Learning to Smell: Olfactory Perception from Neurobiology to Behavior

8. Implications

8 Implications Thomas Kuhn (1962), in his Structure of Scientific Revolutions notes that facts are not like pebbles on the beach waiting to be picked up. Rather, he argues, how observations are interpreted (and thus become facts) is based on the theoretical viewpoint and resulting expectations of the viewer. Kuhn’s argument has dual relevance here. First, we posit that smells (like facts) are not like molecules on the beach waiting to be inhaled, but rather are outcomes of highly synthetic, memory-dependent processing that is further modulated by expectation, context, and internal state. Second, how one interprets the experimental data in olfaction and, in fact, even the nature of the questions being asked, is strongly influenced by the theoretical view one has of the nature of olfaction. Data that do not fit conveniently into the existing theoretical view (“paradigm” in Kuhn’s terminology) are either forced to at least superficially fit or commonly sidelined as anomalous. For example, a physicochemical, analytical theoretical view of olfaction suggests a very clear line of investigation. Identify specific ligands for specific receptors, identify primary odor qualities, look for specific anosmias, attempt to induce specific anosmias through select receptor elimination or central lesions , and attempt to predict olfactory percepts from physicochemical structure (i.e., stimulus-response). We have reviewed historical (and more recent) efforts to address each of these questions, initial claims of success, and frequent subsequent contrary evidence (e.g., primary odors). We suggest (humbly) that it is time for a paradigm shift in olfactory sci- ence, away from physicochemical views toward a synthetic, mnemonic view of olfaction as an object-based sense. The study of visual perception has had to undergo a similar process. As Richard Held (1989) notes, “during the nineteenth century it was apparently easy to believe that a correlation may be established between sensorineural and perceptual states. Knowing little about the neuronal processes left a great deal of latitude for speculation” (p. 140). However, Held goes on, “perhaps the stimulus provides only certain constraints on these processes. Perception is said to be distinguished from imagery by the presence of such stimulus constraints” (p. 142). Finally, Held concludes, “that conflict [between the physical nature of the stimulus, the initial sensorineural processing, and the ultimate percept] may be resolved by considering perception as reflective activity rather than passive reception” (p. 139). In this final chapter we review, in brief, both the case for reflective, experience-based object recognition as the basis for understanding odor perception and the evidence for its operation via encoding novel olfactory experiences and matching inputs to them. We then argue that visual object recognition, which has been explored in considerable depth, offers some important parallels to the psychological and physiological processes that we have suggested underlie olfactory perception, most notably the reliance of all contemporary theories of visual object recognition on experience. The literature on visual object recognition is theoretically and empirically rich and in the penultimate part of this chapter we contend that a paradigm shift toward an object recognition view of olfaction can also provide similar benefits, by generating many testable hypotheses and encouraging theoretical development in this area. Finally, we end by briefly reiterating the central message that we would like to communicate—the perceptual ecology of smell suggests object recognition, the extant data support it, and what we need now is a concerted effort to find out if this perspective really is, as we think, the right one for understanding olfaction. Odor Perception as Mnemonically Mediated Object Recognition The Ecological Perspective Our first consideration must be the role that olfaction plays in the behavior of animals and humans and the implications that flow from this for function and process. In animals and humans, several common roles emerge, including recognizing food, mates, kin, predators, and disease vectors. The comLearning to Smell 244 mon element that underpins all these functions is the need to recognize the combination of chemicals that go to make up these various objects against a shifting and complex chemical background. Thus, the primary task the system faces is to learn what combination of features makes up a biologically significant pattern, encode this information, and then be able to discriminate this combination—the odor object—from both other objects and background sources of olfactory stimulation. The same chemical stimulus may have radically different meaning depending on the receiver...