In the previous chapter, Hogan discussed the concept of behaviour systems (cf. Hogan, 1988). In a development of earlier suggestions by Kruijt (1964), Hogan has proposed that behavioural ontogeny involves the development of various kinds of perceptual, motor, and central mechanisms and the formation of connections among them. In this chapter, I evaluate some of the ways in which the neural substrates of developing behavioural mechanisms have been investigated. The chapter is divided into two main parts. First, research aimed at discovering neural localisation of function is discussed, and I provide a brief review of some of the plastic changes at the neuronal level that have been found to occur during the development of specific perceptual mechanisms. In the second half of the chapter, I show how the analysis of neural mechanisms of behaviour can be important for understanding the causal organisation of behaviour during development. That is, neurobiological interventions may enable us to distinguish between, and independently manipulate, different behavioural mechanisms. I discuss a number of different techniques and evaluate what conclusions can be drawn from them as to the organisation of behaviour. We shall see that the results of this research often lead to a further behavioural analysis of perceptual mechanisms. Specific examples are taken mainly from research into the perceptual mechanisms involved in filial imprinting and song learning in birds. As Hogan observes in Chapter 10, in contrast to motor mechanisms, the development of perceptual mechanisms is often dependent on functional experience.

This chapter is concerned with the development of interactions between mammalian mothers and their infants, especially rat and human mothers and their young. We first consider the hormonal and experiential factors that determine the mother's earliest responses to her newborn. We then focus on the infant and the events that control and guide its changing responses to its early social and physical environment. Throughout, we emphasize the ways in which the behavior of the mother and infant are complementary and mutually dependent, and are based on experiences acquired during the interaction.

As an example of complementarity between mother and infant, consider maternal retrieving behavior. When leaving the nest to retrieve her young, the female moves slowly in a low body position along a seemingly random path until she reaches her hidden pup. At that time, she lifts the pup by the nape of the neck, turns directly to the nest, and with head held high, she returns directly to the nest in a canter-like motion keeping the pup well above the substrate. For their part, the pups become limp and offer no resistance to movement when picked up by the scruff of the neck by dams (or by sharp, tooth-like tweezers by experimenters, Brewster & Leon, 1980). Lifting pups by other parts of the body causes them to twist and squirm. On such occasions that we have seen mothers hastily retrieve pups by parts other than the nape of the neck, the pups were dragged along the substrate.

During development, factors in the animal combine with its ‘experiences’ to produce a functioning adult. When it comes to analyzing what those experiences are and how they have their effects, one immediately confronts basic questions about learning. Are any or all of the effects of experience in development fundamentally different in some way from ‘learning’? What should we include as learning anyway? Are the effects of discrete, welldefined experiences on adults relevant to understanding the role of experience in development? Can we answer all these questions simply by postulating different kinds of learning?

Historically, learning has been studied from two different perspectives. In psychology, interest in learning stems from the philosophical background of associationism. The enduring appeal of the notion that all behavior and mental life are built up of simple associations is evident in the contemporary interest in connectionist modelling (cf. McLaren, this volume). The biological or more functional approach, in contrast, sees learning as part of the animal's adaptation to its environment, without making assumptions about the form that learning might take. To psychologists, the biological approach seems atheoretical and insufficiently general; to zoologists or developmentalists wanting to understand how particular animals develop in their niches, the psychologists' study of learning in the laboratory seems artificial and irrelevant. Psychologists' attempts to synthesize learning theory and the analysis of phenomena like imprinting that were discovered in a developmental context (e.g. Hoffman & Ratner, 1973) have usually seemed forced and unconvincing.

Bird song and sexual imprinting in birds are ideal systems for studying behavioural development, as we have seen already (DeVoogd, Bischof, this volume). They are also ideal systems to compare because of the many parallels between them (see also ten Cate, this volume). In this chapter I compare aspects of song learning and sexual imprinting in birds to show how the relationship between them contributes to our general understanding of how behavioural processes interact during development. I shall focus on the importance of social interactions for both song learning and sexual imprinting, discussing the circumstances under which social interactions can override two key features of imprinting-like processes, namely sensitive phases and stability, and describing some experiments that demonstrate which features of social interaction seem to be important (see ten Cate, this volume; Bolhuis, 1991, for the role of social interaction in filial imprinting). Finally, I shall adopt an interdisciplinary approach by linking the behaviour with its underlying neural substrate. An understanding of the role social interaction plays in learning and memory is important for two reasons: it contributes towards our general understanding of the complex process of behavioural development, and may help to elucidate the fascinating problem of how memory is stored and processed in the brain.

Sexual imprinting

Although the extraordinary phenomenon of newly hatched precocial birds following humans and subsequently developing sexual preferences for them had been described long before, the term imprinting, or ‘Prägung’, was popularised by Konrad Lorenz (1935), who drew attention to its biological significance.

