Olfactory sensory input increases gill ventilation in male round gobies (Neogobius melanostomus) during exposure to steroids

In teleostean fish, ventilation increases have been observed in response to low dissolved oxygen levels, visual stimuli, and gustatory cues. However, olfactory sensory input may also stimulate gill ventilation rate. We investigated whether olfactory sensory input mediates gill ventilation responses, as suggested by the observation that steroidal compounds detected by the olfactory system elicited increases in opercular activity in the perciform teleost, the round goby (Neogobius melanostomus). Close parallels between gill ventilation and olfactory responses, led us to conduct an empirical study that used two different olfactory sensory deprivation techniques to seek a causal relationship between olfactory epithelial activity and hyperventilation. Chemical lesion of olfactory sensory neurons or mechanical occlusion of the nasal cavities inhibited gill ventilation responses of reproductive male round gobies to estrone (1,3,5(10)-estratrien-3-ol-17-one) and to ovarian extracts. This direct evidence demonstrates the role of olfactory sensory input for the gill ventilation response to putative reproductive pheromones and may represent an important regulatory mechanism for odorant sampling during pheromone communication.     

Increased behavioral and neuronal sensitivity to sex pheromone after brief odor experience in a moth

Plasticity in the response to stimuli related to food and oviposition cues is well documented in insects. However, responses to cues related to reproduction, for example, sex pheromones, are considered to be innate and thus not affected by experience. Here we show that brief preexposure to sex pheromones, without ensuing reward, lowers the threshold for behavioral response and augments the sensitivity in antennal lobe interneurons to pheromone compared with naive male moths. Thus, the sex pheromone system in insects can be modulated by experience. In addition, we show that the behavioral attraction to sex pheromone increases after preexposure in a time-dependent manner: a short-term effect, possibly a form of sensitization, and a long-term effect after more than 24 h. The behavioral long-term effect is paralleled by an increase in sensitivity of interneurons in the primary olfactory center, whereas the peripheral olfactory system does not change its sensitivity. We hypothesize that short-term sensitization to sex pheromone serves as a kind of alert system, whereas the long-term effect improves male performance when reproductively active females are present.     

Low doses of a neonicotinoid insecticide modify pheromone response thresholds of central but not peripheral olfactory neurons in a pest insect

Insect pest management relies mainly on neurotoxic insecticides, including neonicotinoids, leaving residues in the environment. There is now evidence that low doses of insecticides can have positive effects on pest insects by enhancing various life traits. Because pest insects often rely on sex pheromones for reproduction, and olfactory synaptic transmission is cholinergic, neonicotinoid residues could modify chemical communication. We recently showed that treatments with different sublethal doses of clothianidin could either enhance or decrease behavioural sex pheromone responses in the male moth, Agrotis ipsilon. We investigated now effects of the behaviourally active clothianidin doses on the sensitivity of the peripheral and central olfactory system. We show with extracellular recordings that both tested clothianidin doses do not influence pheromone responses in olfactory receptor neurons. Similarly, in vivo optical imaging does not reveal any changes in glomerular response intensities to the sex pheromone after clothianidin treatments. The sensitivity of intracellularly recorded antennal lobe output neurons, however, is upregulated by a lethal dose 20 times and downregulated by a dose 10 times lower than the lethal dose 0. This correlates with the changes of behavioural responses after clothianidin treatment and suggests the antennal lobe as neural substrate involved in clothianidin-induced behavioural changes.     

Effects of sensory stimuli on the behavioural phase state of the desert locust,Schistocerca gregaria

The nature of stimuli, emanating from other locusts, which are effective in inducing gregarization in the desert locust was investigated. Isolated-reared fifth-instar nymphs were subjected to tactile, visual and olfactory stimuli, presented singly and in combination, and the effect on the behavioural phase state was quantified using logistic regression analysis. Tactile stimulation provided by rolling paper spheres proved to be highly gregarizing, whether presented alone or in combination with the other stimuli. Olfactory and visual stimuli together caused partial behavioural gregarization. Visual stimulation alone was weakly gregarizing after prolonged exposure, while olfactory stimuli alone were ineffective. Nymphs and pre-reproductive and reproductive adults of both sexes were also treated with synthetic adult male `aggregation' pheromone blend (Torto et al., 1994, Journal of Chemical Ecology 20, 1749). No effect of this blend was found on the behavioural phase state, even when visual stimuli were present. Non-locust related stimuli, including wheat odour and flashing lights, were also tested on nymphs. Neither induced any change in the behavioural phase state, indicating that increased sensory flow is not a sufficient explanation for locust-induced behavioural phase change.     

