Precision and diversity in an odor map on the olfactory bulb

Soucy, Edward R.; Albeanu, Dinu F.; Fantana, Antoniu L.; Murthy, Venkatesh N.; Meister, Markus

doi:10.1038/nn.2262

Cited by 297 publications

(358 citation statements)

References 44 publications

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“…The axons of these OSNs then converge onto two stereotypically located glomeruli in the MOB, thus forming a spatial glomerular map (Ressler et al, 1994;Vassar et al, 1994;Mombaerts et al, 1996). A monomolecular odorant activates a discrete, sparse set of glomeruli (Rubin and Katz, 1999;Uchida et al, 2000;Wachowiak and Cohen, 2001;Soucy et al, 2009), suggesting that olfactory information is encoded by spatially organized glomerular modules. Consistently, mitral/tufted cells respond selectively to odorants that activate their presynaptic OSNs, with their tuning further sharpened by lateral inhibition (Yokoi et al, 1995;Mori et al, 1999;Tan et al, 2010).…”

Section: Odor Representation By Functionally Heterogeneous Populationmentioning

confidence: 99%

“…The axons of OSNs expressing a specific OR typically converge onto two spatially stereotypical glomeruli in the main olfactory bulb (MOB) (Ressler et al, 1994;Vassar et al, 1994;Mombaerts et al, 1996). An odorant activates multiple ORs and produces discrete spatial patterns of glomerular activation (Malnic et al, 1999;Rubin and Katz, 1999;Uchida et al, 2000;Wachowiak and Cohen, 2001;Soucy et al, 2009). Within each glomerulus, a set of 25-50 mitral/tufted cells receive their primary excitatory input from OSNs, and their response selectivity likely reflects that of their associated OR (Mori et al, 1999;Shepherd et al, 2004;Tan et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

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Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice

Zhan¹,

Luo²

2010

J. Neurosci.

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The mammalian piriform cortex receives direct synaptic input from the olfactory bulb and is likely the locus for the formation of odor percept. It remains unclear how individual cortical neurons encode olfactory information in unanesthetized animals. By single-cell recordings from head-restrained awake mice, we studied the odor response profiles of individual neurons in the anterior piriform cortex (aPCX). Neurons were juxtacellularly labeled, and their cell types were determined by their morphology and neurotransmitter phenotypes. We found a considerable level of variability in selectivity patterns among pyramidal neurons (PNs). Approximately one-quarter of PNs were broadly activated by structurally dissimilar odorants, whereas the excitations to the rest of PNs were highly selective. Broad inhibition was only observed from a subpopulation of PNs. GABAergic neurons displayed nonselective excitatory responses to test odorants and rarely exhibited inhibition. In contrast, non-GABAergic nonpyramidal neurons in the deep layer tended to be strongly inhibited by multiple different odorants. Our findings suggest that odor representation is accomplished by both broadly tuned and narrow-tuned PNs in the aPCX of awake animals. In addition, various types of interneurons may play different roles in the intracortical processing of olfactory information.

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Section: Odor Representation By Functionally Heterogeneous Populationmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice

Zhan¹,

Luo²

2010

J. Neurosci.

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“…The neural mechanisms of olfactory processing are a subject of active research (3), and much is known about the encoding of odor identity and concentration (4)(5)(6). However, the issue of ranges of favorable odor concentrations has been less studied.…”

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confidence: 99%

Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans

Narayan

Venkatachalam

Durak

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

112

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Animals find mates and food, and avoid predators, by navigating to regions within a favorable range of available sensory cues. How are these ranges set and recognized? Here we show that male Caenorhabditis elegans exhibit strong concentration preferences for sex-specific small molecule cues secreted by hermaphrodites, and that these preferences emerge from the collective dynamics of a single male-specific class of neurons, the cephalic sensory neurons (CEMs). Within a single worm, CEM responses are dissimilar, not determined by anatomical classification and can be excitatory or inhibitory. Response kinetics vary by concentration, suggesting a mechanism for establishing preferences. CEM responses are enhanced in the absence of synaptic transmission, and worms with only one intact CEM show nonpreferential attraction to all concentrations of ascaroside for which CEM is the primary sensor, suggesting that synaptic modulation of CEM responses is necessary for establishing preferences. A heterogeneous concentrationdependent sensory representation thus appears to allow a single neural class to set behavioral preferences and recognize ranges of sensory cues.T he chemical senses of taste and smell are an important source of sensory input for organisms from worms to humans, and elements of the olfactory system are evolutionarily conserved across metazoa (1, 2). The neural mechanisms of olfactory processing are a subject of active research (3), and much is known about the encoding of odor identity and concentration (4-6). However, the issue of ranges of favorable odor concentrations has been less studied. A reasonable general hypothesis is that physical sensory limitations set perceptual boundaries, limiting the range of an animal to respond favorably. However, there are instances where differences in odor concentrations can have different meanings: For example, both male and female rodents produce the same pheromone at different concentrations (7), and so males need to be able to distinguish between low and high concentrations. Similarly, a very high concentration might signal an adverse environment with overcrowding, in which case the animal is better off looking elsewhere. In such cases, the concentration preferences of the animals are tuned to some optimal value that has a higher probability of a successful outcome. Here, we show that Caenorhabditis elegans exhibits a striking tuning of pheromone concentration preferences, and that this concentration tuning is actively built and maintained by a single class of male-specific neurons, the cephalic sensory neurons (CEMs).The nervous system of C. elegans is famously compact, with 302 hermaphrodite neurons grouped into 118 classes based on morphology and connectivity (8), and 385 male neurons (9-11). Some classes of neurons are sex-specific (Fig. 1A). Members of a class are typically distinguished from each other by their relative anatomical position, such as left/right and dorsal/ventral. Although initially it was thought that members of a class were functionally similar, ...

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“…In the olfactory bulb, axons of olfactory sensory neurons (OSNs) expressing the same odorant receptor (OR) gene converge onto two stereotypically positioned glomeruli (6). The topographic map of the olfactory glomeruli shows remarkable stereotypy among animals of the same species and sometimes across species (6,7). Numerous studies have examined how chemical features are represented in the olfactory bulb (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18).…”

mentioning

confidence: 99%

Distributed representation of chemical features and tunotopic organization of glomeruli in the mouse olfactory bulb

Qiu

Gradwohl

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

137

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In the mammalian brain, similar features of the sensory stimuli are often represented in proximity in the sensory areas. However, how chemical features are represented in the olfactory bulb has been controversial. Questions have been raised as to whether specific chemical features of the odor molecules are represented by spatially clustered olfactory glomeruli. Using a sensitive probe, we have analyzed the glomerular response to large numbers of odorants at single glomerulus resolution. Contrary to the general view, we find that the representation of chemical features is spatially distributed in the olfactory bulb with no discernible chemotopy. Moreover, odor-evoked pattern of activity does not correlate directly with odor structure in general. Despite the lack of spatial clustering or preference with respect to chemical features, some structurally related odors can be similarly represented by ensembles of spatially distributed glomeruli, providing an explanation of their perceptual similarity. Whereas there is no chemotopic organization, and the glomeruli are tuned to odors from multiple classes, we find that the glomeruli are hierarchically arranged into clusters according to their odor-tuning similarity. This tunotopic arrangement provides a framework to understand the spatial organization of the glomeruli that conforms to the organizational principle found in other sensory systems.

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Precision and diversity in an odor map on the olfactory bulb

Cited by 297 publications

References 44 publications

Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice

Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice

Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans

Distributed representation of chemical features and tunotopic organization of glomeruli in the mouse olfactory bulb

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