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Decoding temporal information through slow lateral excitation in the olfactory system of insects.

Sensory information is represented in a spatio-temporal code in the antennal lobe, the first processing stage of the olfactory system of insects. We propose a novel mechanism for decoding this information in the next processing stage, the mushroom body. The Kenyon cells in the mushroom body of insects exhibit lateral excitatory connections at their axons. We demonstrate that slow lateral excitation between Kenyon cells allows one to decode sequences of activity in the antennal lobe. We are thus able to clarify the role of the existing connections as well as to demonstrate a novel mechanism for decoding temporal information in neuronal systems. This mechanism complements the variety of existing temporal decoding schemes. It seems that neuronal systems not only have a rich variety of code types but also quite a diversity of algorithms for transforming different codes into each other.

Animals↗

Odorant identification and quality perception following methyl bromide-induced lesions of the olfactory epithelium.

Using a 5-odorant identification confusion matrix task, the authors assessed the consequence of olfactory epithelial damage on odorant quality perception in the rat. After establishing prelesion identification performance, each rat's epithelium was subjected to 330 ppm methyl bromide gas for 6 hr. Comparison of prelesion and 3-day postlesion performance demonstrated a significant decrease in identification as a consequence of 95%-98% epithelial destruction. Further, there was a differential effect of lesion on the ability of different animals to identify the different individual odorants. Evaluation of the anatomical state of the epithelium relative to performance on the identification task demonstrated a significant relationship between the extent and location of anatomical sparing and changes in individual odorant identifications. Assessment of pre- and postlesion quality perception for the individual rats demonstrated a highly significant shift in quality perception that was independent of any decrease in performance. These results provide strong support for the proposition that the regional variations in mucosal sensitivities within and across olfactory receptor gene expression zones are fundamentally important for the encoding of odorant quality.

Animals↗

Target neuron prespecification in the olfactory map of Drosophila.

In Drosophila and mice, olfactory receptor neurons (ORNs) expressing the same receptors have convergent axonal projections to specific glomerular targets in the antennal lobe/olfactory bulb, creating an odour map in this first olfactory structure of the central nervous system. Projection neurons of the Drosophila antennal lobe send dendrites into glomeruli and axons to higher brain centres, thereby transferring this odour map further into the brain. Here we use the MARCM method to perform a systematic clonal analysis of projection neurons, allowing us to correlate lineage and birth time of projection neurons with their glomerular choice. We demonstrate that projection neurons are prespecified by lineage and birth order to form synapses with specific incoming ORN axons, and therefore to carry specific olfactory information. This prespecification could be used to hardwire the fly's olfactory system, enabling stereotyped behavioural responses to odorants. Developmental studies lead us to hypothesize that recognition molecules ensure reciprocally specific connections of ORNs and projection neurons. These studies also imply a previously unanticipated role for precise dendritic targeting by postsynaptic neurons in determining connection specificity.

Animals↗

Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles.

We used neural ensemble recording to examine odor-evoked ensemble patterns in the moth antennal (olfactory) lobe. Different odors are thought to evoke unique spatiotemporal patterns of glomerular activity, but little is known about the population dynamics underlying formation of these patterns. Using a silicon multielectrode array, we observed dynamic network interactions within and between glomeruli. Whereas brief odor pulses repeatedly triggered activity in the same coding ensemble, the temporal pattern of synchronous activity superimposed on the ensemble was neither oscillatory nor odor specific. Rather, synchrony strongly depended on contextual variables such as odor intensity and intermittency. Also, because of emergent inhibitory circuit interactions, odor blends evoked temporal ensemble patterns that could not be predicted from the responses to the individual odorants. Thus even at this early stage of information processing, the timing of odor-evoked neural representations is modulated by key stimulus factors unrelated to the molecular identity of the odor.

Action Potentials↗

Smell images and the flavour system in the human brain.

Flavour perception is one of the most complex of human behaviours. It involves almost all of the senses, particularly the sense of smell, which is involved through odour images generated in the olfactory pathway. In the human brain, the perceptual systems are closely linked to systems for learning, memory, emotion and language, so distributed neural mechanisms contribute to food preference and food cravings. Greater recognition of the role of the brain's flavour system and its connection with eating behaviour is needed for a deeper understanding of why people eat what they do, and to generate better recommendations about diet and nutrition.

Brain↗

Two chemosensory receptors together mediate carbon dioxide detection in Drosophila.

