Olfactory space has a higher dimensionality than does any other class of sensory stimuli, and the olfactory system receives input from an unusually large number of unique information channels. This suggests that aspects of olfactory processing may differ fundamentally from processing in other sensory modalities. This review summarizes current understanding of early events in olfactory processing. We focus on how odors are encoded by the activity of primary olfactory receptor neurons, how odor codes may be transformed in the olfactory bulb, and what relevance these codes may have for downstream neurons in higher brain centers. Recent findings in synaptic physiology, neural coding, and psychophysics are discussed, with reference to both vertebrate and insect model systems.

Early events in olfactory processing

The present study investigates the hypothesis that complexobject odors (odors that emanate from flowers, foods, sewage, etc.) that consist of dozens of odorants are processed and encoded as discrete entities, as if each was a single chemical odor. To test this hypothesis, the capacity of trained subjects to discriminate and identify the components of stimuli consisting of one to eight object odors was determined. The results indicated that subjects could only identify up to four object odors in a mixture, which is similar to earlier findings with mixtures that contained only single chemical odors. The limited capacity was also reflected in the number of odors selected, regardless of whether the choices were correct or incorrect, in confidence ratings, and in decision times. The identification of a limited number of object odors in every mixture that was presented suggests that both associative (synthetic) and dissociative (analytic) processes are involved in the perceptual analysis of odor mixtures.

/pdf/the-influence-of-chemical-complexity-on-the-perception-of-3gedcu487r.pdf

The influence of chemical complexity on the perception of multicomponent odor mixtures.

Patterned neural activity helps to establish neuronal connectivity, produce coding of sensory information, and shape synaptic strengths. Here we demonstrate that normal olfactory bulb development might rely on spatial and temporal patterns of afferent neural activity. Neonatal naris occlusion profoundly impacts the development of the ipsilateral olfactory bulb, including reduced bulb volume, decreased protein synthesis, and increased cell death. Relatively few morphologic changes occur if closure is performed postweaning. We examined the immediate electrophysiological consequences of occlusion across this developmentally sensitive period by recording spontaneous and odor-driven mitral/tufted cell responses while the naris was open, closed, and then reopened. In 1-week-old animals, occlusion severely attenuated spontaneous activity, and presentation of the broad-spectrum odorant amyl acetate failed to evoke responses. In 2- and 4-week old rats, spontaneous activity was also reduced by naris closure. However, some cells remained responsive to concentrated odors, even in animals with transected anterior commissures, suggesting passage of odors across the septal window or retronasal pathways. In all age groups, cellular activity became uncoupled from the respiratory cycle. Approximately 47% (18 of 38) of the mitral/tufted cells exhibited activity that was correlated with respiration in the open-naris state, while only 5% (2 of 38) were coupled during naris closure. These data (a) indicate that naris closure reduces both spontaneous and odor-evoked responses, and (b) provide an electrophysiological correlate to a sensitive period in bulb development. The loss of respiration-related synchrony and the reduced activity of mitral/tufted cells may synergistically contribute to the diverse consequences of naris closure on bulb development.

Mitral/tufted cell activity is attenuated and becomes uncoupled from respiration following naris closure.

Stimulation of olfactory receptor cells leads to the activation of a G protein-coupled cascade, which culminates in the activation of adenylyl cyclase, causing an increase in intracellular levels of cAMP (for review see Breer, 1994; Schild & Restrepo, 1998). Cyclic AMP opens the olfactory cyclic nucleotide-gated channel, a cation channel that mainly conducts Ca2+ under normal ionic conditions (Frings et al. 1995; Dzeja et al. 1999). The ensuing increase in intracellular Ca2+ concentration (Leinders-Zufall et al. 1997, 1998a) opens a Ca2+-activated Cl− conductance (Kleene & Gesteland, 1991), which augments the excitatory inward receptor current (Kurahashi & Yau, 1993; Lowe & Gold, 1993; Zhainazarov & Ache, 1995).

While responses of the olfactory receptor cells of lower vertebrates to brief stimuli have been characterised extensively (Mathews, 1972; Getchell & Shepherd, 1978a;Firestein et al. 1993; Reisert & Matthews, 1999), relatively little is known about their responses to more prolonged stimulation. Extracellular recordings of action potential firing have revealed that olfactory receptor cells respond to relatively brief odour stimuli of up to 10 s in duration with an initial high-frequency burst of action potentials often followed by more sustained firing at a lower frequency, although in some cases spiking ceased temporarily or completely during stimulation (Shibuya & Shibuya, 1963; Getchell & Shepherd, 1978a; Baylin & Moulton, 1979). In one study a longer 30 s odour stimulus was found to evoke repetitive bursts of spikes driven by underlying oscillations in membrane potential (Frings & Lindemann, 1988). In addition to these excitatory actions, inhibitory responses in the form of a reduction of the basal spike rate have also been reported (O'Connell & Mozell, 1969; Getchell & Shepherd, 1978b; Morales et al. 1994). In the whole-cell voltage-clamp configuration, exposure to high odour concentrations for periods of 20 s and longer caused a rapid increase in receptor current followed by a slow decline, but a measurable receptor current remained present during the entire period of stimulation (Lowe & Gold, 1995; Menini et al. 1995).

Unfortunately, most of these existing studies were hampered by poorly controlled stimulus delivery, too short a stimulus duration, or the application of only a limited range of odour concentrations. We have therefore used the suction pipette technique (Baylor et al. 1979; Lowe & Gold, 1991; Reisert & Matthews, 1999) to study the responses of isolated amphibian olfactory receptor cells to prolonged odour stimuli. This approach enabled us not only to record the receptor current and spiking responses simultaneously but also to achieve the extended stable recording durations that are required to characterise their properties over a wide range of odour concentrations. In addition, rapid superfusion techniques allowed precisely timed exposure of the olfactory cilia to solutions of defined composition. Preliminary results from this study have been presented to The Physiological Society (Reisert & Matthews, 1997).

https://physoc.onlinelibrary.wiley.com/doi/pdf/10.1111/j.1469-7793.2001.t01-1-00179.x

Responses to prolonged odour stimulation in frog olfactory receptor cells

In order to study the problem how the olfactory neural system processes the odorant molecular information for constructing the olfactory image of each object, we present a dynamic model of the olfactory bulb constructed on the basis of well-established experimental and theoretical results. The information relevant to a single odor, i.e. its constituent odorant molecules and their mixing ratios, are encoded into a spatio-temporal pattern of neural activity in the olfactory bulb, where the activity pattern corresponds to a limit cycle attractor in the mitral cell network. The spatio-temporal pattern consists of a temporal sequence of spatial firing patterns: each constituent molecule is encoded into a single spatial pattern, and the order of magnitude of the mixing ratio is encoded into the temporal sequence. The formation of a limit cycle attractor under the application of a novel odor is carried out based on the intensity-to-time-delay encoding scheme. The dynamic state of the olfactory bulb, which has learned many odors, becomes a randomly itinerant state in which the current firing state of the bulb itinerates randomly among limit cycle attractors corresponding to the learned odors. The recognition of an odor is generated by the dynamic transition in the network from the randomly itinerant state to a limit cycle attractor state relevant to the odor, where the transition is induced by the short-term synaptic changes made according to the Hebbian rule under the application of the odor stimulus.

An olfactory recognition model based on spatio-temporal encoding of odor quality in the olfactory bulb

Responses of olfactory bulb neurons to repeated odor stimulations in awake freely-breathing rabbits.

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Responses of olfactory bulb neurons to repeated odor stimulations in awake freely-breathing rabbits.