Once, the late David Ingvar sent me an article with the title of this chapter for an issue of Human Neurobiology, which I was editing; the article was to be devoted to the prefrontal cortex. The flanking quotation marks barely mollified the brashness of the oxymoron. It took me some time to accept the title – and the article (Ingvar, 1985). Now, after more than two decades, I appreciate the profound wisdom of that expression, for it characterizes the most essential feature of the functions of the human prefrontal cortex: their future dimension. At the same time the expression alludes to the fact that the product of those functions consists of past memory transformed by imagination and projected to the future. Ingvar was a pioneer of functional neuroimaging in the human brain, one of the first to discover the activation of the prefrontal cortex in the mental planning of movements and language. Indeed, what he was trying to convey with his peculiar expression was the evidence that the prefrontal cortex is activated by the internal representation of prospective action. Surely, since the action was yet to occur, that representation could hardly be called “memory.” However, the insight of “future memory” becomes glaring when we consider that in our mind there is no planned or future action without the memory, by association, of similar actions in the past, by us or by others. Planning and decision-making consist in recreating old actions in new fashion.

October 2000, University of Paris, La Salpêtrière Hospital, Charcot Amphitheater. I was invited to give a short acceptance speech on a subject of my choosing after being awarded the Jean-Louis Signoret Prize. Determined to deliver it in French, I gave it an ambitious title: “Liberté et l’Exécutif du Cerveau.” In less than half an hour I tried to explain that the prefrontal cortex is the cerebral enabler of the human agenda. Further, that the achievement of biological and social goals is the outcome of the competition between demands of internal and external milieus continuously barraging that cortex. Further, that those demands include unconscious ethical imperatives in addition to instinctual urges. Of course, I dutifully cited Claude Bernard and Benjamin Constant. Human liberty, I concluded, is a phenomenon of the brain’s ability to choose, rationally or not, between alternatives of action.

Only after my talk did I realize I had overreached. I had spoken about a sacred French theme in less than perfect French to an intellectual French audience in an august French forum. Now, a dozen years past, this book is an attempt to say all those things better, in English.

What motivates this brain scientist to write about such a lofty theme as human liberty? And what qualifications does he have to do it? He surely must know that the terrain is fraught with pitfalls. Emphatically yes, he knows the dangers. No one has to convince him that those dangers are very real, especially the disdain, or, worse, the implacable wrath, with which modern neuroscience treats the unsuspecting defender of free will.

Summary

Left–right differences are too complex to be summarized by any simple dichotomy. In particular, interaction between the left and right hemispheres is crucial, with shifts in control reflecting collaboration, as well as bringing to bear the specializations of one rather than the other side. A major theme of this chapter is an attempt to show how specializations of one or other hemisphere interact with those of its partner. It has been argued that left hemisphere control is needed for assessment of a stimulus (e.g. assignment to a category) and for the subsequent selection of an appropriate response. However, initial detection of a stimulus is often made by the right hemisphere, owing to its ability to attend widely across panoramic space and to a wide range of properties of the stimulus. The left hemisphere may then intervene to control further assessment. At the same time, when a task is being performed, the left hemisphere is able to specify relevant properties of the stimulus, which are then used in searching for that stimulus using both the right and left hemispheres.

Introduction

Discussions of brain lateralization, understandably, often attempt to make simple summaries of its organization. We might say that we talk with the ‘left brain’ and are emotional with the ‘right brain’. The term ‘brain’ itself is inadequate here, as we will see when considering the roles of different structures; the term ‘hemisphere’ (i.e. cerebral hemisphere) is used when it is reasonably clear that forebrain structures are chiefly involved. Such terms are a necessary convenience for broad generalizations. Nevertheless, it is clear that, although shortened characterizations of right and left are unavoidable, at some points in discussions they should be treated with caution. An unexpected recent attempt at such characterization (Dien, 2008) is that the left hemisphere ‘anticipates multiple possible futures’, while the right hemisphere ‘integrates ongoing strands of information into a single view of the past’. Novel dichotomies such as this, however, have the merit of provoking new lines of thought.