Pheromones enhance somatosensory processing in newt brains through a vasotocin-dependent mechanism

We tested whether the sex pheromones that stimulate courtship clasping in male roughskin newts do so, at least in part, by amplifying the somatosensory signals that directly trigger the motor pattern associated with clasping and, if so, whether that amplification is dependent on endogenous vasotocin (VT). Female olfactory stimuli increased the number of action potentials recorded in the medulla of males in response to tactile stimulation of the cloaca, which triggers the clasp motor reflex, as well as to tactile stimulation of the snout and hindlimb. That enhancement was blocked by exposing the medulla to a V1a receptor antagonist before pheromone exposure. However, the antagonist did not affect medullary responses to tactile stimuli in the absence of pheromone exposure, suggesting that pheromones amplify somatosensory signals by inducing endogenous VT release. The ability of VT to couple sensory systems together in response to social stimulation could allow this peptide to induce variable behavioural outcomes, depending on the immediate context of the social interaction and thus on the nature of the associated stimuli that are amplified. If widespread in vertebrates, this mechanism could account for some of the behavioural variability associated with this and related peptides both within and across species.     

Interactions of mechanical stimuli and sex pheromone information in antennal lobe neurons of a male moth,<Emphasis Type="Italic"> Spodoptera littoralis</Emphasis>

Male moths respond to sex pheromone sources with up-wind flight behaviour. Localization of the odour source requires not only detection of the olfactory stimulus, but also other sensory input regarding, e.g. visual and mechanical stimuli. Thus, integration of different types of sensory input is necessary. It is, however, not known where in the central nervous system the integration of information regarding different sensory modalities takes place. Using intracellular recording and staining techniques, we investigated neurons in the antennal lobe of Spodoptera littoralis, during stimulation with a mechanical stimulus and a sex pheromone. Fifteen percent of all the neurons investigated responded to the mechanical stimulus and the majority of these neurons showed altered responses if the olfactory stimulus was added. A receptor neuron responding only to the wind stimulus was found to arborise in the antennal lobe. Most projection neurons responded with an enhanced action potential frequency to the combined stimulus. In local interneurons, enhancement, depression, or no change of the responses to the wind stimulus was found when the olfactory stimulus was added. The results suggest that neurons present in the antennal lobe integrate mechanosensory and olfactory input, possibly assisting the moths to orient during up-wind flight towards an odour source.     

The functional upregulation of piriform cortex is associated with cross-modal plasticity in loss of whisker tactile inputs

Background

Cross-modal plasticity is characterized as the hypersensitivity of remaining modalities after a sensory function is lost in rodents, which ensures their awareness to environmental changes. Cellular and molecular mechanisms underlying cross-modal sensory plasticity remain unclear. We aim to study the role of different types of neurons in cross-modal plasticity.

Methodology/Principal Findings

In addition to behavioral tasks in mice, whole-cell recordings at the excitatory and inhibitory neurons, and their two-photon imaging, were conducted in piriform cortex. We produced a mouse model of cross-modal sensory plasticity that olfactory function was upregulated by trimming whiskers to deprive their sensory inputs. In the meantime of olfactory hypersensitivity, pyramidal neurons and excitatory synapses were functionally upregulated, as well as GABAergic cells and inhibitory synapses were downregulated in piriform cortex from the mice of cross-modal sensory plasticity, compared with controls. A crosswire connection between barrel cortex and piriform cortex was established in cross-modal plasticity.

Conclusion/Significance

An upregulation of pyramidal neurons and a downregulation of GABAergic neurons strengthen the activities of neuronal networks in piriform cortex, which may be responsible for olfactory hypersensitivity after a loss of whisker tactile input. This finding provides the clues for developing therapeutic strategies to promote sensory recovery and substitution.     

