Introduction

The large variety of neural and non-neural derivatives that arise from the neural crest raises the fundamental question of how cell fates become specified during its ontogeny. In other words, what is the relative influence of intrinsic cell commitment compared to cell–cell interactions in promoting differentiation of distinct cell types.

Neural crest cells have long been implicitly considered as forming a population of homogeneous pluripotent cells that become specified to distinct lineages only after the arrest of migration and homing to their final destinations. This view would imply that local signals at the sites of homing play an instructive role in determining the precise cell types that develop. This notion has challenged investigators in the field of neural crest development to search for the existence of a stem cell from which all derivatives would arise.

The extreme opposite view of the ontogeny of the neural crest is to assume that this structure arises as, or rapidly becomes, a sum of heterogeneous cell subsets already committed to differentiate along different phenotypes. This would mean that cell fate is lineage-determined. Consequently, progressive cell divisions would specify the fate of successive daughter cells by giving rise to limited sets of crest cells. Then, upon migration, different subsets of committed cells would be expected to arrive at distinct homing sites.

In the 15-year interval separating the first edition of The Neural Crest from the present book, our understanding of the ontogeny of this structure has progressed considerably. New derivatives of the neural crest have not been discovered but truly novel perspectives have illuminated the field. Considering the list of neural crest derivatives summarized in Table 8.1, one can only be overwhelmed by the impressive diversification of phenotypes arising from this discrete and transient embryonic structure and by its paramount participation to the vertebrate organism. By means of the PNS, the neural crest provides the body with an efficient communication system with the outside world, and within the organism itself. By means of pigment cells, the neural crest provides protection from UV light and a means of undergoing adaptative color changes. Furthermore, the neural crest has accommodated the large increase in brain size which took place during vertebrate evolution by providing it with the skull. Thus, it appears to be a highly adaptative structure and, as it is absent from their chordate ancestors, the neural crest can be considered as a “spectacular invention” of vertebrates as pointed out by Gans in 1987.

One is also incited to seek for common denominators between the highly diversified neural crest derivatives. Such a line of thinking is stimulated by the existence of congenital anomalies in which multisystem neural crest defects (neuronal and pigmentary, neuronal and craniofacial, neuronal and endocrine, etc.) are found to be associated. Molecules mutated in specific neurocristopathies have begun to be elucidated, and provide precious tools to tackle these links.

Nervous systems and the study of behaviour

People in antiquity seem to have had no idea that the brain was in any way connected with behaviour. Even that great practical biologist Aristotle was mistaken in his ideas. He observed the rich vascular supply of the brain and concluded that it was an organ for cooling the blood. The ancient Egyptians were positively cavalier in their attitude: when the body of a monarch was being prepared for mummification, the brain was extracted with a spoon and thrown away. The brain was considered unnecessary for the future life, but the entrails were carefully preserved in a jar and kept beside the mummified body.

Modern opinion emphasises the paramount importance of the brain as the source of an individual's behaviour and personality. This trend has gone so far that many a successful work of science fiction has been based on the idea that the brain might be kept alive or transplanted, and that by this means the essential personality of the original individual might be preserved after the rest of the body has been disposed of. This vast change in prevailing opinion about the brain is, of course, due to the anatomical and physiological research of the last 200 years, which has revealed the nature and importance of the central nervous system.

Our present understanding of the way in which nervous systems control animal behaviour owes much to a group of biologists working in the middle of the twentieth century, who pioneered an experimental approach to analysing behaviour.

Basic organisation of nerve cells

The very title of this chapter would have been contentious in the nineteenth century, when detailed scientific study of the nervous system got underway. For it was then not generally agreed that the nervous system is composed of many individual nerve cells. This was mainly due to the fact that nerve cells are difficult to visualise with routine histological methods. Many cells are packed tightly together in nervous tissue (there are 100000 nerve cells in 1mm3 of human brain) and they give off fine, branched processes, so that it is almost impossible to determine the limits of a single cell. Many scientists therefore believed that nerve cells were fused together in a continuous network of branched processes, rather like the capillary beds that link small arteries and veins.

The technique that was most powerful in challenging this view was silver staining, first discovered by Camillo Golgi in 1873 and developed by others, particularly Santiago Ramon y Cajal from 1888 onwards. Ramon y Cajal examined many parts of the nervous system in a wide range of animal species. He realised that the special feature of silver staining is that it only stains a small percentage of cells in a piece of tissue but it stains them in their entirety, so that the structure of an individual nerve cell can be described (Fig. 2.1). Nowadays, single neurons are often stained by the intracellular injection of dye through a microelectrode, or by the use of methods that recognise chemicals characteristically found in particular neurons.

