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.

Peptide hormones, neuropeptides, neurotransmitters and other non-steroid chemical messengers stimulate biochemical activity by binding to receptors on the plasma membranes of their target cells. These chemical messengers cannot enter their target cells to stimulate the nucleus in the manner described for steroid and thyroid hormones in Chapter 9. In order to activate biochemical changes within the target cell, they act as first messengers to activate a second messenger, such as cyclic adenosine monophosphate (cyclic AMP), within the cytoplasm of the target cell. The transduction of information from the first to the second messenger is accomplished through the activation of membrane protein transducers (G-proteins) and enzymes, such as adenylate cyclase. This chapter examines the membrane receptors for peptide hormones and neurotransmitters, the mechanisms by which signal transduction across the cell membrane occurs, the role of G-proteins in this signal transduction, the second messenger systems activated, and the actions of the second messengers in the target cells, with special emphasis on neural target cells.

MEMBRANE RECEPTORS

The membrane receptors are complex glycoproteins embedded in the cell membrane. The function of these receptors is to recognize specific ligands in the blood (e.g. peptide hormones, neuropeptides) or in the synapse (e.g. neurotransmitters) and bind to them. Once this binding occurs, signal transduction across the cell membrane occurs as described in Section 10.2 below. Using a number of pharmacological and biochemical techniques employing radioactively labeled ligands, fluorescent dyes, affinity chromatography and immunochemical identification, it is possible to discover the location and structure of the membrane receptors (see Limbird, 1986; Yamamura, Enna and Kuhar, 1990).

HORMONES, THE BRAIN AND BEHAVIOR

Research on hormones and the brain covers many fields: from cell biology and genetics to anatomy, physiology, pharmacology, medicine and psychology. This book will examine the interactions between hormones, the brain and behavior. The main focus will be on how the endocrine and nervous systems form an integrated functional neuroendocrine system which influences physiological and behavioral responses.

When you hear the term ‘hormone’, you think of the endocrine glands and how their secretions influence physiological responses in the body. That is, however, merely the beginning of the picture. Many of the endocrine glands (although not all of them) are influenced by the pituitary gland, the so-called ‘master gland’, and the pituitary is itself controlled by various hormones from the hypothalamus, a part of the brain lying above the pituitary gland. The release of hypothalamic hormones is, in turn, regulated by neurotransmitters released from nerve cells in the brain. Neurotransmitters also control behavior and the release of neurotransmitters from certain nerve cells is modulated by the level of specific hormones in the circulation. Thus, neurotransmitter release influences both hormones and behavior and hormones influence the release of neurotransmitters. This interaction between hormones, the brain and behavior involves a wide variety of chemical messengers, which are described in this chapter.

This chapter provides an introduction to the chemical messengers found in the neuroendocrine system. Later chapters describe the endocrine glands and their hormones (Chapter 2), the pituitary gland and its hormones (Chapter 3) and the regulation of the pituitary gland by the hypothalamic hormones (Chapter 4).