Physiology and morphology of descending neurons in pheromone-processing olfactory pathways in the male moth Manduca sexta

1. We have characterized the responses and structure of olfactory descending neurons (DNs) that reside in the protocerebrum (PC) of the brain of male sphinx moths Manduca sexta and project toward thoracic ganglia. 2. Excitatory responses of DNs to pheromone blends were of two general types: (a) brief excitation (BE) that recovered to background in less than 1 s after the stimulus, and (b) long-lasting excitation (LLE) that outlasted the stimulus by greater than or equal to 1 s and, in many cases, as long as 30 s. Individual pheromone components were ineffective in eliciting LLE. 3. Some neurons showing LLE also exhibited state-dependent responses to pheromonal stimuli. When such neurons were in a state of low background firing, stimulation with pheromone blend elicited LLE. When they were in a state of LLE, an identical stimulus reduced firing for 5-10 s after which firing gradually increased to the initial higher level. 4. Thirteen stained DNs were reconstructed from serial sections for detailed analysis of their morphology in the brain. DNs exhibiting LLE had neurites concentrated in the lateral accessory lobes (LALs) in the protocerebrum and adjacent neuropil. Most DNs exhibiting only BE to pheromonal stimuli and other DNs showing responses only to visual or mechanosensory stimuli did not have branches in the LALs.     

Physiology and morphology of protocerebral olfactory neurons in the male moth Manduca sexta

1. We have used intracellular recording and staining with Lucifer Yellow, followed by reconstruction from serial sections, to characterize the responses and structure of olfactory neurons in the protocerebrum (PC) of the brain of the male sphinx moth Manduca sexta. 2. Many olfactory protocerebral neurons (PCNs) innervate a particular neuropil region lateral to the central body, the lateral accessory lobe (LAL), which appears to be important for processing olfactory information. 3. Each LAL is linked by its constituent neurons to the ipsilateral lateral PC, where projection neurons from the antennal lobe terminate, as well as to other regions of the PC. The LALs are also linked to each other by bilateral neurons with arborizations in each LAL. 4. Some PC neurons showed long-lasting excitation (LLE) that outlasted the olfactory stimuli by greater than or equal to 1 s, and as long as 30 s in some preparations. LLE was more frequently elicited by the sex-pheromone blend than by individual pheromone components. All bilateral neurons that showed LLE had arborizations in the LALs. LLE responses were also recorded in a single local neuron innervating the mushroom body. 5. In some other PC neurons, pheromonal stimuli elicited brief excitations that recovered to background firing rates less than 1 s after stimulation.     

Critical role of intracellular calcium in plasticity mechanisms of defense behavior command neurons LPl1 and PPl1 of Helix lucorum during nociceptive sensitization

The role of intracellular calcium in changes in excitability and responses of defense behavior command neurons LP11 and PP11 of Helix lucorum to sensory stimulation was investigated in semi-intact preparation of a snail during nociceptive sensitization. It was found that application of sensitizing stimuli onto the snail's head initiated membrane depolarization, increase in its excitability as well as depression of neural responses evoked by sensory stimuli in short-term period of sensitization and significant facilitation of neural responses in long-term period of sensitization. To elucidate the contribution of LP11 and PP11 neurons in plasticity rearrangements involved in the mechanisms of sensitization, we applied sensitizing stimuli during strong hyperpolarization of the neurons or after intracellular injection of calcium chelators. Application of sensitizing stimuli during hyperpolarization of the neurons suppressed the increase in membrane excitability and depressed the neural responses evoked by chemical stimulation of snail's head i.m. short- and long-term periods of sensitization. At the same time, synaptic facilitation of neural responses evoked by tactile stimulation of snail's head and foot was observed, which was similar to synaptic facilitation in the control sensitized snail. Intracellular injection of EGTA or BARTA (calcium chelators) before sensitization suppressed synaptic facilitation in neural responses evoked by sensory stimulation. Under these conditions, the increase in excitability was more pronounced then in the control snail neurons. The experimental results suggest the changes in neural responses evoked by sensory stimulation in sensitized snails involve postsynaptic calcium-dependent mechanisms of plasticity in LP11 and PP11 neurons.     

