Set Of Sensory Neurons Research Articles

Cuticular hydrocarbon reception by sensory neurons in basiconic sensilla of the Japanese carpenter ant.

To maintain the eusociality of a colony, ants recognize subtle differences in colony-specific sets of cuticular hydrocarbons (CHCs). The CHCs are received by female-specific antennal basiconic sensilla and processed in specific brain regions. However, it is controversial whether a peripheral or central neural mechanism is mainly responsible for discrimination of CHC blends. In the Japanese carpenter ant, Camponotus japonicus, about 140 sensory neurons (SNs) are co-housed in a single basiconic sensillum and receive colony-specific blends of 18 CHCs. The complexity of this CHC sensory process makes the neural basis of peripheral nestmate recognition difficult to understand. Here, we electrophysiologically recorded responses of single basiconic sensilla to each of 18 synthesized CHCs, and identified CHC responses of each SN co-housed in a single sensillum. Each CHC activated different sets of SNs and each SN was broadly tuned to CHCs. Multiple SNs in a given sensillum fired in synchrony, and the synchronicity of spikes was impaired by treatment with a gap junction inhibitor. These results indicated that SNs in single basiconic sensilla were electrically coupled. Quantitative analysis indicated that the Japanese carpenter ants have the potential to discriminate chemical structures of CHCs based on the combinational patterns of activated SNs. SNs of ants from different colonies exhibited different CHC response spectra. In addition, ants collected from the same colony but bred in separate groups also exhibited different CHC response spectra. These results support the hypothesis that the peripheral sensory mechanism is important for discrimination between nestmate and non-nestmate ants.

Molecular and neuronal mechanisms for amino acid taste perception in the Drosophila labellum

Amino acids are essential nutrients that act as building blocks for protein synthesis. Recent studies in Drosophila have demonstrated that glycine, phenylalanine, and threonine elicit attraction, whereas tryptophan elicits aversion at ecologically relevant concentrations. Here, we demonstrated that eight amino acids, including arginine, glycine, alanine, serine, phenylalanine, threonine, cysteine, and proline, differentially stimulate feeding behavior by activating sweet-sensing gustatory receptor neurons (GRNs) in L-type and S-type sensilla. In turn, this process is mediated by three GRs (GR5a, GR61a, and GR64f), as well as two broadly required ionotropic receptors (IRs), IR25a and IR76b. However, GR5a, GR61a, and GR64f are only required for sensing amino acids in the sweet-sensing GRNs of L-type sensilla. This suggests that amino acid sensing in different type sensilla occurs through dual mechanisms. Furthermore, our findings indicated that ecologically relevant high concentrations of arginine, lysine, proline, valine, tryptophan, isoleucine, and leucine elicit aversive responses via bitter-sensing GRNs, which are mediated by three IRs (IR25a, IR51b, and IR76b). More importantly, our results demonstrate that arginine, lysine, and proline induce biphasic responses in a concentration-dependent manner. Therefore, amino acid detection in Drosophila occurs through two classes of receptors that activate two sets of sensory neurons in physiologically distinct pathways, which ultimately mediates attraction or aversion behaviors.

Is Anopheles gambiae attraction to floral and human skin-based odours and their combination modulated by previous blood meal experience?

BackgroundMosquitoes use odours to find energy resources, blood hosts and oviposition sites. While these odour sources are normally spatio-temporally segregated in a mosquito’s life history, here this study explored to what extent a combination of flower- and human-mimicking synthetic volatiles would attract the malaria vector Anopheles gambiae sensu stricto (s.s.)MethodsIn the laboratory and in large (80 m2) outdoor cages in Tanzania, nulliparous and parous A. gambiae s.s. were offered choices between a blend of human skin volatiles (Skin Lure), a blend of floral volatiles (Vectrax), or a combination thereof. The blends consisted of odours that induce distinct, non-overlapping activation patterns in the olfactory circuitry, in sensory neurons expressing olfactory receptors (ORs) and ionotropic receptors (IRs), respectively. Catches were compared between treatments.ResultsIn the laboratory nulliparous and parous mosquitoes preferred skin odours and combinations thereof over floral odours. However, in semi-field settings nulliparous were significantly more caught with floral odours, whereas no differences were observed for parous females. Combining floral and human volatiles did not augment attractiveness.ConclusionsNulliparous and parous A. gambiae s.s. are attracted to combinations of odours derived from spatio-temporally segregated resources in mosquito life-history (floral and human volatiles). This is favourable as mosquito populations are comprised of individuals whose nutritional and developmental state steer them to diverging odours sources, baits that attract irrespective of mosquito status could enhance overall effectiveness and use in monitoring and control. However, combinations of floral and skin odours did not augment attraction in semi-field settings, in spite of the fact that these blends activate distinct sets of sensory neurons. Instead, mosquito preference appeared to be modulated by blood meal experience from floral to a more generic attraction to odour blends. Results are discussed both from an odour coding, as well as from an application perspective.

