History and future directions of human brain mapping and functional neuroimaging

Abstract

It has long been known that there is some degree of localisation of function in the human brain, as indicated by the effects of traumatic head injury. Work in the middle of the 20th century, notably the direct cortical stimulation of patients during neurosurgery, suggested that the degree and specificity of such localisation of function were far greater than had earlier been imagined. One problem with the data based on lesions and direct stimulation was that the work depended on the study of what were, by definition, damaged brains. During the second half of the 20th century, a collection of relatively non-invasive tools for assessing and localising human brain function in healthy volunteers has led to an explosion of research in what is often termed “Brain Mapping”. The present article reviews some of the history associated with these tools, but emphasises the current state of development with speculation about the future.

Introduction

Let me begin by defining three terms: psychology, neuropsychology, and brain mapping. The first definition that I learned in college was for the term psychology: “The science that attempts to understand (i.e., explain, predict, and control) behaviour.” This definition was stated by Professor Hans-Lukas Teuber (the founder and then Chair of the Psychology Department at the Massachusetts Institute of Technology) to contrast it with the enterprise that most interested him: neuropsychology: “The science that attempts to understand the interactions between the nervous system and behaviour.” The distinction between psychology and neuropsychology (i.e., the distinction between behaviour and physiology) is another way of thinking about the question which the authors of this special issue of Acta Psychologica have been asked to address: “What is the role of traditional Psychonomics in the broader enterprise that goes by the name Cognitive Neuroscience?” This is a question of current interest and excitement primarily because of the explosion of research in brain mapping: the attempt to specify in as much detail as possible the localisation of function in the human brain. The growth of this research is driven largely by new developments in a collection of non-invasive technologies, with increasing spatial and temporal resolutions. Questions and opportunities are implied by this work for us as psychologists. Can our expertise in the study of behaviour improve the enterprise of brain mapping and, more generally, cognitive neuroscience? Do the new discoveries about human brain function based on neuroimaging experiments really teach us things that are relevant for the study and understanding of behaviour?

You will judge for yourself the answers to the above two questions by reading the collection of articles – addressing specific scientific applications – that compose the bulk of this special issue of Acta Psychologica. The present article will present an overview of the tools of functional neuroimaging, with a mildly historical flavour and an emphasis on the past, current, and future spatial and temporal resolutions of the relevant technologies. There will be an emphasis on functional magnetic resonance imaging (fMRI) because it is, in many ways, the most exciting new volumetric imaging tool, and (not coincidentally) because the experiments in this special issue are mostly based on fMRI.

It is important to note that the enterprise of brain mapping did not begin with fMRI or any other non-invasive imaging tool. The understanding that localisation of function is pervasive in the human brain has been well established for more than 50 years. Consider, for example, the summary of this knowledge represented by Fig. 1, reproduced from a book published in 1957 (Polyak, 1957). There are at least two kinds of questions that should be asked about this figure. The first questions are methodological: What is the basis for this figure? Where did the data come from? What were the technologies that gave rise to this data? The answer to these first questions is that the figure is based upon two techniques: study of people with lesions (caused, for example, by stroke, disease or traumatic wounds) and the direct electrical stimulation of the cortex of patients undergoing brain surgery. More about these techniques will be written below.

The second question that should be asked about Fig. 1 is: “What is the status of the data in terms of our current knowledge of the localisation of human brain function?” In other words, is the information portrayed in the figure accurate, as far as we know today? The answer, perhaps surprisingly, is that this figure is remarkably accurate. There is nothing indicated in the figure that is obviously wrong (though some of the terminology is out-of-date). On the other hand, as will be apparent in the remainder of the articles in this special issue of Acta Psychologica, a great deal more is known about the localisation of function in some areas (perhaps most notably in the multiple visual areas of the occipital lobe), and there are a wide variety of subtle perceptual, cognitive, and emotional tasks that have been used to refine this map at the cortical level, and to add information about subcortical structures, as well.

Thus, Fig. 1 teaches us that we were far from ignorant or misguided about localisation of brain function in 1957. So, what is all the current excitement about? The primary answer¹ is that today there are a host of technologies that can be used to give us information non-invasively that address the same issue. The study of patients with lesions, or those who are undergoing direct cortical stimulation during surgery, has substantial limitations. For ethical reasons, neither lesions (obviously) nor direct electrical stimulation of the brain via surgery (for reasons of general risk associated with exposing the brain) may be used in the study of healthy human subjects. Furthermore, the data in Fig. 1 are based on brains that were (by definition) not in a normal state of health.

Today, we have a plethora of techniques that allow us to measure brain function in healthy human subjects of all ages, repeatedly, and safely, over substantial periods of time. Each of these techniques has its own safety considerations, and each has characteristic limits in terms of spatial and temporal resolutions. Nonetheless, they permit us to generate data that are more refined than the information shown in Fig. 1, and which have the promise to become substantially better in the near future.