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Neuron, 2005

put across nostrils was supported by von Békésy 1 Program in Biophysics (1964), who, in an elegant study, found that differences 2 Program in Bioengineering in odorant concentration or in time of stimulus arrival 3 Helen Wills Neuroscience Institute across the two nostrils enable humans to spatially lo-4 Department of Psychology calize an odorant (1964). University of California, Berkeley To investigate the neural substrates that subserve the Berkeley, California 94720 behavioral mechanism described by von Békésy, we set out to conduct a left versus right odorant localization study within the functional magnetic resonance (fMRI) scanner. The following considerations guided us Summary in the selection of odorants for this task. Odor perception results from the combination of inputs from odor-Forty years ago, von Békésy demonstrated that the ant transduction at a number of different nerves (Bojspatial source of an odorant is determined by comsen-Moller, 1975). Whereas high concentrations of paring input across nostrils, but it is unknown how most known odorants will excite the trigeminal and olthis comparison is effected in the brain. To address factory nerves ("trigeminal odorants"), a very small this, we delivered odorants to the left or right of the number of odorants will excite the olfactory nerve only nose, and contrasted olfactory left versus right local-("pure olfactants"). Although these nerve pathways are ization with olfactory identification during brain imlinked at both peripheral (Bouvet et al., 1987; Schaefer aging. We found nostril-specific responses in primary et al., 2002) and central (Macrides and Chorover, 1972; olfactory cortex that were predictive of the accuracy Stone and Rebert, 1970; Stone et al., 1968) aspects of the of left versus right localization, thus providing a neuolfactory system, they nevertheless induce dissociable ral substrate for the behavior described by von neural responses (Hummel et al., 1992; Savic, 2002; Savic Békésy. Additionally, left versus right localization et al., 2002), and more pertinently, may contribute difpreferentially engaged a portion of the superior temferently to odorant localization. Most attempts to replicate poral gyrus previously implicated in visual and audithe result obtained by von Békésy have suggested that tory localization, suggesting that localization informaspatial localization of an odorant is possible only when tion extracted from smell was then processed in a the odorant is trigeminal (Kobal et al., 1989; Radil and convergent brain system for spatial representation of Wysocki, 1998; Schneider and Schmidt, 1967), although multisensory inputs. some have not ruled out pure olfactory localization under some circumstances (Schneider and Schmidt, 1967). In

SUMMARYThe ability to group sensory stimuli into categories is crucial for efficient interaction with a rich and ever-changing environment. In olfaction, basic features of categorical representation of odours were observed as early as in the olfactory bulb (OB). Categorical representation was described in mitral cells (MCs) as sudden transitions in responses to odours that were morphed along a continuum. However, it remains unclear to what extent such response dynamics actually reflects perceptual categories and decisions therein. Here, we tested the role of learning on category formation in the mouse OB, using in vivo two-photon calcium imaging and behaviour. We imaged MCs responses in naïve mice and in awake behaving mice as they learned two tasks with different classification logic. In one task, a 1-decision boundary task, animals learned to classify odour mixtures based on the dominant compound in the mixtures. As expected, categorical representation of close by odours, which wa...

Cell and Tissue Research, 2021

The ability of the olfactory system to detect and discriminate a broad spectrum of odor molecules with extraordinary sensitivity relies on a wide range of odorant receptors and on the distinct architecture of neuronal circuits in olfactory brain areas. More than 1000 odorant receptors, distributed almost randomly in the olfactory epithelium, are plotted out in two mirror-symmetric maps of glomeruli in the olfactory bulb, the first relay station of the olfactory system. How does such a precise spatial arrangement of glomeruli emerge from a random distribution of receptor neurons? Remarkably, the identity of odorant receptors defines not only the molecular receptive range of sensory neurons but also their glomerular target. Despite their key role, odorant receptors are not the only determinant, since the specificity of neuronal connections emerges from a complex interplay between several molecular cues and electrical activity. This review provides an overview of the mechanisms underly...

Canadian Journal of Philosophy, 2019

Several theorists argue that one does not experience something as being at or coming from a distance or direction in olfaction. In contrast to this, I suggest that there can be a variety of spatial aspects of both synchronic and diachronic olfactory experiences, including spatial distance and direction. I emphasise, however, that these are not aspects of every olfactory experience. Thus, I suggest renouncing the widespread assumption there is a uniform account of the nature, including the spatial nature, of what is experienced in olfactory experience.

