, and certainly most scientists, would probably say they know the meaning of. Yet all four can be misleading for that very reason; all of these words are used in many different ways, and few people are actually aware of these differences. At the risk of seeming pedantic, I shall devote the first few pages of this book to a discussion of some distinctions that should make clear how we are using these words. Some of this discussion will tend to the philosophical, but I trust that most readers will find it useful for putting the subsequent chapters into a general perspective. I shall take each word in turn.

Cause

In his well-known article ‘On aims and methods of ethology’, Tinbergen (1963) stated that there are four kinds of questions one can ask about biological phenomena: causation, survival value, ontogeny, and evolution. These distinctions are important, and have had a great influence on students of animal behavior. However, as I have pointed out elsewhere (Hogan, 1984), these questions do not cover all the important aspects of behavior. A more general classification of questions can be derived from some distinctions made originally by Aristotle.

In discussing physics and metaphysics, Aristotle pointed out that one and the same thing could be described or explained in four different ways.

At birth, young animals are confronted with a variety of stimuli in various modalities. Individuals of precocial species, in particular, have to respond adequately within hours in order to survive. Altricial individuals may have more time available to explore the world around them, but eventually they face the same problem. Of course, the change in stimulation from before until after birth is not one from zero input to a bewildering complexity. Several senses can be stimulated before birth, and learning about features of the external world does occur before birth in both mammals and birds. Also, not all senses may be functioning at full strength at birth, making the increase in incoming stimulation less abrupt. Nevertheless, the task of making sense of the world is not an easy one. One may argue that parents may provide some guidance, but then this requires that the animal recognizes its parent, reducing, but not eliminating the problem. At the same time, ducklings, only a few hours after hatching, and fowl chicks a bit later will follow their mother as though they have known her for a long time; adult zebra finches will court conspecifics as though no other species has ever been around, and many songbirds will sing their father's song as though they had never been exposed to any other sound. However, in all these cases there is abundant evidence that interfering with normal rearing conditions of the birds may severely disrupt the natural outcome of the processes.

This book is dedicated to Jaap Kruijt. His pioneering approach to the study of the causal mechanisms of behavioural development has inspired many, as is obvious in many of the contributions to this volume. We have both had the pleasure of working with him, as postdoctoral fellow and as doctoral student, respectively. Chapters in this book were commissioned from a wide range of scientists interested in behavioural development. Some of these have been former students or colleagues of Jaap Kruijt, but many are workers in the field with interests and approaches that are compatible with the approach Kruijt has taken to development. Each author was asked to review a specific area of the field in such a way that we think almost all the important conceptual and empirical advances in the study of development have been covered in one chapter or another. A special feature of the approach taken here is that learning, as studied by experimental psychologists, is considered to be one process contributing to the development of the individual from conception to death. Learning is seen to play an important part in development in several chapters in the book, and the relation of learning to other developmental processes is discussed specifically in the last three.

We are grateful to Bob Lockhart and Rob Honey who have read several of the chapters in manuscript form and commented on them.

How do action patterns develop in early life? In this chapter, I examine the early development of patterns of action such as walking, hatching, feeding, and grooming. Such behavior patterns I consider to be instinctive or innate. Use of the terms instinct or innate has been strongly criticized by ethologists and comparative psychologists, for essentially two reasons, so I will begin with a few words to justify my use here.

The first criticism traditionally attacked the role of innate as a causal explanation for behavior (e.g. Dewey, 1918; Kuo, 1921; Beach, 1955; Lehrman, 1953, 1970; Hinde, 1968). Kruijt has condensed this criticism succinctly: ‘… for ontogenetic purposes, the term instinctive or innate can be said to be completely empty. No light at all is thrown on the nature of the factors underlying the development of instinctive behavior except for the fact that certain specific factors are not necessary’ (Kruijt, 1971, p. 10); and ‘the term innate does not invite one to ask causal questions about the ontogeny to its final consequences’ (Kruijt, 1964, p. 5).

The second criticism has attacked innate as a classification for behavior. If innate, or instinctive, is meant to refer to behavior that is absolutely predetermined by genotype, independent of experience, and unmodifiable by feedback, then no behavior can be found that qualifies. Instead, concerning this absolute sense of innate, the conclusion has prevailed that there might be said to exist only innate behavioral differences between individuals, if their developmental histories were identical yet their behavior differed (e.g. Jensen, 1961; Hinde, 1968, 1970; Bateson, 1991).

Unravelling the causal processes through which species-characteristic behaviour develops in the individual is one of the most important issues of ethology. This analysis is not only of purely theoretical interest, but has an applied value as well in the prevention and cure of behavioural disturbances. Jaap Kruijt's retirement at the end of the academic year 1992/93 concludes a period of almost 40 years in which he devoted himself to developing this branch of ethology within the framework of the Zoological Laboratory of the University at Groningen (The Netherlands). By focusing his research on relatively complex social behaviour and by strongly opposing the dichotomous classification of behaviour into innate and learned, Kruijt has rendered an internationally unique contribution to the study of behavioural development. This makes it worthwhile to dwell briefly upon some phases of his own ontogeny.

Jakob Pieter Kruijt was born in Amsterdam in 1928. In his boyhood he developed a strong interest in wildlife, influenced – like many of us – by the writings of two Dutch naturalists, E. Heimans and Jac. P. Thijsse, and also by participating in the activities of the Dutch Youth Association for Nature Study. This interest made him ripe for the study of biology, which he started in 1946 at the University of Utrecht. At that time zoological research in Utrecht was mainly concerned with laboratory work; comparative and developmental physiology were strongly represented.

The study of the role of experience during ontogeny provides an opportunity for testing the generality of existing principles of learning and may lead to the discovery of new ones. Developmental psychologists and learning theorists share an interest in how experience produces behavioral change, yet differences in the set of problems, methods, and levels of conceptualization traditionally employed have led to largely nonoverlapping areas of research (cf. Shettleworth, this volume). Nevertheless, the relationship between learning theory and behavioral development has been studied within both traditions. At one extreme is the notion that much of development can be explained by learning principles (Baer & Wright, 1975; Bijou & Baer, 1961; Gewirtz & Boyd, 1977; Watson, 1930; Holt, 1931; Skinner, 1953; Staats, 1975). At the other extreme is the suggestion that learning principles have contributed little to understanding behavioral development (e.g. Gottlieb, 1983).

There are two strategies for exploring the contributions of learning to behavioral development. One approach, not taken in this chapter, is to study animals of different ages in traditional learning experiments (Amsel, 1979; Spear, 1978; Johanson & Terry, 1988; Spear & Rudy, 1991). In so far as age-related differences in performance on a learning task can be attributed to changes in process, this strategy reveals the range of processes whereby experience might induce changes in behavior during development. For example, Rudy and his colleagues (Rudy, 1992) have suggested that young animals can learn about single events before they can learn about relationships between events during ontogeny.