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The European corn borer Ostrinia nubilalis (ECB; Lepidoptera: Crambidae) is a widely recognized pest of agricultural significance over much of the northern hemisphere. Because of the potential value of pheromone-based control, there has been considerable effort devoted to elucidation of the ECB chemical ecology. The species is polymorphic regarding its female-produced pheromone. Partly because of this feature, over the years the ECB has become a model to study pheromone evolution. This review should assist in identifying new areas of pheromone research by providing an overview of the literature produced on this subject for the ECB since the late 1960's.

In the mouse, each class of olfactory receptor neurons expressing a given odorant receptor has convergent axonal projections to two specific glomeruli in the olfactory bulb, thereby creating an odour map. However, it is unclear how this map is represented in the olfactory cortex. Here we combine rabies-virus-dependent retrograde mono-trans-synaptic labelling with genetics to control the location, number and type of ‘starter’ cortical neurons, from which we trace their presynaptic neurons. We find that individual cortical neurons receive input from multiple mitral cells representing broadly distributed glomeruli. Different cortical areas represent the olfactory bulb input differently. For example, the cortical amygdala preferentially receives dorsal olfactory bulb input, whereas the piriform cortex samples the whole olfactory bulb without obvious bias. These differences probably reflect different functions of these cortical areas in mediating innate odour preference or associative memory. The trans-synaptic labelling method described here should be widely applicable to mapping connections throughout the mouse nervous system. Scent tracking In the mouse, glomeruli in the olfactory bulb receive projections from single classes of olfactory neurons, thereby forming an odour map. Information from the glomeruli is then relayed to the cortex but the projection patterns from individual glomeruli are not known. Three papers now examine the details of this projection. Luo and colleagues use a combination of genetics and retrograde mono-trans-synaptic rabies virus labelling. They trace the presynaptic connections of individual cortical neurons and find no evidence of connections supporting a stereotyped odour map in the cortex, but see systematic topographical differences in amygdala connectivity. The lack of stereotypical cortical projection is corroborated, both at the level of bulk axonal patterning and in projections of individually labelled neurons, by two papers — one from the Axel laboratory, and one from the Baldwin laboratory — that examine the anterograde projections from individual glomeruli. Together, these findings provide anatomical evidence for combinatorial processing of information from diverse glomeruli by cortical neurons and may also reflect different functions of various areas in mediating innate or learned odour preferences.

The cortical amygdala is necessary and sufficient for processing odours that evoke aversive and attractive responses without learning. Cortical processing of odour stimuli Sensory neurons in the nose transmit information to various areas in the brain via the olfactory bulb. The roles of these different brain areas, and how they code and process odour-related information, are not well understood. Richard Axel and colleagues show that one area, the cortical amygdala, is both necessary and sufficient for processing odours that evoke aversive and attractive responses without prior learning. Such signals may play a role in shaping learned adaptive responses linking specific odours to experience. Innate behaviours are observed in naive animals without prior learning or experience, suggesting that the neural circuits that mediate these behaviours are genetically determined and stereotyped. The neural circuits that convey olfactory information from the sense organ to the cortical and subcortical olfactory centres have been anatomically defined 1 , 2 , 3 , but the specific pathways responsible for innate responses to volatile odours have not been identified. Here we devise genetic strategies that demonstrate that a stereotyped neural circuit that transmits information from the olfactory bulb to cortical amygdala is necessary for innate aversive and appetitive behaviours. Moreover, we use the promoter of the activity-dependent gene arc to express the photosensitive ion channel, channelrhodopsin, in neurons of the cortical amygdala activated by odours that elicit innate behaviours. Optical activation of these neurons leads to appropriate behaviours that recapitulate the responses to innate odours. These data indicate that the cortical amygdala plays a critical role in generating innate odour-driven behaviours but do not preclude its participation in learned olfactory behaviours.

The evolution of animal behaviour is poorly understood 1 , 2 . Despite numerous correlations between interspecific divergence in behaviour and nervous system structure and function, demonstrations of the genetic basis of these behavioural differences remain rare 3 – 5 . Here we develop a neurogenetic model, Drosophila sechellia , a species that displays marked differences in behaviour compared to its close cousin Drosophila melanogaster 6 , 7 , which are linked to its extreme specialization on noni fruit ( Morinda citrifolia ) 8 – 16 . Using calcium imaging, we identify olfactory pathways in D. sechellia that detect volatiles emitted by the noni host. Our mutational analysis indicates roles for different olfactory receptors in long- and short-range attraction to noni, and our cross-species allele-transfer experiments demonstrate that the tuning of one of these receptors is important for species-specific host-seeking. We identify the molecular determinants of this functional change, and characterize their evolutionary origin and behavioural importance. We perform circuit tracing in the D. sechellia brain, and find that receptor adaptations are accompanied by increased sensory pooling onto interneurons as well as species-specific central projection patterns. This work reveals an accumulation of molecular, physiological and anatomical traits that are linked to behavioural divergence between species, and defines a model for investigating speciation and the evolution of the nervous system. A neurogenetic model, Drosophila sechellia —a relative of Drosophila melanogaster that has developed an extreme specialization for a single host plant—sheds light on the evolution of interspecific differences in behaviour.