Spatial organization of antennal olfactory sensory neurons in the female Spodoptera littoralis moth: differences in sensitivity and temporal characteristics

Single-cell recordings from olfactory sensory neurons (OSNs), housed in sensilla located at the base and at the tip of the antenna, showed selective responses to plant odors and female sex pheromone in this polyphagous moth. A spatial variation existed in sensitivity: OSNs present on the more proximal segment (P) were more sensitive than those on the more distal segment (D). OSNs of the 2 locations also differed in temporal characteristics: OSNs on P had shorter latency and displayed more phasic responses, whereas those on D had more tonic responses, especially at low stimulus concentrations. The 196 OSNs responding to our 35 monomolecular stimuli in the screening were housed in 32 functional sensillum types: 27 in basiconic, 3 in long-trichoid, 2 in coeloconic, and 3 in auricillic sensilla. The OSNs in basiconic, coeloconic, and auricillic sensilla responded to plant-associated odorants, whereas OSNs in long-trichoid sensilla responded to female-produced sex pheromone components. Short-trichoid sensilla showed spontaneous activity, but no responses to any odorant tested. OSN specificity to plant stimuli ranged from highly specific to broadly tuned, but it did not differ clearly from females in more specialized moths. OSN response diversity is discussed in terms of olfactory coding, behavior, and ecological specialization.     

Chemosensory-induced motor behaviors in fish

Chemical sensory signals play a crucial role in eliciting motor behaviors. We now review the different motor behaviors induced by chemosensory stimuli in fish as well as their neural substrate. A great deal of research has focused on migratory, reproductive, foraging, and escape behaviors but it is only recently that the molecules mediating these chemotactic responses have become well-characterized. Chemotactic responses are mediated by three sensory systems: olfactory, gustatory, and diffuse chemosensory. The olfactory sensory neuron responses to chemicals are now better understood. In addition, the olfactory projections to the central nervous system were recently shown to display an odotopic organization in the forebrain. Moreover, a specific downward projection underlying motor responses to olfactory inputs was recently described.     

Representation of a mixture of pheromone and host plant odor by antennal lobe projection neurons of the silkmoth Bombyx mori

Pheromone-source orientation behavior can be modified by coexisting plant volatiles. Some host plant volatiles enhance the pheromonal responses of olfactory receptor neurons and increase the sensitivity of orientation behavior in the Lepidoptera species. Although many electrophysiological studies have focused on the pheromonal response of olfactory interneurons, the response to the mixture of pheromone and plant odor is not yet known. Using the silkmoth, Bombyx mori, we investigated the physiology of interneurons in the antennal lobe (AL), the primary olfactory center in the insect brain, in response to a mixture of the primary pheromone component bombykol and cis-3-hexen-1-ol, a mulberry leaf volatile. Application of the mixture enhanced the pheromonal responses of projection neurons innervating the macroglomerular complex in the AL. In contrast, the mixture of pheromone and cis-3-hexen-1-ol had little influence on the responses of projection neurons innervating the ordinary glomeruli whereas other plant odors dynamically modified the response. Together this suggests moths can process plant odor information under conditions of simultaneous exposure to sex pheromone.     

Chemoreception in chronically anosmiated fish: A phenomenon of compensatory development of the gustatory system

The main results of studying the phenomenon of recovery of sensitivity to food smells after a long olfactory deprivation found in fish are presented. This ability is detected in fish of different taxonomic groups (Chondrostei, Teleostei) having normally external gustatory receptors. At the behavioral level, this effect starts to manifest itself six weeks upon anosmia, and its development apparently ends during the first three to five months in a partial, rather than complete, recovery of sensitivity to food smells. A more prolonged olfactory deprivation (6–14 months) does not cause any further decrease in the threshold concentration of stimulus solutions. The response to other types of chemical signals (alarm pheromone) is not restored. The ability of fish after a prolonged olfactory deprivation to recover sensitivity to food smells is provided by compensatory processes taking place in the external gustatory system. Recovery occurs due to substances that have taste attraction for fish. Species were found in which the food search response in the norm is provided simultaneously by the olfactory and the gustatory systems. The anosmia of such fish leads only to a partial decrease in the efficiency of search behavior. The complementarity of chemosensory systems, their functional interaction, capacity for a compensatory development, and vicariation are considered sensory mechanisms providing the reliability of realization by fish of the most important behavioral patterns, of food, in particular.     