Research on lateralization of brain and behaviour in animals has expanded rapidly over the past two decades and continues to grow exponentially. The same is true of studies on lateralization in humans, and the evidence from these two sources is integrated in this book in a way not previously attempted. We were motivated to write this book because of the widening interest in the subject and a perceived need to make the most up-to-date information available in a form that, we hope, is stimulating and easy to read. Since there are many general texts on cerebral specialization in humans, our chief focus was on left–right differences in brain and behaviour in non-human animals, with the aim of bringing together recent striking advances arising from study of lateralization in these species and the state of knowledge of lateralization in humans.

We approached the topic of lateralization from the perspective of Tinbergen’s four questions (function, evolution, development, causation), to each of which we have devoted one chapter.

Summary

This chapter considers potential applications of our knowledge about brain lateralization and some of the important questions for future research. First, it covers the potential to improve animal welfare by measuring lateralized behaviour. In doing so, it highlights the role of the right hemisphere in the expression of intense emotions and stress responses and extends this to consider unusual lateralization in humans. Then it outlines some of the areas important for future investigation of lateralization in animals and humans. The latter includes understanding of personality theory, thought processes, and formation and recall of memory. Lateralization in the different sensory systems and the interactions between the hemispheres in natural as well as laboratory contexts are important topics for further investigation.

Application of knowledge of lateralization

Now that lateralization has been established as a general characteristic of the vertebrate brain, it is worthwhile considering how this knowledge might be applied usefully to understanding animal behaviour and what lines of research are likely to be fruitful in the future.

Animal welfare

Can knowledge of lateral preferences be usefully applied to improving the welfare of animals? It seems very possible that continuous or exaggerated dependence on the right hemisphere occurs in animals suffering stress and that we might determine which animals are in this condition or which environments induce it by measuring eye, ear or nostril preferences. Although some studies have touched on this question, few have investigated it in any detail.

Summary

Once thought to be unique to the human brain, lateralization of structure and behaviour is now known to be widespread in vertebrates and, furthermore, it has a similar plan of organization in the different species. This chapter introduces the basic pattern of lateralization of vertebrate species and does so in a historical context to highlight the fact that, until some 20 years ago, it was widely and incorrectly assumed that having a lateralized brain was a mark of the cognitive superiority of humans. It also introduces some of the new evidence showing the presence of lateralization in invertebrate species.

Summary

Experience can enhance, suppress or change in other ways the development of lateralization. Exactly which of these occurs depends on the species, the nature of the experience and the stage of life at which it takes place. Lateralization of individuals and groups can be modulated by experience and by steroid hormones. The latter may be important in the development of sex differences in lateralization. Research in this area is in its infancy compared with our knowledge of species differences in lateralization, but we are able to give some potent examples to illustrate the importance of experience and hormone levels at particular stages of development.

Introduction

The brain is not as hard-wired as once thought. It changes its connections in response to experience, especially in early life but also in adulthood. Some regions of the brain even change size in response to specific kinds of experience. The hippocampus is such a region. In humans, we know that the hippocampus has a special role in spatial memory. A study of London taxi drivers has shown that they have a larger than average posterior region of the right hippocampus and a smaller than average anterior region of the hippocampus (Maguire et al., 2000). In animals too, the size of the hippocampus is related to spatial ability. Species that cache food and retrieve it at a later time have a larger hippocampus than do closely related non-caching species. This is known to be the case in squirrels (Johnson et al., 2010), kangaroo rats (Jacobs and Spencer, 1994) and several species of birds, including marsh tits and Clarke’s nutcrackers (Shettleworth, 2003).

Summary

Lateralization is manifested in two main ways: (1) in individuals but with no common direction (bias) in the group or population, or (2) in individuals and in the same direction in most individuals so that the group or population is biased. The first is discussed in terms of evidence of efficiency of neural processing in a lateralized brain. The second is discussed mainly in terms of the hypothesis that population biases occur as evolutionarily stable strategies when lateralized individuals coordinate with each other. This hypothesis is supported both by recent evidence and by mathematical models.

Introduction

It is believed that bilateral symmetry evolved when organisms adopted an axial orientation to their direction of movement and it is usually agreed that the pathway to a bilateral nervous system led from radial symmetry. In addition to being bilaterally divided, however, the nervous system of vertebrates shows a pervasively contralateral organization in that afferent and efferent pathways cross the midline of the body so that each side of the brain connects to the opposite side of the body. Also, as we have already seen (Chapter 1), the nervous system has a certain degree of asymmetry between the left and the right sides, and this is seen in both function and structure. Before considering the function of such an asymmetrical organization let us discuss the problem of why the nervous system is organized contralaterally (Figure 2.1), given that we shall refer to such an organization almost continuously while describing experiments and observations on asymmetries in animal behaviour.

