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VISCERAL SENSORY NEUROSCIENCE: INTEROCEPTION

Clare J. Fowler
DOI: http://dx.doi.org/10.1093/brain/awg120 1505-1506 First published online: 1 June 2003

VISCERAL SENSORY NEUROSCIENCE: INTEROCEPTION

By Oliver G. Cameron

2002. Oxford: Oxford University Press

Price £39.50. pp. 372. ISBN 0‐19‐513601‐2

Interoception: it is perhaps surprising that this word is not common medical parlance since amongst the other terms introduced by Sherrington, proprioception certainly is. As originally defined interoception encompassed just visceral sensations but now the term is used to include the physiological condition of the entire body and the ability of visceral afferent information to reach awareness and affect behaviour, either directly or indirectly. The system of interoception as a whole constitutes “the material me” and relates to how we perceive feelings from our bodies that determine our mood, sense of well‐being and emotions. Clearly this is a field of great relevance to many areas of medicine, to all branches of “internal medicine” as well medical psychology and possibly some branches of psychiatry.

The reason why this term is probably missing from our clinical vocabulary so far is that although we have been aware of the underlying concepts of interoception for decades there have been few methods of systematically studying the underlying principles in humans until the advent of functional imaging. Certainly it has been one of the disappointed aims of clinical neurophysiological research that has been unable to contribute much to our understanding of self‐awareness. This is because all that is accessible to that discipline is the response of large, heavily myelinated fibres, usually to electrical stimuli, whereas the interceptive system afferents are small diameter fibres that can usefully be considered as the afferent limb of the autonomic nervous system.

I accepted the offer to review this book from my position as one interested in the clinical problems of bladder sensations (and a disillusioned clinical neurophysiologist). It was clear to me that, with the emerging clinical potential of functional imaging, some understanding of interoception was essential and therefore undertook the task in hope that I would learn, and indeed I have, a lot. This topic and ways of studying it give us a new direction in including the importance of perception of homeostatic mechanisms in medicine as well as the shedding light on more philosophical problems like an hypothesis of consciousness. An already expert in these fields might think differently and perhaps be criticising the book because of inadequate coverage of ideas of the most modern theories which have evolved from functional imaging experiments, but to me the book was very valuable in many ways. It appears that its greatest strength is its detailed review of the pre‐functional imaging literature. The reference list is formidable and the author is clearly a master of the meaning of interoception and the ideas behind its historical development.

An early chapter starts with a review of theories of homeostasis, and leads as it did controversially at the time, onto theories of emotion. The James‐Lange theory is the necessary starting point, linking as it does emotion and interoception. As quoted from James his theory states “ that the bodily changes follow directly the perception of the exciting fact, and that our feeling of the same changes as they occur IS the emotion”. The counter arguments from Cannon who held that the primary source of the emotions was in the central nervous system are then presented.

The roots of the study of interoception came from Russia and Eastern Europe, starting with Pavlov, and it is thus fitting that considerable attention is given to reviewing his work. We are told that there is also an extensive literature; largely inaccessible now, written by followers of Pavlov and a whole chapter gives some insight into this. Before 1960 conditioning research was done in relative isolation and published only in Russian or Eastern European languages but from 1960s it became better integrated into general psychobiology. Although the contribution of Pavlov is unassailable it is much less clear what contribution was made by his successors: certainly a large number of creatures were sacrificed in conditions that modern animal licence regulations would not permit! It is probably important that these studies are reviewed if only to ensure there is no need for them to be repeated.

This is then followed by a review of early studies of operant conditioning of visceral function and the author admits that writing the chapter posed a dilemma. He warns that the reader “should bear in mind the tentative, doubtful, nature of some of the results” and describes how a theory of visceral learning experiments required a decade of observations and more than 2,500 rat studies for the researchers to conclude that their earlier observations were not replicable.

Most informative is a chapter on the neuronal pathways that carry visceral sensory information to higher centres. It provides a valuable review of combined higher function and anatomical structure and is much focussed on that fifth lobe of the brain, the insular cortex. This section would have been enhanced by more illustrations but whether these were considered to be too elementary by the author or expensive by the publisher is unknown. It is at this point that it would be appropriate to comment on the illustrations throughout the book, which are sadly disappointing. All are black and white line drawings somewhat cheaply reproduced and furthermore the captions are often poor. For example Figure 7‐4 illustrates pathways in the rat brain carrying visceral and somatic afferent information to the hypothalamus and limbic system and includes many abbreviations but for the meaning of these we are told to “see original”. Likewise Figure 9‐4. From Figure 5‐1 it is nice to know the experimenters gave their dogs names such as “Volga”, “Rex” and “Rongyos” and to see the presumably original script labelling, but it is extremely difficult to fathom its contribution with the information given. Furthermore, every figure has the same rather irritatingly uninformative statement to comply with legalities of copyright.

Following the excellent review of the neural basis of visceral perception, specific systems are addressed. The cardiovascular and respiratory systems are areas where the author himself has contributed, and the literature relating to cardiac interoception is included in very great detail. However a little more of medical relevance would have been welcome. More functional imaging work has been carried out so far on the alimentary tract than other systems and here the potential importance of the findings to gastroenterology become apparent. A striking and major omission from this whole section is a chapter on interoception and the uro‐genital tract; a formidable task but one that must be addressed (with colour illustrations please) in any second edition.

I enjoyed the apposite and amusing quotes beneath each chapter heading—particularly that of Lewis Thomas in 1972 who said about Autonomy “I’d rather leave all my autonomic functions with as much autonomy as they please. Imagine having to worry about running leukocytes, keeping track, herding them here and there, listening for signals. After the first flush of pride in ownership, it would be exhausting and debilitating and there would be no time for anything else.” These and other bon mot have all been selected widely from either science or literature and introduce the content of each new chapter splendidly.

The volume concludes on a philosophical note with concerns as to consciousness and bodily awareness, an area now of hot debate. Perhaps neurophilosophy will always remain beyond medicine although not psychology and perhaps not psychiatry.

The book would be a useful resource for students of psychology and neurobiology in general. As a novice in the field of interoception I learnt a great deal from it and would recommend others embarking on the fascinating investigation of brain processing of bodily sensations now possible through functional imaging methods to read it. It is with a sense of achievement that I dispatch this review to the journal—evidence that I have digested a learned tome about a new and significant area of neuroscience, and aware through intellectual interoceptive systems that it has altered my thinking and future approach to my particular branch of neurology.