SUMMARY

Recent data from research on spatial learning mechanisms with the water maze are discussed, with emphasis on the role of NMDA receptor-dependent long-term potentiation (LTP). Detailed analysis of behavior in the water maze has indicated a need to distinguish among different components of this seemingly simple task. Nonspatial pretraining allows for the separation of behavioral strategy learning and learning the spatial location of the hidden platform. Nonspatially pretrained rats can learn the location of a hidden platform as quickly as controls despite being treated with any of a variety of pharmacologic agents. When a water maze task of conventional difficulty is used, nonspatially pretrained rats given an NMDA receptor antagonist to block hippocampal LTP can learn the location of the hidden platform as quickly as controls. When an especially difficult water maze task is used, involving repeated one-trial learning with repeated reversal learning, blockade of hippocampal LTP produces a spatial memory impairment for long but not short retention intervals in nonspatially pretrained rats. These and other experiments point to an important issue of task difficulty in the research. It should prove useful to systematically vary experimental treatments and task difficulty as a means of identifying specific brain circuits that are important for specific components of the water maze or other tasks. This information can then be used to further evaluate the role of LTP in the learning.

Introduction

Long-term potentiation (LTP) has properties of central nervous system change that are inherently interesting and that could be relevant to a variety of behavioral phenomena. Chief among these is its relevance to systematic and enduring behavioral change, or learning and memory.

SUMMARY

This chapter begins with a brief discussion of the complexity of the long-term potentiation (LTP)-memory debate. We suggest that the notion of LTP as a unitary “memory encoding device” is too simplistic to survive rigorous experimentation and debate. However, while there are difficulties in making the direct connection between LTP and memory, we have not abandoned the proposition that LTP studies can enhance our understanding of the physiology of memory. The primary focus of this chapter is to incorporate studies on LTP, memory, and stress into a synthesis on the dynamics of emotional memory storage in the hippocampus and amygdala. The work is based on the idea that the induction or blockade of LTP can serve as a “diagnostic” measure of how stress affects information processing by different brain structures. The synthesis provides a novel perspective on why the characteristics of nonemotional memories differ from the pathologically intense, and fragmented, characteristics of traumatic memories.

Introduction

Long-term potentiation (LTP) has long been embraced as a model of memory because its characteristics are consistent with models of synaptic storage mechanisms and it has features in common with learning and memory. Just as memory is a lasting trace formed as a result of a brief experience, LTP is a lasting enhancement of synaptic efficacy produced by brief electrical stimulation. Initially, the field was buoyed by repeated findings of commonalities between LTP and memory. The early work showed, for example, that drugs that blocked hippocampal LTP impaired hippocampal-dependent learning, and that LTP, as with memory, was impaired in old animals.

Introduction

Apart from our curiosity about the mechanisms underlying neurite extension and growth cone motility, understanding the cytoskeleton in growth cones is important because it is the ‘final common path’ of action of extrinsic guidance cues (reviewed in: Letourneau & Cypher, 1991; Strittmatter & Fishman, 1991; O'Connor & Bentley, 1993; Bentley & O'Connor, 1994; Lin, Thompson & Forscher, 1994; Tanaka & Sabry, 1995; Challacombe, Snow & Letourneau, 1996a; Letourneau, 1996). Broadly speaking, neurite extension depends upon the integrity of microtubules whereas, in common with motile events in other cell types, the motility of the growth cone, the extension and retraction of filopodia and lamellipodia, is supported by actin microfilaments. Pathfinding, the ability of the growth cone to navigate a route through the embryo to its target cell (see Chapter 3), depends on both of these parts of the cytoskeleton and their associated proteins.

Neurite extension is a special case of cellular motility. When a flbroblast or other motile cell in culture migrates across a substratum it extends a cellular process (lamellipodium) at the leading edge of the cell which attaches to the substratum so that, following traction, the entire cell including the nucleus, can move forward (Bray, 1992). Although there are similarities between neurite extension and cellular translocation, there are two important differences.