Exploring minimal models of sensory integration in nematode C. elegans

To survive, animals must select and execute appropriate actions in response to cues in rich, variable environments. Key to effective sensory processing is the ability to integrate inputs from different sensory modalities in a behaviorally meaningful way. Remarkably, even the simplest animals exhibit non-trivial forms of sensory integration. The roundworm Caenorhabditis elegans is a particularly interesting system in this context, due to the compactness of its small nervous system: unlike the modular organization of vertebrate or even insect brains, in C. elegans, sensory neurons responding in all different modalities (smell, taste, touch, temperature, and much more) all project onto a single circuit, the so called head navigation circuit. How this circuit integrates these inputs to generate appropriate behaviors is a wide open question. In fact, past computational models of this system short circuit the problem, by connecting model sensory neurons directly to motor neurons. That said, this approach may be adequate for modeling sensory responses to a single set of sensory neurons, and a single stimulus type. Here we take the first steps to model sensory integration, with the aim of better understanding the computational role of the navigation circuit and its constituent neurons. We follow an iterative process of model design, validation and refinement against experimental data, and design and implementation of critical in silico experiments to test model predictions. We begin with a model, inspired by results from published sensory integration experiments [1], with a minimal set of neurons directly implicated in the computation. Importantly, this model includes sensory, interneuron and motor layers; it is embodied and fully situated, allowing us to test the model performance against experimentally obtained behavioral metrics. We explicitly demonstrate the necessity of including a full sensorimotor pathway to assess multi-sensory integration. The motor behavior of the worm is relatively well characterized. However, this classification relies mostly on experiments in the absence of external stimuli, or during navigation on gradients of attractive chemicals. Our integration experiments are based on responses to a combination of attractive and repulsive stimuli. Interestingly, we find that the existing repertoire of behaviors fails to account for the animal's responses to repellents. Therefore, a key prediction of our model is the existence of a novel motor behavior mediated by a distinct sensorimotor pathway. Surprisingly, we prove that a fully linear circuit, with rectified motor outputs is sufficient to qualitatively capture complex sensory integration as seen in behavioral data. This result is consistent with experimental findings implicating a single pair of interneurons in this form of sensory integration [1] but dispenses the postulated requirements for nonlinear input-output function of these neurons and feedback connections to the sensory layer. Furthermore, we show that changes in the ratios of afferent synaptic weights from different sensory neurons onto a linear integration interneuron allow precise control over the processing of single and combined stimuli. Implementation of novel sensory receptor properties and a sigmoidal activation function in the integration interneuron results in quantitatively correct model performance. Finally, we study the behavior of defective worms, (with virtually mutations or ablated neurons) and use this analysis to predict a role for additional interneurons in the navigation circuit.

Differential bulbar and extrabulbar projections of diverse olfactory receptor neuron populations in the adult zebrafish (Danio rerio)

Immunohistochemical methods were used to characterize the expression of two calcium-binding proteins, calretinin (CR) and S100, in the olfactory rosette of the adult zebrafish. These proteins are expressed in different sets of sensory neurons, and together represent a large proportion of these cells. Double immunofluorescence for CR and Gα(olf) protein, and CR immunoelectron microscopy, indicated that most CR-immunoreactive (ir) cells were ciliary neurons. Differential S100- and CR-ir projections to glomerular fields of the olfactory bulb were also observed, although these projections overlap in some glomeruli. Application of the carbocyanine dye DiI to either S100-ir or CR-ir glomerular regions led to labeling of cells mostly similar to S100-ir and CR-ir neurons, respectively. Instead, these bulbar regions project to similar telencephalic targets. On the other hand, antibodies against keyhole limpet hemocyanin (KLH)-stained numerous sensory cells in the olfactory rosette, including cells that were CR- and S100-negative. This antiserum also stained most primary bulbar projections and revealed extrabulbar olfactory primary projections coursing to the ventral area of the telencephalon through the medial olfactory tract. This extrabulbar projection was confirmed by tract-tracing with DiI. A loose association of this extrabulbar primary olfactory projection and the catecholaminergic populations of the ventral area was also observed with double tyrosine hydroxylase/KLH-like immunohistochemistry. Comparison between KLH-like-ir pathways and the structures revealed by FMRFamide immunohistochemistry (a marker of terminal ganglion cells and fibers) indicated that the KLH-like-ir extrabulbar projection was different from the terminal nerve system. The significance of the extrabulbar olfactory projection of zebrafish is discussed.