Microscopy Research and Technique, 1993

Complete understanding of the role of the mammalian main olfactory bulb in sensory processing has remained elusive despite many detailed studies on its anatomy and physiology. Several lines of recent evidence viewed in the context of earlier knowledge have provided new insights into the bulbar mechanisms of olfactory coding. The output cells of the olfactory bulb receive a localized olfactory nerve input and interneuronal input via dendrodendritic synapses on distinct sets of dendrites. The spatial arrangement of granule cell contacts on output cell basal dendrites suggests that lateral inhibitory interactions may occur between neighboring output cells. The input from olfactory receptor cell axons to the bulb also has spatial order, but does not represent a precise map of the receptor surface. Recent studies with antibodies and lectins suggest that different groups of axons from chemically similar receptor cells collect into certain glomeruli, even if the axons originate from cells that are not contiguous in the mucosa. Electrophysiological studies have begun to explore the participation of spatially organized circuits in olfactory processing. The degree to which neighboring output cells respond similarly to odor stimulation, for example, depends on the distance between the cells, with those further apart showing complementary responses. Also, a single output cell can show 2 or more different temporal response patterns when different odors are presented. Intracellular recordings indicate that these responses are shaped by IPSPs. Electrical stimulation during such recordings shows that some mitral cells are excited by nerve inputs close to their glomerular tufts, while they are inhibited by nerve inputs to other parts of the bulb. Finally, recordings from granule and periglomerular cells indicate their potential in mediating components of output cell odor responses. These considerations suggest that the olfactory bulb performs a spatially based analysis on the information coming from the receptor cells. While the spatial organization of the olfactory bulb is probably not faithfully represented in the projections to the olfactory cortex, bulbocortical projections are not random. The fact that spatial factors exist at each of these levels in the olfactory system must be considered in developing models of central olfactory processing. © 1993 Wiley-Liss, Inc.

Nature Neuroscience, 2011

1 4 5 5 a r t I C l e S Receptive surfaces have evolved to optimally encode the sensory scene. Thus, their organization typically reflects key perceptual axes relevant to their function. For example, vision is spatial, and retinal coordinates reflect spatial coordinates 1 . Audition is tonal, and cochlear coordinates reflect tonal coordinates 2 . In contrast, the perceptual axes of olfaction are poorly understood, and organizational coordinates of olfactory epithelium have yet to be linked to perception.

Journal of Neuroscience, 2010

Odor identity is coded in spatiotemporal patterns of neural activity in the olfactory bulb. Here we asked whether meaningful olfactory information could also be read from the global olfactory neural population response. We applied standard statistical methods of dimensionality-reduction to neural activity from 12 previously published studies using seven different species. Four studies reported olfactory receptor activity, seven reported glomerulus activity, and one reported the activity of projection-neurons. We found two linear axes of neural population activity that accounted for more than half of the variance in neural response across species. The first axis was correlated with the total sum of odor-induced neural activity, and reflected the behavior of approach or withdrawal in animals, and odorant pleasantness in humans. The second and orthogonal axis reflected odorant toxicity across species. We conclude that in parallel with spatiotemporal pattern coding, the olfactory system can use simple global computations to read vital olfactory information from the neural population response.

Frontiers in Psychology, 2014

In the present work we present an overview of experimental findings corroborating olfactory imagery observations with the visual and auditory modalities. Overall, the results indicate that imagery of olfactory information share many features with those observed in the primary senses although some major differences are evident. One such difference pertains to the considerable individual differences observed, with the majority being unable to reproduce olfactory information in their mind. Here, we highlight factors that are positively related to an olfactory imagery capacity, such as semantic knowledge, perceptual experience, and olfactory interest that may serve as potential moderators of the large individual variation.

Nature Neuroscience, 2008

No two roses smell exactly alike, but our brain accurately bundles these variations into a single percept 'rose'. We found that ensembles of rat olfactory bulb neurons decorrelate complex mixtures that vary by as little as a single missing component, whereas olfactory (piriform) cortical neural ensembles perform pattern completion in response to an absent component, essentially filling in the missing information and allowing perceptual stability. This piriform cortical ensemble activity predicts olfactory perception.

Frontiers in Computational Neuroscience, 2020

We describe an integrated theory of olfactory systems operation that incorporates experimental findings across scales, stages, and methods of analysis into a common framework. In particular, we consider the multiple stages of olfactory signal processing as a collective system, in which each stage samples selectively from its antecedents. We propose that, following the signal conditioning operations of the nasal epithelium and glomerular-layer circuitry, the plastic external plexiform layer of the olfactory bulb effects a process of category learning-the basis for extracting meaningful, quasi-discrete odor representations from the metric space of undifferentiated olfactory quality. Moreover, this early categorization process also resolves the foundational problem of how odors of interest can be recognized in the presence of strong competitive interference from simultaneously encountered background odorants. This problem is fundamentally constraining on early-stage olfactory encoding strategies and must be resolved if these strategies and their underlying mechanisms are to be understood. Multiscale general theories of olfactory systems operation are essential in order to leverage the analytical advantages of engineered approaches together with our expanding capacity to interrogate biological systems.