Introduction

One of the most important, intriguing aspects of animal behaviour is that it continually changes. Some of the changes are parts of the processes of development and maturation, whereas others allow the animal to learn about alterations in its environment. Learning enables an animal to make and modify predictions based on experience, for example that a particular action will be followed by a rewarding or an aversive event. The ability to change is a fundamental property of many nerve cells and their interconnections, and much recent research has focused on events at the molecular and cellular level that could underlie learning or events during the development of a nervous system. A major challenge in neuroethology is to relate these changes in cellular properties to alterations in animal behaviour.

One type of trigger for changes in behaviour is provided by hormones, which can ensure that events are initiated at particular times. Steroid hormones act by regulating gene expression and can produce modifications in the morphology of nervous systems that are correlated with changes in behaviour (Breedlove, 1992; Weeks & Levine, 1995). Polypeptide hormones, on the other hand, often act to trigger particular behaviour patterns by exciting particular target neurons. Another type of mechanism triggers learning, in which an animal forms a new association between a sensory stimulus and a motor program.

Introduction

Most animals are active organisms and need up-to-date information about their environment if they are to behave appropriately. Much information is potentially available in the many forms of energy and chemicals that impinge on the surface of the organism and act as stimuli. An animal must be able to detect the various forms of energy and to sort them all out, a job that is carried out by its sense organs, which act as instruments monitoring stimuli coming in from the environment. Sense organs are thus an animal's mechanism for gathering up-to-date information, and as such it is hard to exaggerate their importance in behaviour.

Clearly, a monitoring instrument is useful only if it measures one particular form of stimulus; having an instrument that responded indiscriminately to all forms of stimuli would be nearly as uninformative as having no monitoring facility at all. Hence, one of the most fundamental properties of sense organs is selectivity. Each sense organ contains specific receptor cells that are tuned to be sensitive to one particular stimulus. In many sense organs, the receptor cells are also nerve cells, having axons that convey their information to the central nervous system, and receptor cells of this kind are, therefore, often called sensory neurons. In other sense organs, such as the eyes of vertebrates and insects, the receptor cells do not have long axons themselves but instead make synaptic contact with separate nerve cells that send trains of spikes to the central nervous system.

Our aim in this book is to introduce university students to research on nervous systems that is directly relevant to animal behaviour, and to do so at a level that assumes no detailed knowledge of neurophysiology. Many topics that fall within the scope of neurobiology are omitted or passed over lightly, and attention is concentrated on particular examples that illustrate clearly how the activity of nerve cells is linked with animal behaviour. Since the first edition was published, many new books on neurobiology have appeared, but most concentrate on the cellular and physiological aspects of the nervous system. By reviewing some of the modern stories in neuroethology, we hope that this book will also be useful to postgraduate students and others who wish to learn something of the way in which behaviour is controlled.

Each major topic in Chapters 3–9 is dealt with as far as possible by introducing a particular type of behaviour and then working towards a description of how nerve cells control it. We have selected subjects from studies in which the links between nerve cells and animal behaviour are particularly clear. In doing this,w e hope to illustrate the principles that have been revealed in modern research in neuroethology. Inevitably, there are many interesting stories that we have not been able to touch upon.

Readers who are familiar with the first edition of the book will notice several changes in content and arrangement. The final two chapters, on circuits of nerve cells and on plasticity in behaviour, are completely new.

Introduction

Sensory systems have evolved to provide information that is particularly relevant to an animal's way of life. Sensory neurons have modalities and receptive fields that are strongly biased in favour of gathering information that is behaviourally significant for that species. Whatever their bias, sense organs can pick up large amounts of information about an animal's environment: for example, the photoreceptors of an insect's eye provide a point-by-point representation of light levels in the surrounding visual environment. Higher-order neurons in a sensory system cope with all this information by discarding much of it and keeping only the most significant aspects. These neurons act essentially as filters, and transmit only certain aspects of the signal they receive. A consequence of this is that much of the information present at the level of the sensory receptors is thrown away.

Filtering is largely achieved by circuits, in which neurons interact with each other through their synaptic connections. As a result of these interactions, some features of the signal are enhanced and others are discarded at each level in a sensory system. This progressive refinement of the sensory signal begins at the very first synapse, between a sensory receptor and a second-order neuron. Generally, lower-order neurons respond to fairly simple characteristics of stimuli, such as changes in brightness. Higher-order neurons, on the other hand, often respond to particular patterns of stimuli in which information coming from particular groups of sensory receptors is combined together.