Evolution of bistable dynamics in spiking neural controllers for agents performing olfactory attraction and aversion

Research on the olfactory system of Drosophila has shown that individual glomeruli mediate innate olfactory attraction and aversion [1]. The authors showed that increasing concentrations of vinegar result in excitation of an additional glomerulus, which can initiate a behavioral switch from attraction to aversion. This implies that high concentrations of vinegar activate a specific set of sensory neurons that is not activated by low concentrations. In this research, we used a genetic algorithm to evolve spiking neural controllers for agents that were attracted by low concentrations of a simulated chemical but were repelled by high concentrations of the same chemical. We investigated how the evolved neural controllers could encode information about the chemical concentration to perform this task. We also wanted to see if the neural controllers needed to be equipped with different types of olfactory sensory neurons or if only one type was sufficient. We first performed experiments where the agent could use only one kind of sensors that responded to the whole range of concentrations. In a second set of experiments, the agents could use an additional pair of sensors only activated by high concentrations. In our model, simulated agents could move in a 2D environment and the neural controller was placed on a 2D substrate. We used leaky integrate-and-fire neurons with temporal synaptic integration and transmission delays. The neural network was generated using a developmental model with an indirect encoding strategy that mapped an artificial genome onto the network connectivity. Our model was able to evolve neural controllers with complex dynamics that used both neuronal firing rates and temporal coincidence to encode information about the olfactory environment. Surprisingly, the fittest evolved agent did not require an additional pair of sensors that responded only to high concentrations, different from what has been observed in Drosophila. A central feature that implemented the attraction and aversion behavior of the agent was the combination of bilateral inhibition and excitatory self-connections. This resulted in a cascade of two bi-stable systems, one of which was responsible for basic motor control and for attraction at low concentrations. The second bi-stable system controlled the switching between the states of the first bi-stable system when the concentration was too high. These results show that an artificial life based approach to the study of natural processes like olfaction is feasible, and that it can suggest neural coding strategies that may be used by natural systems.

The Drosophila pheromone cVA activates a sexually dimorphic neural circuit

Courtship is an innate sexually dimorphic behaviour that can be observed in naive animals without previous learning or experience, suggesting that the neural circuits that mediate this behaviour are developmentally programmed. In Drosophila, courtship involves a complex yet stereotyped array of dimorphic behaviours that are regulated by Fru(M), a male-specific isoform of the fruitless gene. Fru(M) is expressed in about 2,000 neurons in the fly brain, including three subpopulations of olfactory sensory neurons and projection neurons (PNs). One set of Fru(+) olfactory neurons expresses the odorant receptor Or67d and responds to the male-specific pheromone cis-vaccenyl acetate (cVA). These neurons converge on the DA1 glomerulus in the antennal lobe. In males, activation of Or67d(+) neurons by cVA inhibits courtship of other males, whereas in females their activation promotes receptivity to other males. These observations pose the question of how a single pheromone acting through the same set of sensory neurons can elicit different behaviours in male and female flies. Anatomical or functional dimorphisms in this neural circuit might be responsible for the dimorphic behaviour. We therefore developed a neural tracing procedure that employs two-photon laser scanning microscopy to activate the photoactivatable green fluorescent protein. Here we show, using this technique, that the projections from the DA1 glomerulus to the protocerebrum are sexually dimorphic. We observe a male-specific axonal arbor in the lateral horn whose elaboration requires the expression of the transcription factor Fru(M) in DA1 projection neurons and other Fru(+) cells. The observation that cVA activates a sexually dimorphic circuit in the protocerebrum suggests a mechanism by which a single pheromone can elicit different behaviours in males and in females.