Intraspecific communication is of crucial importance for survival and reproduction in the majority of animal species. Much of this communication takes place by means of ‘displays’, conspicuous, stereotyped and species-specific postures, movements and vocalizations that are specifically adapted to serve as a signal to another member of the species (cf. Tinbergen, 1952). Because of these characteristics, social displays provide interesting material for the study of behavioural development. First, displays are especially suitable for the study of the development of complex stereotyped motor patterns that may be influenced by social experience. Second, the study of display development can provide a better understanding of the ontogeny of social behaviour in general and of the immediate causation of adult social behaviour (Kruijt, 1964). Third, displays are believed to be derived in the course of evolution from intention movements (such as to flee, to attack, to preen) as a result of ritualization and emancipation (Tinbergen, 1952; see below). Because phylogeny is modified ontogeny, changes in ontogeny may reflect changes that have occurred in evolution. Consequently, the study of the ontogeny of displays may also provide insight into the evolution of displays.

Despite these interesting properties of displays, their ontogeny has hardly been analysed quantitatively. A notable exception is the development of bird song. Because of its relation to learning, the discovery of the neural systems involved in song, and the possibility of manipulating feedback by deafening the bird, the study of bird song has become one of the most flourishing fields in ethology.

Young organisms cannot do many of the things that adults can, and some of these things are cognitive in nature. Very young humans cannot understand or produce speech very well. Young animals cannot recognize predators or collect food at the adult level of proficiency. Young humans, however, develop the ability to understand and produce speech at a rate that is scarcely believable, and young animals can learn to forage and avoid predators, as well as form social attachments, learn to communicate, and learn to orient themselves in the world, sometimes by means that are not available to adults. This chapter offers a highly selective review of cognitive development in animals, concentrating on a few questions. The two fundamental questions are, do animals have ‘cognitions’, and do they change ontogenetically? The next question concerns the nature of cognitive development. Cognitive development clearly involves a multitude of changes in behaviour and the nervous system. This discussion will emphasize that there is an important difference between the acquisition of information by naive animals and developmental change in cognitive mechanisms. Several examples, drawn from foraging, aversion learning, and spatial behaviour illustrate this distinction, and allow for some discussion in passing of developmental changes in the brain that are correlated with cognitive development.

I begin this chapter with a brief discussion of what I mean by a behavior system, and then use the dustbathing, hunger, aggression, and sex systems of chickens to illustrate how such systems develop. Using these examples plus comparable information from investigations of mammalian behavior, I next consider the questions of whether there are any general differences between the development of perceptual and motor mechanisms and between social and non-social behavior systems. In the context of social behavior systems, I review some ways in which early experience can have far-reaching effects. Finally, I look at the development of interactions among behavior systems, and ask whether any new principles are necessary to understand this complex process.

Behavior systems

A definition of a behavior system and its components is given in Chapter 1, and a depiction of the concept is presented there in Figure 1.1 (p. 6). A more extensive discussion of this concept and many of the other issues considered in this chapter can be found in Hogan (1988). In brief, a behavior system consists of an organization of its components: perceptual, motor, and central behavior mechanisms. Each of these components is also organized. The study of development comprises: (1) describing the changes in both the organization of the components themselves and the organization of the system as whole (i.e. the connections among the behavior mechanisms), and (2) investigating the causes of those changes.

Avian song has received extensive attention, both as a natural behavior that is easily studied and can be related to ecology or to principles of natural selection, and as a neuroethological preparation in which it is possible to determine the neural basis for a complex motor activity in a vertebrate. This chapter is a survey of some of the central findings in both domains. It concentrates on the development of song and of brain regions that are responsible for song. It attempts to relate the behavioral and neurobiological findings in this system to more general issues of the nature of early perceptual and motor development and juvenile learning. In addition, it attempts to extend ideas on behavioral development to the neurobiological substrate for this behavior.

Overview of singing behavior

Acquisition of song – the perceptual phase

Several key findings are central to understanding avian song acquisition and performance. First, many features of song are learned. Thus, for example, many of the sounds comprising a canary's song closely resemble songs heard by the bird as a juvenile, and are distinct from sounds produced by other canaries (Marler & Waser, 1977, Waser & Marler, 1977). Zebra finches form a song by splicing elements of the songs of several individuals that they heard as juveniles, apparently favoring adults which had fed or interacted with them (Williams, 1990a). Similarly, nightingales form an elaborate song repertoire by acquiring and retaining ‘packages’ of sounds as a juvenile (Hultsch & Todt, 1989b), and swamp sparrows form a song by selecting from songs heard when young (Marler & Peters, 1988a).

I still recall a pronouncement from my earliest days of graduate training in linguistics that ‘phonemes are the building blocks of language’. I have forgotten who said it – possibly a number of linguists issued similar pronouncements and I am only recollecting a composite. In any case, the statement is believed by many individuals who study language. In this chapter I shall show that the phoneme is not the elemental unit best suited for understanding the development of spoken language.