Blood-feeding insects, including the malaria mosquito Anopheles gambiae, use highly specialized and sensitive olfactory systems to locate their hosts. This is accomplished by detecting and following plumes of volatile host emissions, which include carbon dioxide (CO2). CO2 is sensed by a population of olfactory sensory neurons in the maxillary palps of mosquitoes and in the antennae of the more genetically tractable fruitfly, Drosophila melanogaster. The molecular identity of the chemosensory CO2 receptor, however, remains unknown. Here we report that CO2-responsive neurons in Drosophila co-express a pair of chemosensory receptors, Gr21a and Gr63a, at both larval and adult life stages. We identify mosquito homologues of Gr21a and Gr63a, GPRGR22 and GPRGR24, and show that these are co-expressed in A. gambiae maxillary palps. We show that Gr21a and Gr63a together are sufficient for olfactory CO2-chemosensation in Drosophila. Ectopic expression of Gr21a and Gr63a together confers CO2 sensitivity on CO2-insensitive olfactory neurons, but neither gustatory receptor alone has this function. Mutant flies lacking Gr63a lose both electrophysiological and behavioural responses to CO2. Knowledge of the molecular identity of the insect olfactory CO2 receptors may spur the development of novel mosquito control strategies designed to take advantage of this unique and critical olfactory pathway. This in turn could bolster the worldwide fight against malaria and other insect-borne diseases.

Animals↗

Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages.

An essential feature of the organization and function of the vertebrate and insect olfactory systems is the generation of a variety of olfactory receptor neurons (ORNs) that have different specificities in regard to both odorant receptor expression and axonal targeting. Yet the underlying mechanisms that generate this neuronal diversity remain elusive. Here we demonstrate that the Notch signal is involved in the diversification of ORNs in Drosophila melanogaster. A systematic clonal analysis showed that a cluster of ORNs housed in each sensillum were differentiated into two classes, depending on the level of Notch activity in their sibling precursors. Notably, ORNs of different classes segregated their axonal projections into distinct domains in the antennal lobes. In addition, both the odorant receptor expression and the axonal targeting of ORNs were specified according to their Notch-mediated identities. Thus, Notch signaling contributes to the diversification of ORNs, thereby regulating multiple developmental events that establish the olfactory map in Drosophila.

Animals↗

How smell develops.

The mouse's sense of smell is built of approximately 1000 input channels. Each of these consists of a population of olfactory sensory neurons that express the same odorant receptor gene and project their axons to the same targets (glomeruli) in the olfactory bulb. A neuron must choose to express a singular receptor gene from a repertoire of approximately 1000 genes, and its axon must be wired to the corresponding glomerulus, from an array of approximately 1800 glomeruli. Genetic experiments have shown that the expressed odorant receptor specifies axonal choice of the innervated glomerulus, but it is not the only determinant. The mechanisms of odorant receptor gene choice and axonal wiring are central to the functional organization of the mammalian olfactory system. Although principles have emerged, our understanding of these processes is still limited.

Animals↗

Serine protease inhibitor Spi2 mediated apoptosis of olfactory neurons.

The olfactory epithelium of adult mouse, where primary sensory neurons are massively committed to apoptosis by removal of their synaptic target, was used as a model to determine in vivo mechanisms for neuronal cell death induction. A macro-array assay revealed that the death of olfactory neurons is accompanied with over-expression of the serine protease inhibitor Spi2. This over-expression is associated with decreased serine protease activity in the olfactory mucosa. Moreover, in vitro or in vivo inhibition of serine proteases induced apoptotic death of olfactory neuronal cells. Interestingly, Spi2 over-expression is not occurring in olfactory neurons but in cells of the lamina propria, suggesting that Spi2 may act extracellularly as a cell death inducer. In that sense, we present evidence that in vitro Spi2 overexpression generates a secreted signal for olfactory neuron death. Hence, taken together these results document a possible novel mechanism for apoptosis induction that might occur in response to neurodegenerative insults.

Animals↗

Background odour induces adaptation and sensitization of olfactory receptors in the antennae of houseflies.

The presence of background odour was found to have a small but significant effect on the sensitivity of the antennal olfactory system of houseflies, Musca domestica Linnaeus (Diptera: Muscidae), to new pulses of odour. We show that cross-adaptation and cross-sensitization between a background odour of (+/-)-1-octen-3-ol and pulses of (+/-)-1-octen-3-ol, 2-pentanone and R-(+)-limonene can occur, confirming that olfactory receptor cells are sensitive to different odours. Background odour can increase the responses to low concentration odour pulses and decrease the responses to higher concentration odour pulses. It is suggested that background odour has a larger effect on olfactory receptor cells that respond with a tonic increase of spike frequency, giving information about the level of odour concentration, i.e. the 'static' environment. Cells that respond in a phasic way only provide information on the dynamics of the olfactory environment.

Adaptation, Physiological↗