Potential roles of smell and taste in the orientation behaviour of coral-reef fish larvae: insights from morphology

An ontogenetic analysis of the olfactory organ and the number and distribution of internal taste buds was carried out in two neon gobies (Elacatinus lori and Elacatinus colini) with the goal of revealing morphological trends that might inform an understanding of the roles of olfaction and taste in larval orientation behaviour. The pattern of development of the olfactory organ is unremarkable and enclosure of the olfactory epithelium occurs concurrently with metamorphosis and settlement in both species. Like other gobies, juvenile and adult E. lori and E. colini lack complex olfactory lamellae, and lack the accessory nasal sacs present in some adult gobies that could facilitate active olfactory ventilation (i.e., sniffing). A small number of internal taste buds are present at hatch with most found in the caudal region of the buccal cavity (on gill arches, roof of buccal cavity). As taste bud number increases, they demonstrate an anterior spread to the lips, buccal valves and tongue (i.e., tissue covering the basihyal). In the absence of an active ventilatory mechanism for the olfactory organs, the water that moves through the buccal cavity with cyclic gill ventilation may provide chemical cues allowing the internal taste buds to play a role in chemical-mediated orientation and reef-seeking behavior in pelagic larval fishes.     

Smelling of odorous sex hormone-like compounds causes sex-differentiated hypothalamic activations in humans.

The anatomical pathways for processing of odorous stimuli include the olfactory nerve projection to the olfactory bulb, the trigeminal nerve projection to somatosensory and insular cortex, and the projection from the accessory olfactory bulb to the hypothalamus. In the majority of tetrapods, the sex-specific effects of pheromones on reproductive behavior is mediated via the hypothalamic projection. However, the existence of this projection in humans has been regarded as improbable because humans lack a discernable accessory olfactory bulb. Here, we show that women smelling an androgen-like compound activate the hypothalamus, with the center of gravity in the preoptic and ventromedial nuclei. Men, in contrast, activate the hypothalamus (center of gravity in paraventricular and dorsomedial nuclei) when smelling an estrogen-like substance. This sex-dissociated hypothalamic activation suggests a potential physiological substrate for a sex-differentiated behavioral response in humans.     

Loss of smelling is an early marker of aging and is associated with inflammation and DNA damage in C57BL/6J mice

Olfactory dysfunction is a prevalent symptom and an early marker of age-related neurodegenerative diseases in humans, including Alzheimer's and Parkinson's Diseases. However, as olfactory dysfunction is also a common symptom of normal aging, it is important to identify associated behavioral and mechanistic changes that underlie olfactory dysfunction in nonpathological aging. In the present study, we systematically investigated age-related behavioral changes in four specific domains of olfaction and the molecular basis in C57BL/6J mice. Our results showed that selective loss of odor discrimination was the earliest smelling behavioral change with aging, followed by a decline in odor sensitivity and detection while odor habituation remained in old mice. Compared to behavioral changes related with cognitive and motor functions, smelling loss was among the earliest biomarkers of aging. During aging, metabolites related with oxidative stress, osmolytes, and infection became dysregulated in the olfactory bulb, and G protein coupled receptor-related signaling was significantly down regulated in olfactory bulbs of aged mice. Poly ADP-ribosylation levels, protein expression of DNA damage markers, and inflammation increased significantly in the olfactory bulb of older mice. Lower NAD⁺ levels were also detected. Supplementation of NAD⁺ through NR in water improved longevity and partially enhanced olfaction in aged mice. Our studies provide mechanistic and biological insights into the olfaction decline during aging and highlight the role of NAD⁺ for preserving smelling function and general health.     

Assessing implicit odor localization in humans using a cross-modal spatial cueing paradigm

Background

Navigation based on chemosensory information is one of the most important skills in the animal kingdom. Studies on odor localization suggest that humans have lost this ability. However, the experimental approaches used so far were limited to explicit judgements, which might ignore a residual ability for directional smelling on an implicit level without conscious appraisal.

Methods

A novel cueing paradigm was developed in order to determine whether an implicit ability for directional smelling exists. Participants performed a visual two-alternative forced choice task in which the target was preceded either by a side-congruent or a side-incongruent olfactory spatial cue. An explicit odor localization task was implemented in a second experiment.

Results

No effect of cue congruency on mean reaction times could be found. However, a time by condition interaction emerged, with significantly slower responses to congruently compared to incongruently cued targets at the beginning of the experiment. This cueing effect gradually disappeared throughout the course of the experiment. In addition, participants performed at chance level in the explicit odor localization task, thus confirming the results of previous research.