The term phoneme refers to the smallest difference that can differentiate two spoken words. In English, /p/ and /t/ are phonemes because they distinguish ‘pie’ from ‘tie’, /s/ and /z/ are phonemes because they distinguish ‘hiss’ from ‘his’. It makes intuitive sense to suppose that these sound units are in fact the building blocks of language because words and grammatical markers are made of such sounds, and phrases and sentences are made of words. But this logic serves us poorly if our intent is to understand what human developments produce linguistic capacity and determine the form of linguistic behaviors. These are ontogenetic questions, and in asking them our concern cannot reside with elemental units of a behavior not yet acquired. Rather, we must concentrate on developmental mechanisms which facilitate or enable behaviors that – as the human child ultimately discovers – are decomposable into those units. From a developmental perspective, then, the phoneme is unavoidably a posteriori and therefore incapable of building any of the child's earlier behaviors.

There is now a considerable literature concerning the phenomenon known as sexual imprinting and the mechanisms underlying it (for reviews see Bateson, 1966; Immelmann and Suomi, 1981; Kruijt, 1985), However, recent findings by Immelmann, Lassek, Pröve & Bischof (1991) and by Kruijt & Meeuwissen (1991) suggest that earlier concepts of imprintinglike learning have to be revised. In this chapter I will analyse this new evidence and discuss its implications for some of the presumed characteristics of imprinting, such as the existence of a sensitive period and the stability of preferences. Further, I will consider some important questions such as stimulus selection and the reasons for stability of preferences. Many of the ideas I will present here are speculative and have little experimental backing. However, they may help us discard some of the old ideas concerning imprinting and so allow for the generation of new ones.

I will start with a brief description of the findings which prompted this chapter. Then I will propose an interpretation of these findings in terms of a two-stage process. The period in early development where information about the appearance of the parents is stored is called ‘acquisition phase’ here. Subsequently, there is a ‘consolidation process’ which takes place when the animal becomes sexually mature. In the final section of this chapter, I summarize the main features of the two-stage process and try to evaluate how the ideas presented here can be generalized to other learning paradigms.

This chapter is concerned with mental representations, and their development by learning via association. By representation, I mean to imply structures that permit recognition and identification of a stimulus without necessarily entering the conceptual domain. I hope to show that associative mechanisms can construct and employ representations of this type in such a way as to permit explanation of phenomena such as latent inhibition, perceptual learning, and the trade-off between context-specificity and generalisation. To this end, an outline model of associative learning, that concerns itself with the formation of associations between elements representing motivationally neutral stimuli, is developed in the course of the chapter. The emphasis, however, will be on the representational assumptions contained within the model and their consequences. The chapter starts by examining an elemental approach to stimulus representation, which proves surprisingly powerful in an associative context. Nevertheless, there are drawbacks to an elemental approach, which the latter half of the chapter attempts to solve by invoking a configural modification of an elemental account.

Introduction

The modern concept of an association, and hence of an associative learning system, probably stems from the work of the British empiricists (e.g. Locke, Hume). At the heart of this approach is the essential idea that one stimulus can bring about some recollection of another by virtue of the fact that the two stimuli were associated at some time in the past.

ENDOCRINOLOGY JOURNALS

Acta Endocrinologica

Advances in Steroid Biochemistry and Pharmacology

Annual Review of Biochemistry

Annual Review of Physiology

Biology of Reproduction

Clinical Endocrinology

Endocrine Reviews

Endocrinology

Frontiers in Hormone Research

General and Comparative Endocrinology

Journal of Clinical Endocrinology and Metabolism

Journal of Endocrinology

Journal of Reproduction and Fertility

Journal of Steroid Biochemistry

Peptides

Physiological Reviews

Recent Progress in Hormone Research

Seminars in Reproductive Endocrinology

Steroids

Trends in Endocrinology and Metabolism

As pointed out in Chapter 1, the nervous, endocrine and immune systems interact in many ways. Damage to the brain or changes in neurotransmitter and neurohormone release alter immune responses and the chemical messengers released by the cells of the immune system can alter the activity of the nervous and endocrine systems (Smith and Blalock, 1986; Kordon and Bihoreau, 1989). This chapter begins with an overview of the cells of the immune system and their chemical messengers, the cytokines, and then discusses the immune functions of the thymus gland and its hormones. The functions of the cytokines in the immune response to antigens and in the development of blood cells are then summarized and the neuromodulatory effects of cytokines on the brain and neuroendocrine system are examined. This is followed by a discussion of the neural and endocrine regulation of the immune system and the hypothalamic integration of neural, endocrine and immune systems.

THE CELLS OF THE IMMUNE SYSTEM

The immune system consists of a number of different cell types, including the monocytes and macrophages, T lymphocytes (T cells), B lymphocytes (B cells), granulocytes and natural killer (NK) cells. The role of the immune system is to help maintain homeostasis in the body and its best known function is the protection of the body from foreign invaders such as bacteria and viruses and from abnormal cellular development as occurs in tumor cells. To do this, the immune system must be able to discriminate foreign (non-self) cells from the body's own cells (self). Almost all substances have regions called antigenic determinants or ‘epitopes’ which can stimulate an immune response.