Learning to Smell: Olfactory Perception from Neurobiology to Behavior

Preface

Preface This book represents a rather unusual collaboration between a neurobiologist and a psychologist that grew out of the similarities emerging between physiological and psychophysical research in olfaction. The major problem in olfactory behavioral neuroscience is to determine how the brain discriminates one smell, or perceptual odor, from another. Olfactory and chemical sensory systems were one of the first sensory systems to evolve, and some form of chemosensory system is expressed in every living organism from bacteria to primates. Critical aspects of olfactory system anatomy appear highly convergent across both invertebrates and vertebrates, perhaps in evidence of the unique requirements of a system for dealing with complex, often unpredictable stimuli. The traditional approach for understanding olfactory perception involves identifying how particular features of a chemical stimulus are represented in the olfactory system. This perspective is at odds, however, with a growing body of evidence, from both neurobiology and psychology, which places primary emphasis on synthetic processing and experiential factors—perceptual learning—rather than on the structural features of the stimulus as critical for odor discrimination. Research from our laboratory and others increasingly argues that experience-based, synthetic olfactory processing leads to treatment of multifeature odorants as individual “odor-objects.” This is a process similar to, and perhaps evolutionarily predating, visual object perception, a comparison we frequently make in this book. Furthermore, experience-based, synthetic olfactory processing can be multidimensional, with odor representations coming to integrally include, for example, both multimodal components (e.g., taste) and affective components. In this volume, we present a new theoretical view of olfactory perception that puts old psychological, ethological, and sensory physiological data in a new light and is backed by new psychophysical and physiological data. In the opening chapter we explore the function of olfactory systems in humans and other animals and the unique difficulties presented by highly complex and often unpredictable chemical stimuli. In the second chapter, we discuss the conceptual and historical roots of the stimulus feature extraction/feature detection approach and its detrimental consequences in shaping thinking about olfaction. We then compare this with contemporary thinking about visual and haptic object recognition and how synthetic and experience-based processing incorporated into those fields offers a better model for understanding olfaction. In chapter 3, we review the anatomy of the olfactory system from a novel theoretical view emphasizing function and how known circuitry may allow the type of synthetic information processing we have proposed . Specific comparisons are made with the circuitry underlying visual object perception. Chapter 4 deals with detection and intensity and demonstrates that, even here, experience plays a role in what would typically be considered low-level processes. Chapters 5 and 6 address the nature of odor perceptual quality in animals and humans and present the argument that odor quality is not dictated solely by the physicochemical stimulus; rather, it is a synthetic construct of physicochemical stimulus properties, memory, and biological constraints. This theoretical view not only encompasses a large range of physiological and behavioral findings but also explains some apparent anomalies, such as difficulty in identifying individual odors in mixtures. Chapter 7 explores the large literature on explicit, associative memory for odors in humans and animals and suggests how these findings may be accounted for by the perceptual memory system dealt with in earlier chapters. Finally, in chapter 8 we summarize the evidence favoring an experiential approach to olfactory perception. We then compare the neural and psychological processing that underpins object perception in olfaction and vision and consider the strengths and weaknesses of drawing such an analogy. In addition , we identify existing data that need to be reinterpreted in light of this new view of olfaction, as well as new questions raised by the mnemonic view of odor perception. In summary, we propose that experience and cortical plasticity play a critPreface viii ical, defining role in odor perception and that current views of a highly analytical , “receptor-centric” process are insufficient to account for current data. don wilson thanks his family for their love and support over the years, his students for their hard work, and the National Institutes of Health and the National Science Foundation for their generous financial support. Dick Stevenson thanks Caroline, Lucy, Harry, Gemma, and Chris and Mike Thomas for their patience and support. Many colleagues played an important role in developing the ideas described here, notably Trevor Case and Bob Boakes. Much of the work reported here...