Multiple Pathways Give a No-Frills Nervous System a Flexible Oxygen Response

The tiny nematode Caenorhabditis elegans spends most of its life in the soil, searching for an abundance of food and just the right amount of oxygen. But what happens when optimal oxygen and food supplies can’t be found in the same place? More generally, how does the organization of an animal’s neural networks help it produce the right behaviors in competing contexts? With only 302 neurons, and powerful genetic tools available to the researchers who study it, C. elegans is a valuable subject for exploring the neural control of behavior. Previous work has identified just three kinds of neurons as important for sensing and responding to oxygen. These neurons express a family of genes that appear to encode enzymes called soluble guanylate cyclases (sGCs). C. elegans sGCs bind oxygen and initiate signaling cascades within the neurons. Animals lacking certain members of this gene family no longer respond normally to oxygen. But, since other neurons also express sGCs, these neurons could play a role in oxygen sensing as well. C. elegans’ response to high ambient oxygen (above 14%) in the presence of food depends on the activity of a neuropeptide receptor called NPR-1. Naturally occurring npr-1(215F) nematode strains and laboratory-induced npr-1(lf) strains avoid high oxygen whether or not food is present and aggregate in the presence of food. Another naturally occurring strain, npr-1(215V), avoids high oxygen only when food is absent. How does npr-1(215V) integrate the information about the two stimuli? To learn the answer, Andy Chang, Cornelia Bargmann, and colleagues systematically assessed the possible role of a number of neurons and genes using mutation and selective gene replacement. Their experiments involved first removing the function of a particular gene (for example, an sGC), then assessing the change in response to oxygen (by looking for changes in the typical distribution of animals along an oxygen gradient), and then finally replacing that gene in only one kind of neuron to see if normal function returns. Their results revealed some surprises. Previous studies showed that the neurons URX, AQR, and PQR suppress npr-1(215V)’s locomotor response to oxygen. In this study, the researchers found another set of neurons—SDQ, ALN, and PLN—expressing sGCs that were able to process information about ambient oxygen levels. They also found that the ion channels OSM-9 and OCR-2 in yet another set of neurons (ADF and ASH) promote high-oxygen avoidance. The researchers concluded that these neurons interact with sGC neurons to produce high-oxygen avoidance and modulation of this response by food. Another aggregating strain of C. elegans, daf-7, gave the researchers yet another angle to explore. In crowded, low-food conditions, the developmental gene daf-7 shows low activity and the nematode enters an alternative larva stage called a dauer. The researchers found that daf-7 mutants avoided high oxygen with or without food, suggesting that daf-7, like npr-1(215V), is involved in suppressing high-oxygen avoidance in the presence of food. Further studies suggested that food might be exerting its influence in part by altering daf-7 expression in ASI neurons. The researchers also found that daf-7 mutants expressed higher levels of a gene involved in serotonin synthesis in ADF neurons, suggesting that ADF may represent a convergence point for networks that promote response to high oxygen and those that suppress it. The researchers concluded that at least four sets of sensory neurons (some or all of URX, AQR, and PQR; some or all of SDQ, ALN, and PLN; ADF; and ASH) in C. elegans promote high-oxygen avoidance, and that these neurons can be suppressed in some cases by other neurons that provide information about food availability. The result is an integrated system that allows this simple organism to respond to its complex environment in an equally complex manner. Electrophysiological examination of other “simple” systems, like motor circuits in the leech and the lobster, has demonstrated comparable complexity in well-defined neural networks, with context-dependent neuronal participation in a particular behavior. The principles uncovered in these systems are likely to be applicable to even more complex brains, whose neuronal circuits are not amenable to comparable dissection.

Mustard High

Mustard and horseradish get their zing from isothiocyanates, which depolarize nociceptors (sensory neurons that detect pain). Jordt et al. used calcium imaging to investigate the mechanism by which allyl isothiocyanate (mustard oil) acts and found that it elicited an increase in intracellular calcium in about 35% of dissociated rat trigeminal sensory neurons. Neurons stimulated by Δ 9 -tetrahydrocannabinol (THC, the psychoactive ingredient in marijuana) were also sensitive to mustard oil. THC- and mustard oil-dependent increases in calcium were sensitive to ruthenium red, which blocks some transient receptor potential (TRP) family cation channels, as were currents induced by these compounds measured by whole-cell patch clamp analysis. HEK 293 cells transfected with rat or human ANKTM1 (a TRP family channel) responded to mustard oil and various other natural isothiocyanate compounds, as well as to THC, but not to capsaicin (the active ingredient in chili papers, which activates the TRPV1 cation channel), with increases in intracellular calcium. Similarly, isothiocyanates, wasabi and mustard extracts, and THC all elicited currents in Xenopus oocytes expressing ANKTM1. These data suggest that THC and mustard oil excite the same set of sensory neurons through similar mechanisms involving the TRP family channel ANKTM1 and support previous research suggesting a role for TRP channels as cannabinoid receptors. S.-E. Jordt, D. M. Bautista, H.-H. Chuang, D. D. McKemy, P. M. Zygmunt, E. D. Hogestatt, I. D. Meng, D. Julius, Nature 427 , 260-265 (2004). [Online Journal]