Frontiers in Cellular Neuroscience

Knowing which elements in the environment are associated with various opportunities and dangers is advantageous. A major role of mammalian sensory systems is to provide information about the identity of such elements which can then be used for adaptive action planning by the animal. Identity-tuned sensory representations are categorical, invariant to nuances in the sensory stream and depend on associative learning. Although categorical representations are well documented across several sensory modalities, these tend to situate synaptically far from the sensory organs which reduces experimenter control over input-output transformations. The formation of such representations is a fundamental neural computation that remains poorly understood. Odor representations in the primary olfactory cortex have several characteristics that qualify them as categorical and identity-tuned, situated only two synapses away from the sensory epithelium. The formation of categorical representations is lik...

BMC neuroscience, 2006

Background: Contrast enhancement within primary stimulus representations is a common feature of sensory systems that regulates the discrimination of similar stimuli. Whereas most sensory stimulus features can be mapped onto one or two dimensions of quality or location (e.g., frequency or retinotopy), the analogous similarities among odor stimuli are distributed highdimensionally, necessarily yielding a chemotopically fragmented map upon the surface of the olfactory bulb. While olfactory contrast enhancement has been attributed to decremental lateral inhibitory processes among olfactory bulb projection neurons modeled after those in the retina, the two-dimensional topology of this mechanism is intrinsically incapable of mediating effective contrast enhancement on such fragmented maps. Consequently, current theories are unable to explain the existence of olfactory contrast enhancement.

Neuron, 2003

manner (Laurent et al., 2001). This model, however, has not yet been extended to the context of intensity coding. Computation and Neural Systems Program Pasadena, California 91125 This is essential, because recordings from amphibians and mammals indicate that MC temporal response patterns change as odor concentration is varied (Kauer and Moulton, 1974; Meredith, 1986; Wellis et al., 1989), Summary raising the possibility that spatiotemporal codes for concentration and identity are confounded. In addition, im-We examined the encoding and decoding of odor idenaging results indicate that higher odor concentrations tity and intensity by neurons in the antennal lobe and increase glomerular response intensity and recruit addithe mushroom body, first and second relays, respectional glomeruli (Ng et al., 2002; Wang et al., 2003; Cinelli tively, of the locust olfactory system. Increased odor et al., 1995; Friedrich and Korsching, 1997; Joerges et concentration led to changes in the firing patterns al., 1997; Meister and Bonhoeffer, 2001; Rubin and Katz, of individual antennal lobe projection neurons (PNs), 1999; Stewart et al., 1979), consistent with the observasimilar to those caused by changes in odor identity, tion that MC responses change both quantitatively and thus potentially confounding representations for idenqualitatively with odor concentration (Kauer and Moultity and concentration. However, when these timeton, 1974; Meredith, 1986; Wellis et al., 1989). How then varying responses were examined across many PNs, are odors represented such that they can be identified concentration-specific patterns clustered by identity, over many concentrations, as behavioral experiments resolving the apparent confound. This is because PN in humans, rodents, and insects indicate (Engen and ensemble representations changed relatively continu-Pfaffmann, 1959; Slotnick and Ptak, 1977; Pelz et al., ously over a range of concentrations of each odorant. 1997)? Are there, for example, some invariant features The PNs' targets in the mushroom body-Kenyon cells in the responses of principal neurons that allow accurate (KCs)-had sparse identity-specific responses with diodor classification across concentrations? We examverse degrees of concentration invariance. The tuning ined this issue in the locust olfactory system by reof KCs to identity and concentration and the patterning cording the activity of neurons in the AL and of Kenyon of their responses are consistent with piecewise decells (KCs), the PNs' targets in the mushroom bodies, coding of their PN inputs over oscillation-cycle length a structure known to participate in olfactory memory epochs. (Heisenberg et al., 1985; Heisenberg, 2003). Stimuli consisted of common odorants at dilutions spanning several (LFP) recordings (n ϭ 38, see Experimental Procedures) and Laurent, 2001; Laurent, 2002; Laurent et al., 1996; were made from the mushroom body, the target of the Wehr and Laurent, 1996) across dynamic assemblies of AL PNs (Figure 1A). Oscillatory potentials (20-30 Hz) principal neurons (mitral cells, MCs in vertebrates; PNs were evoked when odorants were applied to the anin insects) in the first olfactory relay (olfactory bulb [OB] tenna, revealing coordinated, periodic PN activity, as or antennal lobe [AL]). Each odor representation can previously described (Laurent et al., 1996; Wehr and Laurent, 1996). The oscillatory frequency remained con

Current Biology, 2006