Scent tracking In the mouse, glomeruli in the olfactory bulb receive projections from single classes of olfactory neurons, thereby forming an odour map. Information from the glomeruli is then relayed to the cortex but the projection patterns from individual glomeruli are not known. Three papers now examine the details of this projection. Luo and colleagues use a combination of genetics and retrograde mono-trans-synaptic rabies virus labelling. They trace the presynaptic connections of individual cortical neurons and find no evidence of connections supporting a stereotyped odour map in the cortex, but see systematic topographical differences in amygdala connectivity. The lack of stereotypical cortical projection is corroborated, both at the level of bulk axonal patterning and in projections of individually labelled neurons, by two papers — one from the Axel laboratory, and one from the Baldwin laboratory — that examine the anterograde projections from individual glomeruli. Together, these findings provide anatomical evidence for combinatorial processing of information from diverse glomeruli by cortical neurons and may also reflect different functions of various areas in mediating innate or learned odour preferences. Sensory information is transmitted to the brain where it must be processed to translate stimulus features into appropriate behavioural output. In the olfactory system, distributed neural activity in the nose is converted into a segregated map in the olfactory bulb 1 , 2 , 3 . Here we investigate how this ordered representation is transformed in higher olfactory centres in mice. We have developed a tracing strategy to define the neural circuits that convey information from individual glomeruli in the olfactory bulb to the piriform cortex and the cortical amygdala. The spatial order in the bulb is discarded in the piriform cortex; axons from individual glomeruli project diffusely to the piriform without apparent spatial preference. In the cortical amygdala, we observe broad patches of projections that are spatially stereotyped for individual glomeruli. These projections to the amygdala are overlapping and afford the opportunity for spatially localized integration of information from multiple glomeruli. The identification of a distributive pattern of projections to the piriform and stereotyped projections to the amygdala provides an anatomical context for the generation of learned and innate behaviours.

Scent tracking In the mouse, glomeruli in the olfactory bulb receive projections from single classes of olfactory neurons, thereby forming an odour map. Information from the glomeruli is then relayed to the cortex but the projection patterns from individual glomeruli are not known. Three papers now examine the details of this projection. Luo and colleagues use a combination of genetics and retrograde mono-trans-synaptic rabies virus labelling. They trace the presynaptic connections of individual cortical neurons and find no evidence of connections supporting a stereotyped odour map in the cortex, but see systematic topographical differences in amygdala connectivity. The lack of stereotypical cortical projection is corroborated, both at the level of bulk axonal patterning and in projections of individually labelled neurons, by two papers — one from the Axel laboratory, and one from the Baldwin laboratory — that examine the anterograde projections from individual glomeruli. Together, these findings provide anatomical evidence for combinatorial processing of information from diverse glomeruli by cortical neurons and may also reflect different functions of various areas in mediating innate or learned odour preferences. Sensory information may be represented in the brain by stereotyped mapping of axonal inputs or by patterning that varies between individuals. In olfaction, a stereotyped map is evident in the first sensory processing centre, the olfactory bulb (OB), where different odours elicit activity in unique combinatorial patterns of spatially invariant glomeruli 1 , 2 . Activation of each glomerulus is relayed to higher cortical processing centres by a set of ∼20–50 ‘homotypic’ mitral and tufted (MT) neurons 3 . In the cortex, target neurons integrate information from multiple glomeruli to detect distinct features of chemically diverse odours 4 , 5 , 6 . How this is accomplished remains unclear, perhaps because the cortical mapping of glomerular information by individual MT neurons has not been described. Here we use new viral tracing and three-dimensional brain reconstruction methods to compare the cortical projections of defined sets of MT neurons. We show that the gross-scale organization of the OB is preserved in the patterns of axonal projections to one processing centre yet reordered in another, suggesting that distinct coding strategies may operate in different targets. However, at the level of individual neurons neither glomerular order nor stereotypy is preserved in either region. Rather, homotypic MT neurons from the same glomerulus innervate broad regions that differ between individuals. Strikingly, even in the same animal, MT neurons exhibit extensive diversity in wiring; axons of homotypic MT pairs diverge from each other, emit primary branches at distinct locations and 70–90% of branches of homotypic and heterotypic pairs are non-overlapping. This pronounced reorganization of sensory maps in the cortex offers an anatomic substrate for expanded combinatorial integration of information from spatially distinct glomeruli and predicts an unanticipated role for diversification of otherwise similar output neurons.