Offspring care or parental/maternal behaviour has received scant coverage in most books on motivation. This activity is manifested mainly by the mother, but in some species the father also engages in caregiving behaviour. Pryce (1992) defined maternal motivation as ‘a female's tendency to make infants the goal of her behaviour where that behaviour can be described as promoting infant well-being’. This topic, if considered in motivation books, is often subsumed in the chapter on sexual activities and sometimes in the discussion on social attachment. Why should parental behaviour deserve more interest and attention? This activity ensures the survival of offspring and thereby enhances the parents’ reproductive success. In most mammalian species active copulators who are unconcerned with the product or outcome of their mating activities may not leave many survivors to continue their genetic line. However, there is variation in the prevalence of parental behaviour among species. Wilson (1975, p. 168) declared that ‘the pattern of parental care is a biological trait like any other; it is genetically programmed and varies from one species to the next. Whether any care is given in the first place and what kind and for how long are details that can distinguish species as surely as diagnostic anatomical traits used by taxonomists’.

The extent of parental care varies and is partly related to the complexity of the organism. Many aquatic invertebrates simply shed their eggs and sperm into the water and leave the embryos, arising from the consequent union, to fend for themselves. In contrast, caring for one's offspring is widespread among birds and mammals.

MOTIVATION AND FITNESS

I trust that, after studying the material presented up to this point, the reader has a fair idea about the various factors underlying such motivated behavioural activities as mating, parental care, feeding, food selection, drinking, stimulus seeking and defensive or agonistic reactions. The material in the preceding chapters indicate that although the response patterns may differ, these motivated acts have one important feature in common. They are terminated when an end-point corresponding to a goal is achieved. The concept of fitness was discussed in the early part of this book with the presumption that organisms have evolved in such a way to maximise fitness. I discussed how evolutionary processes may have selected mechanisms that result in a particular behaviour. From this perspective, the functional significance of any aspect of behaviour is seen in terms of fitness maximisation or the chances it gives to the perpetuation of the organism's genes. The functional significance of mating behaviour is obvious, even though it may not directly enhance the survival of the individual. Although a motivated act such as feeding contributes directly to the survival chances of the individual, it does so through its contribution to the chances of gene perpetuation. The traditional distinction made between activities such as feeding, drinking or attacking and activities concerned with gene perpetuation such as sexual behaviour is unwarranted. All behaviour has been affected by evolutionary processes with consequences on fitness.

In discussing sexual selection, I presented material indicating that sexual dimorphism and sexual behaviour may decrease an individual's survival even though such attributes increase the chance of gene perpetuation.

What are growth cones?

Of all animal cells, neurons have the most diverse and remarkable shapes. They vary in appearance from the simple, unipolar cells of invertebrate ganglia to the highly complex pyramidal cells of the human cerebral cortex with their profusion of processes and thousands of synapses. The basis for this diversity of shape is the ability of developing neurons to produce long and branching cellular processess, of which two distinct kinds are recognised: axons and dendrites. In mature neurons, axons convey action potentials away from the neuronal cell body, or soma, to the axon terminals, whereas dendrites transmit information toward the soma. Primary sensory neurons form an exception to this general rule since they have an axon which conveys action potentials towards the cell body. Axons and dendrites, collectively referred to as neurites when they are growing, are necessary for neurons to carry out their primary function, in which they have no equal, that of intercellular communication. In the central nervous system (brain and spinal cord), neurons usually communicate with each other, whereas in the peripheral nervous system they also communicate with a variety of effector cells such as muscle and secretory cells. In the adult, the distance over which the neuron must sustain its cellular processes to communicate with another cell may be considerable; it is many metres in the case of pyramidal motoneurons in large mammals such as the whale.