Introduction

There are very few instances in which complete neuronal pathways can be traced from the level of sense organs all the way to that of motor neurons. Notable exceptions are some startle behaviours like those described in Chapter 3, in which the size of the giant neurons involved makes experimental study relatively easy and in which the links between sensory processing and motor control are short. However, most of an animal's behavioural repertoire is not performed with the same urgency as escape movements. Much sensory analysis, particularly in visual and auditory pathways, involves several different stages, distributed over different regions of a brain. How are different sensory messages identified, and how are appropriate motor programs selected? The type of problem can be illustrated with a simple example. If a fly lands on your cheek, or if the skin of your knee itches, you can move your hand without thinking to those locations to remove the source of annoyance. This might seem like a trivial example of behaviour, but the neuronal mechanisms that allow us to perform such an act are far from being understood. It is relatively straightforward to map the locations of sensory receptors in the skin in an orderly manner within the brain, which generates a somatotopic map. However, it is not simple to generate the correct commands that will generate the correct balance of activation in different muscles of a jointed limb so that its end arrives at a specific location on the body surface.

Introduction

The interaction between a predator and its prey represents a dramatic example of animal behaviour in which the capabilities of nervous systems are stretched to the limit. A hunting animal faces the fundamental problems of detecting and localising the prey, and it must solve them on the basis of purely passive information given out inadvertently by the prey. This is a formidable task and it has led to the evolution of some remarkably sophisticated neuronal systems in species that are adapted for hunting.

If one is asked to name a hunting species, the natural choice is a suitably complex animal such as a large cat or a hawk. These animals do, indeed, possess central nervous systems with the necessary sophistication to handle the complex task of tracking prey, but this sophistication makes most birds and mammals unsuitable as subjects for neuroethological research. However, the difficulty can be overcome by looking at species with a highly specialised method of hunting, based on a sensory system that is dedicated to the specialised method of prey detection and localisation. It then becomes easier to correlate the properties of particular neurons in that system with the particular behavioural task (see section 1.2).

Such dedicated systems are found in two groups of animals that employ hearing as a means of tracking prey, namely owls and bats, which use specialised auditory systems to hunt at night when visually guided predators are at a disadvantage.

Introduction

When an animal is suddenly attacked by a predator, it must respond with great urgency if it is to escape. The neuronal circuits that initiate such an escape response must be both straightforward and reliable in order to fulfil their biological function. A staightforward circuit is essential to ensure speed in initiating the escape, and a reliable circuit is needed not only to make sure the response occurs when required but also to avoid false alarms. These qualities of simplicity and reliability, which are of great survival value to the animal, are also of service to the neuroethologist exploring the role that nerve cells play in behaviour. Consequently, several of these startle responses have been studied in detail and they provide valuable insight into the flow of information through the nervous system from sensory inputs to muscular output.

Furthermore, these neuronal circuits often involve neurons that are exceptionally large and, because of this, are called giant neurons. The function of giant neurons is to conduct spikes rapidly along the body, but their size also makes them readily accessible to study with microelectrodes. The giant neurons therefore offer a major opportunity to investigate the role of individual nerve cells in behaviour.

Two main functions must be carried out by the neuronal circuit that initiates any behaviour pattern, including escape. First of all, a decision to initiate an activity must be made at some point in the circuit.

Introduction

Understanding the mechanisms which generate and control locomotory movements is fundamental to a complete knowledge of the neuronal control of behaviour. We can regard locomotion, such as jumping, walking or flying, as basic building blocks for much of an animal's behavioural repertoire; and we can pose three basic questions about the control of such movements. First, what mechanisms ensure that muscles contract in the appropriate sequence? In walking, for example, the basic pattern is repeated flexion and then extension of each leg, with flexion of the left leg coinciding with extension of the right. Second, how does a nervous system select, initiate and terminate a particular type of movement? For example, what initiates the pattern of walking; and how is walking rather than running or swimming selected? Third, how is the basic pattern for movement modulated appropriately? Stride pattern changes, for example, when a person walks up a flight of steps or turns a corner.

Experimental approaches to these questions have often involved work on invertebrates and lower vertebrates, animals in which the parts of the nervous system that generate programs for movement contain a limited number of neurons. This offers the opportunity to identify and characterise all the components involved in generating a particular movement. A specific question that has occupied many investigators is how to determine the source of rhythmical activity that underlies many regularly repeated movements, such as walking or flying.

Development of Startle Modification by Lead Stimulation

Background from Adult Studies

The magnitude of the startle-blink reflex in the human adult can be modified by nonstartling lead stimulation in at least three ways (Graham, 1975; Anthony, 1985).