Regional expression of three homeobox transcripts in the inner ear of zebrafish embryos

The inner ear of all jawed vertebrates arises from the epithelium of the otic vesicle and contains three semicircular canals, otoliths, and- sets of sensory neurons, all positioned precisely within the cranium to detect head orientation and movement. The msh-C gene and two new homeobox genes, msh-D and a gene related to distal-less, dlx-3, are each expressed in distinct regions of the otic vesicle during its early development in zebrafish embryos. Cells in the ectoderm express dlx-3 before induction of the otic vesicle, suggesting that dlx-3 has an early function in this process. Later, cells aligned with the future axes of the semicircular canals specifically express either dlx-3 or msh-D. Even later, sensory hair cells express msh-C and msh-D, while other cells of the epithelium express dlx-3. The early expression of these genes could specify the orientation and morphogenesis of the inner ear, whereas their later expression could specify the fates of particular cell types.

Selective modulation of spike duration by serotonin and the neuropeptides, FMRFamide, SCPB, buccalin and myomodulin in different classes of mechanoafferent neurons in the cerebral ganglion of Aplysia

An examination of the cellular properties and synaptic outputs of mechanoafferent neurons found on the ventrocaudal surface of the cerebral ganglion of Aplysia indicated that the cerebral mechanoafferent (CM) neurons are a heterogeneous population of cells. Based on changes in action potential duration in response to bath applications of 5-HT in the presence of TEA, CM neurons could be divided into 2 broad classes: mechanoafferents whose spikes broaden in response to 5-HT (CM-SB neurons) and mechanoafferents whose spikes narrow in response to 5-HT (CM-SN neurons). Morphological and electrophysiological studies of the CM-SN neurons indicated that they were comprised of previously identified interganglionic cerebral-buccal mechanoafferent (ICBM) neurons and a novel set of sensory neurons that send an axon into the LLAB cerebral nerve and have perioral zone receptive fields that are similar to those of ICBM neurons. Changes in spike width due to 5-HT were correlated with changes in synaptic output as indicated by the magnitudes of EPSPs evoked in postsynaptic neurons. Electrical stimulation of cerebral nerves and connectives also produced spike narrowing or broadening, and the sign of the effect was a function of the parameters of stimulation. Both heterosynaptic facilitation and heterosynaptic depression of EPSPs evoked in follower cells could be demonstrated. A variety of putative neuromodulators other than 5-HT were also found to affect the duration of action potentials in both classes of CM neurons. FMRFamide had effects opposite to that of 5-HT. SCPB and a recently characterized Aplysia neuropeptide, buccalin, broadened the spikes of both CM classes. Another neuropeptide, myomodulin, decreased the duration of CM-SB neuron spikes but had no effect on CM-SN spikes. Since the CM neurons appear to mediate a variety of competing behaviors, including feeding, locomotion, and defensive withdrawal, the various neuromodulator actions may contribute to the mechanisms whereby behaviors are selected and modified.

Multifunctional interneurons in behavioral circuits of the medicinal leech.

We are using the medicinal leech to study the neuronal basis of behavioral choice. In particular, we are recording from neurons, both extracellularly and intracellularly, in preparations that can express three different behaviors: the shortening reflex, crawling and swimming. We have found that particular mechanosensory neurons can elicit any of the behaviors, and that the movements are produced by just four sets of muscles, each controlled by a small number of motor neurons. Hence, there must be three different pattern-generating neuronal circuits, each of which can be activated by the same set of sensory neurons. We are studying how the choice is made among the three behaviors by recording, while one behavior is being performed, from neurons known to be involved in the initiation of the other two. We have found that an interneuron, cell 204, which is known to initiate and maintain swimming, is also active during shortening and crawling. The activity level in this interneuron can influence whether a mechanosensory stimulus produces shortening or swimming. The neuronal mechanisms by which this choice is normally effected awaits further elucidation of the circuits that elicit and generate shortening and crawling.

Peripheral Neurogenesis in "Drosophila"

During metamorphosis, the wings of Drosophila form from the wing imaginal discs of the larva and acquire a highly specific set of sensory neurons. The developing neurons leave the cell cycle, differentiate, and grow their axons in a fixed order. The axons follow stereotyped paths through nonneural tissue, fasciculate together, and ultimately reach the CNS, where they form regular arborizations. Neurons differentiating ectopically (in mutant flies) grow irregularly and often away from the CNS. We are analyzing the factors that generate order and appropriate polarity along the normal nerve paths; lack of order and of consistent polarity prevail elsewhere. (Accepted for publication 1 June 1983)