Most of the literature in psychology and physiology that deals with feeding in animals and humans focuses on hunger or how much is eaten (the regulation of food intake) rather than what is eaten (the selection of foods). Motivation textbooks rarely elaborate on the determinants of food selection, and if they do, such discussions occur in the section on hunger. The fact that food habits are used in the naming of higher-level taxonomic groups (e.g. carnivores, herbivores or omnivores, etc.) supports the notion that food selection is a major force in evolution. The prominence of food selections in our daily life is also evident amongst humans. If animals and humans are to survive and reproduce in their environments, they must find and eat foods that provide all the nutrients necessary for self-maintenance and reproduction, as well as to avoid eating lethal amounts of toxic plants or animals that they encounter.

This chapter describes and discusses the mechanisms that explain how animals and humans manage to discriminate foods containing needed nutrients from ingestible sources that are either valueless or dangerous to eat. The other major issue concerns the tendency amongst humans to be selective in their acceptance of a small subset of many edible items that are available to them. Explanations of these two major issues will be accomplished by a discussion of built-in ‘hardware and software programmes’ cognitive or learning processes and socio-cultural factors (mainly in humans) which are responsible for the choice of foods.

I wrote this book as a text for intermediate and advanced level courses in motivation, and as supplementary material for courses on comparative psychology and biopsychology. Although there may be overlap with material in other current textbooks on motivation, the approach and treatment taken in this one is quite different. It does not present an exhaustive review of facts and anthology of theories in the field, but instead, attempts to cover selected material linked in a coherent fashion. In doing so I have attempted to make some sense of the diverse range of topics that are covered in other motivation texts. I have also attempted to indicate the interplay of material on animal and human research, and hope that the reader will find the presentation a natural one in which the transition between the two appears unforced.

The organisation of each of the substantive chapters begins with a consideration of ‘classic’ theories and studies of a specific motivated activity, and is followed by discussion of selected current developments indicating further complexities of the issue. Even though some earlier theories have been superseded by recent models, like Mook (1996), I believe that students will benefit from such exposure, and consequently, develop a better understanding of how current models and research evolved. Shortly after I had completed this book, I encountered others offering new insights that were not available during my preparation. Within the limited time remaining for the production of this book, I have attempted to fine-tune some of my presentation with some ideas that I have learned from these new works.

Until recently most psychologists studying reproductive behaviour focused on proximate causal mechanisms and paid scant attention to issues concerning the functional aspects of such behaviour. There are some outstanding exceptions. Although Donald Hebb is best remembered for his seminal work on physiological models of learning, memory and other cognitive processes, his views on evolution and behaviour also revealed foresight in the following statement. ‘The function of behavior in evolution is simply to keep an animal alive and well enough to mate and in other ways to get the next generation established, the process then repeating itself and leading to still another generation’ (Hebb, 1972, p. 171). Few psychologists during that era considered ultimate causal mechanisms in their theoretical analysis aside from short passing reference to the significance of evolutionary factors in the explanation of behaviour. They seldom ventured beyond that level. Textbooks on the psychology of motivation with an experimental emphasis tended to focus on proximate causal mechanisms underlying rat behaviour (Beck, 1978; 1990; Bindra, 1959; Bolles, 1967; Brown, 1961; Hall, 1961; Young, 1961).

Following the publication of E. O. Wilson's Sociobiology: the new synthesis (1975) and R. Dawkins' The selfish gene (1976), a new group of psychologists were inspired by the implications of evolutionary factors to the explanation of motivational processes. This ‘new generation’ of behavioural scientists which include Buss (1989, 1999), Cosmides & Tooby (1987; 1992; 1995), Daly & Wilson (1983; 1988; 1994) and Symons (1979) have reconceptualised motivational analysis through their incorporation of evolutionary theory.