Conclusion

The implicit cueing task suggests the existence of spatial information processing in the olfactory system. Response slowing after a side-congruent olfactory cue is interpreted as a cross-modal attentional interference effect. In addition, habituation might have led to a gradual disappearance of the cueing effect. It is concluded that under immobile conditions with passive monorhinal stimulation, humans are unable to explicitly determine the location of a pure odorant. Implicitly, however, odor localization seems to exert an influence on human behaviour. To our knowledge, these data are the first to show implicit effects of odor localization on overt human behaviour and thus support the hypothesis of residual directional smelling in humans.     

In Ovo Olfactory Experience Influences Post‐hatch Feeding Behaviour in Young Chickens

In several mammalian species, prenatal exposure to odours can elicit later positive consummatory behaviour in response to substrates bearing that odorant. In birds, the sense of smell has been considerably underestimated, and very little is known about the effects of early sensory experience on the regulation of feeding behaviour. We tested the hypothesis that the feeding behaviour of the domestic chicken could be regulated by olfactory learning during the embryonic life. To that end, chicken embryos were exposed to an olfactory stimulus (blend of essential oil of orange and nature identical vanillin) from embryonic day (ED) 12 to ED20, and chicks were tested between 4 and 9 d of age. In short‐term choice tests, at day 4 and 5, chickens previously exposed to a low concentration (LC) of the olfactory stimulus spent a higher proportion of time eating a familiar or an unfamiliar food bearing the olfactory stimulus compared to non‐exposed control chickens. Conversely, chickens previously exposed to a high concentration (HC) of the olfactory stimulus were found to avoid all foods bearing the olfactory stimulus. On a 24‐ h time scale at day 7–8, LC and HC birds, but not controls, ingest significantly less familiar food containing the olfactory stimulus. This result indicated a long‐term effect of the early olfactory experience on feeding preferences. We demonstrated that chickens can utilize information from their pre‐hatch chemosensory environment to guide their later feeding behaviour. A pre‐hatch effect of the intensity of odour signals in the regulation of feeding behaviour is reported here for the first time.     

Suckermouth armored catfish resolve the paradox of simultaneous respiration and suction attachment: a kinematic study of Pterygoplichthys disjunctivus

Suckermouth armored catfishes (Loricariidae) use their suckermouth for inspiration, feeding, and attachment to substrates. The sucker consists of a pre-valvular cavity, formed by a modified lip disc, and is separated from the larger post-valvular buccal cavity by a muscular oral valve. The combination of respiration and suction attachment seems paradoxal, as a properly functioning suction device would need a sucker without leakage (yet inspiration must occur via the sucker), and continuous subambient pressure in the sucker cavity (even during expiratory mouth floor elevation). In the loricariid Pterygoplichthys disjunctivus, the anatomy of the suckermouth structures was examined, and a kinematic analysis was performed to acquire insights into how respiration and attachment are combined. High-speed external and X-ray recordings show that suckermouth attachment influences respiratory parameters such as decreasing excursion amplitudes of mouth floor elements, and the way water enters the mouth via furrows in the lip disc. Respiration, however, continues during attachment and is not blocked. Our data show that the muscular oral valve actively separates the post-valvular buccal cavity from the pre-valvular sucker cavity. Volume changes of this pre-valvular cavity are opposite to those of the post-valvular cavity and assure sucker function even during expiration. These volume changes are caused by movements of the lower lip, the lower jaws, and the oral valve. The lateral inflow furrow openings, controlled by the maxillary barbels, can occur unilaterally. Morphological and kinematic data also show that the opercle is anatomically and functionally decoupled from the gill opening.     

The action of the anterior feeding apparatus of Caenorhabditis elegans (Nematoda: Rhabditida)

From analysis of ciné film, combined with ultrastructural observations, the anterior feeding structures and their behaviour in the free-living microbivorous nematode Caenorhabditis elegans during ingestion in dense and sparse suspensions of Escherichia coli are described In dense suspensions bacteria accumulate in the buccal cavity against the three metastomal flaps that nearly close it, and are then swallowed down the three tubular apical expansions of the triradiate oesophageal lumen when the flaps open. Excess medium is then expelled, as the oesophageal lumen closes and traps the swallowed bacteria. The flaps and oesophagus operate by contractions in the seven most anterior oesophageal muscle cells, probably coordinated via proprioceptive nerve endings between the cells. About one million nematode hours are needed to extract 1 g of bacteria from 30 ml of medium. With few or no bacteria, the head moves more, the metastomal flaps do not close and medium seems to pass in and out of the buccal cavity, probably as part of the widespread exploration phase of food-finding behaviour. Abnormal feeding behaviour, control and functions of the metastomal flaps and associated structures, and control of food intake volume are discussed.     