Summary

This chapter discusses the evolution of lateralization in vertebrates and their ancestors. Vertebrate asymmetry was dominated from the start by extraordinary bodily asymmetry, which determined the course of evolution of nervous system asymmetries. Modern Echinoderms (starfish and sea urchins) and all chordates (the group to which vertebrates belong) came from an ancestor that had extreme right–left asymmetry. Evidence from invertebrates, discussed later in this chapter, suggests that the possession of paired sense organs (including sensory inputs from paired appendages, as well as from paired eyes) has sometimes been sufficient to allow the evolution of lateralization of functions of the central nervous system. The evidence takes us far from the earlier notion that hemispheric specialization evolved in humans about 2.5 million years ago along with language, handedness and tool using. Although important steps in human evolution, discussed here, involved brain lateralization, they were shaped by pre-existing asymmetries, rather than appearing de novo.

Origins of asymmetry in chordates

Ancestral chordates lived in a marine environment (in the Cambrian/Precambrian periods) very different from any present today. Food was available as tiny algae near the surface of the sea and as organic remains that had sunk to the sea floor; both were exploited by animals. The rarity of deep burrowing forms of life (Bambach et al., 2007) meant that accumulation of edible particles in the deposits on the sea floor was greater than now. The structure of food webs (‘what ate what’) reveals that, because efficient predators were relatively scarce (albeit not non-existent, as shown by the recent discovery of a Cambrian, arthropod predator; Paterson et al., 2011), many organisms did well at this time without the need for very effective defences against predators or the ability to flee (Bambach et al., 2007).

Over the past ten or so years, brain plasticity has become an extremely hot scientific trend and a huge commercial enterprise. From the parent who wants to give his or her newborn an enriched environment to promote superior brain growth to the aging adult who wants to stave off Alzheimer's disease, exercising, enriching, and training the brain has become a multimillion-dollar industry. Hundreds of brain promotion companies have sprouted up, such as The Baby Einstein Company, LLC, and hundreds of new books are published each year on brain enrichment. “Brain health,” “brain training,” and “brain fitness” are terms that are bandied about in the advertising world, suggestive of the possibility of improving and prolonging intellectual health. However, this “brain improvement” commercialism, although occasionally overstated, is not without some foundation in hard science: the discovery of brain plasticity.

The roots of the concept of “brain plasticity” can be traced toWilliam James's seminal work, The Principles of Psychology (1890), in which he clearly understood that behavior, habits, or instincts are governed by certain physiological limitations. He states, “Plasticity, … in the wide sense of the word, means the possession of a structure weak enough to yield to an influence, but strong enough not to yield all at once.… Organic matter, especially nervous tissue, seems endowed with a very extraordinary degree of plasticity of this sort; so that we may without hesitation lay down as our first proposition the following, that the phenomena of habit in living beings are due to the plasticity of the organic materials of which their bodies are composed” (p. 106).

Introduction

We mostly take object vision for granted, simply because our brain makes it seem easy. As a consequence, most of what we learn about objects during both development and adulthood goes unnoticed. Once the input to the system is in order (so excluding retinal disorders), almost all people can recognize cars, Coca-Cola bottles, and Barbie dolls. We only get a glimpse of the complexity of the underlying processes when we go through the most challenging tasks that we are typically confronted with. For example, some people have below average skills in face recognition. In this respect, interindividual differences in the most challenging object recognition tasks, created either naturally or in the lab by manipulating experience, serve as a gold mine for trying to understand the brain's exceptional ability to recognize objects.

My favorite example of an idiosyncratic object recognition talent is Gudrun, my eight-year-old daughter. She has a favorite teddy bear, are affection that developed when she was only a few months old. When Gudrun was one year old, my wife and I bought a second identical bear (just in case the first one was lost). Obviously, she noticed the difference between the old bear (which she calls “pretty bear”) and the new one. It was also easy for us parents to differentiate between the old worn bear and the new exemplar. However, over the years these differences became very minor, and now no one can reliably differentiate “pretty bear” from “new bear.”