Observations of animals placed into an unfamiliar environment indicate that they display a characteristic pattern of behaviour which suggests exploration. They typically move throughout the physical space and enter many parts of it. If unfamiliar objects are present in this environment, the animals may approach these objects and make physical contact with them. These actions are characteristic of stimulus seeking behaviour ‘which serves to acquaint the animal with the topography of the surroundings included in the range’ (Shillito, 1963). Such behaviour in which the animal familiarises itself with its environment may serve an adaptive role. By doing so, the animal acquires information that is potentially useful, such as discovering potential food sources and escape routes. The phenomenon is manifested in all mammals. The notion that familiarity of the environment assists solutions to problems encountered later is also relevant to humans using the World Wide Web. Users who surf the Web without any particular goal acquire information which may become useful to them in later contexts (Seltzer, 1998).

Russell (1983) suggested that there is more to be gained from immediate exploration of a new environment than from not exploring, and thus regards the former as an adaptive strategy. Not exploring would lay an animal open to the hazards of an unknown environment. In social animals such as the rat, exploration may also have the goal of establishing contact with conspecifics. This is often the case when the animal has been removed from a group for testing (Suarez & Gallup, 1985).

WHY THIS BOOK?

This book is concerned with the analysis of motivated behaviour from a biological perspective. Although some psychology students may find biological topics less to their personal tastes than material that is specifically human-oriented with a social emphasis, I hope that they may be pleasantly surprised by the material in this book. It is possible to link these topics and it has been attempted in a third year undergraduate Motivation course which I taught from such a perspective at the University of British Columbia, Canada, for over 30 years. The encouraging reactions of these students during lectures and in their course ratings has motivated me to share some of this material with you.

Texts by Colgan (1989) and Toates (1986) have focused on some issues in animal motivation which form the corpus of the present book, but these earlier books were relatively short and very selective in their coverage. Although this book adopts a conceptual framework similar to that developed in the Colgan and Toates books, it is less restrictive and thus appropriate for a broader based Motivation course. Most of the recent texts on motivation (e.g. Franken, 1994; Mook, 1996; Petri, 1996) are expansive, eclectic and almost encyclopaedic in their coverage of topics. Although the framework of this book is derived from the animal motivation tradition, it can also be used to analyse relevant issues in human motivation. Thus this work sits between the larger omnibus motivation texts and the smaller ones that focus specifically on animal motivation.

Almost every text devotes a chapter, or at least a section of one to the history of motivation, and then lists various definitions of this concept by different theorists.

If I had known how long it would take me to write this monograph on neuronal growth cones for Cambridge University Press, I would never have started it! I agreed to do so over seven years ago at a time when the task seemed considerably less daunting than it would be if I were starting now. However, as the years passed and the annual rate of publication of papers on growth cones became exponential, I began to feel I was facing a Herculean task. Of course, I did manage to get in a few games of tennis between writing chapters. I have tried to cover all topics concerning growth cones with the exception of regeneration, and I hope that the book is useful to both those entering the field and those who already work in it.

Introduction

It has been realised for over a century that growth cones can navigate precise routes through the developing embryo to locate an appropriate cell with which to form a synapse (Ramón y Cajal, 1892). Growth cone navigation is generally known as ‘pathfinding’. Growth cone pathfinding has attracted considerable attention, both because of its importance in the formation of a properly connected, and therefore properly functioning, nervous system and because it is one of the most remarkable examples of cellular morphogenesis (for reviews see: Dodd & Jessell, 1988; Bixby & Harris, 1991; Hynes & Lander, 1992; Goodman & Shatz, 1993; Culotti, 1994; Tessier-Lavigne, 1994; Goodman, 1996; Goodman & Tessier-Lavigne, 1997). The distances over which growth cones must navigate in the embryo are usually relatively short, of the order of hundreds of micrometres (see ‘Demonstration of chemotropic factors in vitro’ below). Despite this, the navigational task facing growth cones is rarely simply a matter of following a straight path of least resistance; there may be many places along the route at which the growth cone must make large steering manoeuvres to locate the correct path.