Food sensitizes C. elegans avoidance behaviours through acute dopamine signalling

Many behavioural states are modulated by food availability and nutritional status. Here, we report that in Caenorhabditis elegans, the presence of an external food source enhances avoidance responses to soluble repellents sensed by the polymodal ASH neurons. This enhancement requires dopamine signalling and is mimicked by exogenous dopamine. Food modulation is dependent on the mechanosensory cilia of the dopaminergic neurons, indicating that dopamine is released in response to sensation of bacteria. Activation of the dopamine neurons leads within seconds to a transient state of increased sensory acuity. In vivo imaging experiments indicate that this dopamine-dependent sensitization results in part from modality-specific increases in the magnitude and duration of gustatory responses in the ASH neurons. The D1-like dopamine receptor DOP-4 acts cell autonomously in ASH to mediate effects on response magnitude. Thus, dopamine functions as a direct signal of the presence of food to control context-dependent behavioural states.     

Peripheral modulation of olfaction by physiological state in the Egyptian leaf worm Spodoptera littoralis (Lepidoptera: Noctuidae)

Insects show behavioural plasticity based on their physiological state. Deprivation from a resource will normally make them more responsive to it or to perform behaviour increasing the probability of encountering such a resource. Modulation of the olfactory system has been shown mainly in the central nervous system, but also in the periphery. In this study, antennal sensitivity of females of the Egyptian cotton leaf worm Spodoptera littoralis to different plant and sex pheromone odours was measured using electroantennography (EAG). Different mating status, age, and feeding status were used to investigate peripheral changes in olfactory responses. Virgin females were found to be more sensitive to plant odours and sex pheromone compared to mated females. Age also had an impact on antennal sensitivity, 2 and 4 days old females being more sensitive than just-emerged ones. Such an increase in sensitivity could be explained by maturation of olfactory receptor neurons after emergence or by an increase in motivation as the available expected life time remaining decreases. Finally, feeding status did not modify the antennal sensitivity of females. A peripheral modulation could thus be demonstrated in the olfactory system of female Spodoptera littoralis at certain life stages.     

Physiology and glomerular projections of olfactory receptor neurons on the antenna of female Heliothis virescens (Lepidoptera: Noctuidae) responsive to behaviorally relevant odors

The neurophysiology and antennal lobe projections of olfactory receptor neurons housed within short trichoid sensilla of female Heliothis virescens F. (Noctuidae: Lepidoptera) were investigated using a combination of cut-sensillum recording and cobalt-lysine staining techniques. Behaviorally relevant odorants, including intra- and inter-sexual pheromonal compounds, plant and floral volatiles were selected for testing sensillar responses. A total of 184 sensilla were categorized into 25 possible sensillar types based on odor responses and sensitivity. Sensilla exhibited both narrow (responding to few odors) and broad (responding to many odors) response spectra. Sixty-six percent of the sensilla identified were stimulated by conspecific odors; in particular, major components of the male H. virescens hairpencil pheromone (hexadecanyl acetate and octadecanyl acetate) and a minor component of the female sex pheromone, (Z)-9-tetradecenal. Following characterization of the responses, olfactory receptor neurons within individual sensilla were stained with cobalt lysine (N=39) and traced to individual glomeruli in the antennal lobe. Olfactory receptor neurons with specific responses to (Z)-9-tetradecenal, a female H. virescens sex pheromone component, projected to the female-specific central large female glomerulus (cLFG) and other glomeruli. Terminal arborizations from sensillar types containing olfactory receptor neurons sensitive to male hairpencil components and plant volatiles were also localized to distinct glomerular locations. This information provides insight into the representation of behaviorally relevant odorants in the female moth olfactory system. Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Low-dose furosemide modulates taste responses in the nucleus of the solitary tract of the rat