This study demonstrates an epigenetic inheritance of a learned behavior that is transmitted across generations via the gametes whereby learning about a specific olfactory stimulus changes brain structure and the behavior of future generations. Specifically, Dias and Ressler show that behavioral response to olfactory fear conditioning in male parents is transmitted to their offspring via DNA methylation changes in the corresponding odorant receptor gene in the sperm, which is accompanied by the changes to the corresponding neuroanatomical structure that mediates olfactory perception. Using olfactory molecular specificity, we examined the inheritance of parental traumatic exposure, a phenomenon that has been frequently observed, but not understood. We subjected F0 mice to odor fear conditioning before conception and found that subsequently conceived F1 and F2 generations had an increased behavioral sensitivity to the F0-conditioned odor, but not to other odors. When an odor (acetophenone) that activates a known odorant receptor ( Olfr151 ) was used to condition F0 mice, the behavioral sensitivity of the F1 and F2 generations to acetophenone was complemented by an enhanced neuroanatomical representation of the Olfr151 pathway. Bisulfite sequencing of sperm DNA from conditioned F0 males and F1 naive offspring revealed CpG hypomethylation in the Olfr151 gene. In addition, in vitro fertilization, F2 inheritance and cross-fostering revealed that these transgenerational effects are inherited via parental gametes. Our findings provide a framework for addressing how environmental information may be inherited transgenerationally at behavioral, neuroanatomical and epigenetic levels.

In Drosophila , olfactory sensory neurons project to spatially invariant loci (glomeruli) and stereotyped circuitry is maintained in projections to a brain centre thought to mediate innate behaviours; here it is shown that neurons of the mushroom body, a centre that translates olfactory information into learned behaviours, integrate input from an apparently random combination of glomeruli, which could allow the fly to contextualize novel sensory experiences. Direct and indirect olfactory inputs Some odours elicit fixed, innate behavioural responses, based on stereotyped neuronal circuits — or 'labelled lines' — that form direct links to the deeper layers of the brain. It has been suggested that less stereotyped circuits allow other odours to acquire their behavioural 'valence' based on individual experience, but such randomness is harder to demonstrate than structure. Now Richard Axel and colleagues have used sophisticated tracing of neural connectivity in the fruitfly to show that projections from the peripheral olfactory system to the associative memory centre in the mushroom bodies are largely random, which may allow the animal to contextualize new sensory experiences. The mushroom body in the fruitfly Drosophila melanogaster is an associative brain centre that translates odour representations into learned behavioural responses 1 . Kenyon cells, the intrinsic neurons of the mushroom body, integrate input from olfactory glomeruli to encode odours as sparse distributed patterns of neural activity 2 , 3 . We have developed anatomic tracing techniques to identify the glomerular origin of the inputs that converge onto 200 individual Kenyon cells. Here we show that each Kenyon cell integrates input from a different and apparently random combination of glomeruli. The glomerular inputs to individual Kenyon cells show no discernible organization with respect to their odour tuning, anatomic features or developmental origins. Moreover, different classes of Kenyon cells do not seem to preferentially integrate inputs from specific combinations of glomeruli. This organization of glomerular connections to the mushroom body could allow the fly to contextualize novel sensory experiences, a feature consistent with the role of this brain centre in mediating learned olfactory associations and behaviours.

The rostral migratory stream (RMS) is the main pathway by which newly born subventricular zone cells reach the olfactory bulb (OB) in rodents. However, the RMS in the adult human brain has been elusive. We demonstrate the presence of a human RMS, which is unexpectedly organized around a lateral ventricular extension reaching the OB, and illustrate the neuroblasts in it. The RMS ensheathing the lateral olfactory ventricular extension, as seen by magnetic resonance imaging, cell-specific markers, and electron microscopy, contains progenitor cells with migratory characteristics and cells that incorporate 5-bromo-2'-deoxyuridine and become mature neurons in the OB.

The nervous system flexibly processes information under different conditions. To do this, neural networks frequently rely on uniform expression of modulatory receptors by distinct classes of neurons to fine tune the computations supported by each neuronal class. Here, we explore an alternate organization in which one population of neurons in the olfactory system of Drosophila expresses all of the receptors for the modulator serotonin. We find extensive, heterogeneous receptor co-expression by ventral projection neurons (v-PNs), with many receptor combinations present. Despite overlap in glomerular innervation of v-PNs expressing each serotonin receptor, their axon terminals innervate largely distinct zones within a higher order olfactory region. Serotonin differentially modulates odor-evoked responses of v-PNs with distinct receptor expression and these v-PNs synapse upon separate sets of third order olfactory neurons. This functional organization implies that serotonin differentially modulates the responses of v-PNs that participate in divergent, downstream olfactory circuits. Jonaitis et al demonstrate that serotonin differentially modulates feedforward inhibitory neurons in the olfactory system of Drosophila which likely reflects odor categorization in higher order brain regions.