Odor Images and Tunes

Conspicuously absent from these anatomical and physiological considerations is time, a critical parameter in the expression of neural activity. Neuronal responses are often inferred simply from the observation of increased or decreased fluorescence signals or spike numbers, in response to a stimulus. Although such measures are, to a great extent, appropriate, they rest on the assumption that information about the stimulus lies simply in average neuronal activity (mean rate codes). This need not be the case. Patterns of action potentials (their fine temporal structure, such as delays between spikes produced by one neuron, or relational codes, precise temporal relationships between spikes produced by different neurons; 1xAbbott, L.F. Quart. Rev. Biophys. 1994; 27: 291–331Crossref | PubMed | Scopus (86)See all References, 22xTheunissen, F. and Miller, J.P. J. Comp. Neurosci. 1995; 2: 149–162Crossref | PubMed | Scopus (199)See all References) or of field potentials (Barrie et al. 1996xBarrie, J.M., Freeman, W.J., and Lenhart, M.D. J. Neurophysiol., in press. 1996; See all ReferencesBarrie et al. 1996) may indeed contain significant information. Such considerations are interesting in the case of olfaction, because odor sampling is often periodic (sniff, antennal flick) and therefore provides stereotypical epochs during which temporal patterns might be used for coding. This aspect is important because studies in arthropods, molluscs and vertebrates have long revealed odor-induced temporal response patterns in olfactory neurons. RecentlyCinelli et al. 1995xCinelli, A.R., Hamilton, K.A., and Kauer, J.S. J. Neurophysiol. 1995; 73: 2053–2071PubMedSee all ReferencesCinelli et al. 1995, for example, described temporal response patterns distributed over populations of neurons. Mori's results in rabbit (Mori and Yoshihara 1995xMori, K. and Yoshihara, Y. Prog. Neurobiol. 1995; 45: 585–619Crossref | PubMed | Scopus (193)See all ReferencesMori and Yoshihara 1995) indicate patterned responses of individual M/T cells.How can we determine whether these patterns are significant? Two criteria must be fulfilled. First, the temporal patterns should be consistent for individual stimuli presented repeatedly, and different for different stimuli (stimulus specificity). Second, disrupting the temporal relationships between active neurons, but not their mean activity, should disrupt the perception of the stimulus. This requires a behavioral measure of perception, a task that very few neurobiological model systems can accomplish yet. Any study of coding, whether it addresses temporal, relational, or mean rate codes, should, of course, attempt to address this point. We are not there yet! Two recent studies, however, focused specifically on the dynamics of neuronal responses in invertebrate olfactory circuits. In the first, the electrical activity in the procerebral lobe of Limax was studied using optical and electrophysiological techniques. Delaney et al. 1994xDelaney, K.R., Gelperin, A., Fee, M.S., Flores, J.A., Gervais, R., Tank, D.W., and Kleinfeld, D. Proc. Natl. Acad. Sci. USA. 1994; 91: 669–673Crossref | PubMedSee all ReferencesDelaney et al. 1994 found slow (<1 Hz) waves of electrical activity traveling the entire length of the lobe. The waves, possibly due to a gradient of excitability, exist in the absence of odorant. Presentation of a behaviorally significant odor, however, appears to modify this gradient of excitability so that the lobe, rather than produce a traveling wave, now experiences the oscillation uniformly. The role of this odor-induced collapse of the phase gradient is not yet known. Delaney et al. propose that it may underlie a stimulus-induced attentive state. It is also possible that the deciphering of very strict temporal relationships between odor-specific neuronal groups requires transient synchrony of all of the active neurons. It will be fascinating to discover the details of the firing patterns that underlie these population signals between and during odor presentations.A second study, carried out in an insect, revealed a macroscopic phenomenon similar to that observed in most vertebrates, the generation of field potential oscillations (20–30 Hz) by odor presentation (Laurent and Davidowitz 1994xLaurent, G. and Davidowitz, H. Science. 1994; 265: 1872–1975Crossref | PubMedSee all ReferencesLaurent and Davidowitz 1994). Like in other systems, the frequency of these oscillations is independent of the nature of the odorant. By recording from several neurons at once, however, it was found that the oscillations mask complex patterns of activity, which are distributed not only among odor-specific groups of neurons, but also distributed in time. In other words, the oscillatory population synchrony is in fact created by dynamic ensembles of neurons, each of which participate in the synchronized activity only in odor-specific time windows. It is as if the neuronal ensemble were a choir, and each neuron of a select group contributed to a song during a limited number of measures. A different odor would generate a different song with the same beat, but with different singers: each singer would be assigned different measures to interpret. This study fulfills the stimulus-specificity criterion proposed above. More work, however, is needed to prove that these patterns (synchronization and slower modulation of firing) are important for perception. Animals such as the honeybee, where behavior and physiology can be combined, may hold the key to these questions.The last few years have seen some major advances in the study of olfaction and its underlying mechanisms. It is important to remember, however, that smelling, like seeing or hearing, is an active process. A full understanding of olfaction will therefore require not only a description of the events and activity patterns caused by olfactory stimuli, but also of the influences that the brain exerts on olfactory circuits during smelling. Kay 1995xKay, L.M. See all ReferencesKay 1995, for example, recorded field potentials simultaneously from the OB, prepiriform cortex (PPC), entorhinal cortex (EC), and dentate gyrus of freely behaving rats. She showed that odor-evoked high frequency bursts (60–100 Hz) originate in the OB before sequentially invading the other centers. By contrast, she found that low frequency bursts (∼20 Hz) often originated in EC, before invading PPC and OB. Such centrifugal patterns, however, were generally seen only in trained animals expecting an odor after conditioning. These results suggest, therefore, that some efferent control of OB circuits (possibly modulating their dynamical state) can occur under behavioral conditions such as anticipation. Because olfaction is so closely associated with memory, interplay between the peripheral sensory circuits and the central networks involved in storage and recall may play a very important role in odor discrimination and recognition. Understanding odor processing in the early olfactory circuits (olfactory bulb, antennal lobe, procerebral lobe) will thus require not only a clear description of the functional mapping of afferent projections, but also a better understanding of the dynamic responses that may arise from the interaction of inputs originating in the nose and in the brain.