Taste-evoked neural responses in the nucleus of the solitary tract (NST) are subject to both excitatory and inhibitory modulation by physiological conditions that influence ingestion. Treatments that induce sodium appetite predominantly reduce NST gustatory responsiveness to sapid stimuli. When sodium appetite is aroused with 10 mg of the diuretic furosemide (Furo), however, NST gustatory neurons exhibit an enhanced responsiveness to NaCl. In addition to inducing a sodium appetite, 10 mg Furo supports a conditioned taste aversion (CTA). A lower, 2-mg dose of Furo induces an equivalent sodium appetite, but not a CTA. To determine whether the anomalous electrophysiological results reflected the adverse effects of the 10-mg dose, we replicated the original experiment but instead used 2 mg of Furo. In chronically prepared, lightly anesthetized rats, the responses of 49 single NST neurons to 12 taste stimuli were recorded after subcutaneous injections of either 2 mg Furo or saline. There was no effect of treatment on NST neural responses to the four standard taste stimuli. In the NaCl concentration series, however, 2 mg Furo evoked significantly higher responses to the two highest concentrations of NaCl. There was no effect of treatment in the sucrose concentration series. Thus, unlike other methods that induce a sodium appetite, Furo increases NST neural responsiveness to NaCl. At least as far as the first central relay, sodium appetite apparently does not depend on specific changes in the sensory neural code for taste.     

Bitter taste stimuli induce differential neural codes in mouse brain

A growing literature suggests taste stimuli commonly classified as "bitter" induce heterogeneous neural and perceptual responses. Here, the central processing of bitter stimuli was studied in mice with genetically controlled bitter taste profiles. Using these mice removed genetic heterogeneity as a factor influencing gustatory neural codes for bitter stimuli. Electrophysiological activity (spikes) was recorded from single neurons in the nucleus tractus solitarius during oral delivery of taste solutions (26 total), including concentration series of the bitter tastants quinine, denatonium benzoate, cycloheximide, and sucrose octaacetate (SOA), presented to the whole mouth for 5 s. Seventy-nine neurons were sampled; in many cases multiple cells (2 to 5) were recorded from a mouse. Results showed bitter stimuli induced variable gustatory activity. For example, although some neurons responded robustly to quinine and cycloheximide, others displayed concentration-dependent activity (p<0.05) to quinine but not cycloheximide. Differential activity to bitter stimuli was observed across multiple neurons recorded from one animal in several mice. Across all cells, quinine and denatonium induced correlated spatial responses that differed (p<0.05) from those to cycloheximide and SOA. Modeling spatiotemporal neural ensemble activity revealed responses to quinine/denatonium and cycloheximide/SOA diverged during only an early, at least 1 s wide period of the taste response. Our findings highlight how temporal features of sensory processing contribute differences among bitter taste codes and build on data suggesting heterogeneity among "bitter" stimuli, data that challenge a strict monoguesia model for the bitter quality.     

Morphological and electrophysiological examination of olfactory sensory neurons during the early developmental prolarval stage of the sea lamprey Petromyzon marinus L

This study examined olfactory sensory neuron morphology and physiological responsiveness in newly hatched sea lamprey, Petromyzon marinus L. These prolarvae hatch shortly after neural tube formation, and stay within nests for approximately 18 days, before moving downstream to silty areas where they burrow, feed and pass to the larval stage. To explore the possibility that the olfactory system is functioning during this prolarval stage, morphological and physiological development of olfactory sensory neurons was examined. The nasal cavity contained an olfactory epithelium with ciliated olfactory sensory neurons. Axons formed aggregates in the basal portion of the olfactory epithelium and spanned the narrow distance between the olfactory epithelium and the brain. The presence of asymmetric synapses with agranular vesicles within fibers in the brain, adjacent to the olfactory epithelium suggests that there was synaptic connectivity between olfactory sensory axons and the brain. Neural recordings from the surface of the olfactory epithelium showed responses following the application of L-arginine, taurocholic acid, petromyzonol sulfate (a lamprey migratory pheromone), and water conditioned by conspecifics. These results suggest that lampreys may respond to olfactory sensory input during the prolarval stage.