Olfactory Information Processing in the Brain: Encoding Chemical and Temporal Features of Odors Thomas A. Christensen, zyxwvuts * Thomas Heinbockel, and John G. Hildebrand Arizona Research Laboratories, Division of Neurobiology,University of Arizona, Tucson, Arizona 85721 SUMMARY zyxwvutsr A fundamental problem in studying the neural mecha- nisms of odor recognition and discrimination in the olfac- tory system lies in determining the features or “primi- tives” of an odor stimulus that are analyzed by glomeru- lar circuits at the first level of processing in the brain. Several recent studies support the idea that it is not sim- ply the molecular features of odors that contain impor- tant information, but also the intermittent pattern of their presentation to the olfactory epithelium that helps deter- mine the behavioral response to odor. @ 1996 John zyx Wiley & Sons, Inc. zyxwvut Keywords: coding, intermittency, olfaction, sensory maps, synaptic integration. INTRODUCTION Odors have been celebrated for their ability to evoke powerful emotions and behavioral reactions in diverse species, and olfactory stimuli carry with them distinctive features that the brain must ana- lyze in order to discriminate among a vast number of scents. Quality and quantity are two stimulus features that are undoubtedly critical to odor signal processing and discrimination, but these can be greatly affected by another basic but frequently overlooked feature of olfactory stimuli: intermit- tency. Stimulus intermittency is a physical prop- erty that is fundamental to the delivery of all olfac- tory stimuli, and it therefore has a dramatic effect on an animal’s initial recognition of an odor (reviewed in Dethier, 1987).Active sampling strat- egies, such as sniffing in vertebrates (Youngentob et al., 1987), or “flicking” the olfactory appendages in invertebrates (Schmitt and Ache, 1979), result in distinct temporal patterns of odor presentation to the olfactory epithelium. Even in cases where an animal might sample its olfactory environment Received November 15, 1995; accepted November 27, 1995 Journal of Neurobiology, Vol. 30, No. 1, pp. 82-91 ( 1996) zyxwvut 0 1996 John Wiley & Sons, Inc. CCC 0022-3034/96/0 10082- 10 * To whom correspondence should be addressed. zyxwvutsrq 82 continuously, it is now clear that odors, whether delivered in air or water, possess an intrinsic spa- tiotemporal structure ( Murlis and Jones, 198 1 ; Murlis et al., 1990).Stimulus intermittency, there- fore, whether natural or induced, is a basic feature of all environmental odors; and new evidence indi- cates that it plays an important role in odor percep- tion. For some animals, like certain insects and crustaceans, it is now apparent that temporal changes in an odor stimulus dictate adjustments in the animals’ behavior, and these changes may be an important determinant in helping the animal lo- cate the odor source (Moore, 1994; Mafra-Net0 and Card;, 1994; Vickers and Baker, 1994). A crit- ically important function of such intermittency is that it helps reduce sensory adaptation, thus maxi- mizing the amount of olfactory information avail- able to the brain for subsequent analysis (cf. Dethier, 1987). It follows that neural circuits in ol- factory information-processing centers, while able to analyze the quality and quantity of the stimulus, might also be designed to encode (or even to enhance) these temporal contrasts in order to max- imize the steady flow of olfactory information to the brain. This review, drawing on evidence from both vertebrate and invertebrate olfactory systems, summarizes our present understanding of how ol- factory circuits at the first level of processing in the brain encode the chemical and temporal features