Functional Morphology of the Olfactory Organ in Spinachia spinachia (L.) (Teleostei,Gasterosteidae)

The functional morphology of the olfactory organ in Spinachia spinachia (L.), which has only a single nare, was studied by light microscopy, scanning electron microscopy, and experimental investigations. It was shown that only the incoming water passes over the olfactory epithelium. The device for ventilating this olfactory organ is an accessory ventilation sac activated by respiratory pressure changes in the buccal cavity. This one-way water current over the olfactory epithelium in a monotrematous olfactory organ was found to be possible because of the morphology of the olfactory organ combined with movements of the lateral wall of the olfactory organ and the nasal tube during respiration. The olfactory epithelium is divided into irregular islets. Both ciliated receptor cells and microvillous receptor cells are present.     

Mechanisms for obtaining water for flotation feeding in the soldier crab, Mictyris longicarpus Latreille, 1806 (decapoda,mictyridae)

During feeding Mictyris longicarpus Latreille collects interstitial and free standing water via setae on the posterior border of the carapace and the proximal edge of the first abdominal segment. Water is lifted to the bases of the scaphognathites by capillary action, travelling from the posterior setae into a posterior chamber, along lateral canals, and through the branchial chambers under the epibranchial membranes. The scaphognathites provide the necessary force to pump water into the buccal cavity. Water which flows out of the buccal cavity is collected between the abdomen and cephalothorax by setae fringing the abdomen, and returned to the posterior chamber by the ventrolateral canals.     

Role of the giant serotonin-containing cell of the cerebral ganglion in the edible snail in organizing its food-acquiring behavior

By adding dopamine or serotonin to a bath with snail's isolated nervous system and by intracellular activation of giant cerebral serotonergic cells it was established in neurophysiological experiments that, in spite of activating effect of serotonin on buccal motorneurones, dopamine is the transmitter triggering feeding movements of the buccal mass and feeding pattern in buccal motorneurones. This conclusion is confirmed by behavioural experiments in which an experimental group was injected by neruotoxin 5,6-dihydroxytryptamine selectively impairing serotonergic neurones. The consumatory phase of feeding (triggered by dopamine) did not change in treated animals, while the appetitive phase was significantly impaired. It was noted that the giant metacerebral cell was activated during burst activity in buccal motoneurones. The conclusion is made that giant serotonergic cerebral cells only modulate but do not trigger the feeding behaviour in the snail Helix lucorum.     

Drosophila Avoids Parasitoids by Sensing Their Semiochemicals via a Dedicated Olfactory Circuit

Detecting danger is one of the foremost tasks for a neural system. Larval parasitoids constitute clear danger to Drosophila, as up to 80% of fly larvae become parasitized in nature. We show that Drosophila melanogaster larvae and adults avoid sites smelling of the main parasitoid enemies, Leptopilina wasps. This avoidance is mediated via a highly specific olfactory sensory neuron (OSN) type. While the larval OSN expresses the olfactory receptor Or49a and is tuned to the Leptopilina odor iridomyrmecin, the adult expresses both Or49a and Or85f and in addition detects the wasp odors actinidine and nepetalactol. The information is transferred via projection neurons to a specific part of the lateral horn known to be involved in mediating avoidance. Drosophila has thus developed a dedicated circuit to detect a life-threatening enemy based on the smell of its semiochemicals. Such an enemy-detecting olfactory circuit has earlier only been characterized in mice and nematodes.     

Suctorial feeding in a deep-sea octopus as a means of niche partitioning (Cephalopoda: Octopodidae)

Molecular phylogenetic analyses indicate that two clades of deep-sea octopuses evolved at opposite ends of the earth to become globally sympatric. Coexistence of these overtly similar, but phylogenetically distinct octopuses requires some means of niche partitioning. To investigate details of feeding, the buccal complexes of specimens of each clade, Muusoctopus and Graneledone, were sectioned at 90° to the radular ribbon. The buccal complex of Muusoctopus is the same as reported in Octopus; the radula and its bolsters extend the length of the buccal complex. In Graneledone, however, the radula and its bolsters are restricted to anterior half of the buccal complex. Posterior to the radular sac, a vertically oriented muscle, named here the buccal abductor, extends from the floor of the mouth to the base of the buccal complex. In Muusoctopus, the bolsters extend the radula to bring food into the mouth; the palps propel it to the esophagus. In Graneledone, although the bolsters extend the radula, contraction of the buccal abductor to expand the posterior mouth may be the primary food mover. The negative pressure differential created draws food into the mouth and to the entry to the esophagus. The buccal abductor may permit the ingestion of larger pieces of prey, as gut contents show. Its evolution may represent a key innovation that heightens deep-sea octopus diversity.     

Feeding mechanisms in anuran larvae

Larvae of the neotropical frogs Phyllomedusa are distinctive in that they feed normally in mid-water on phytoplankton, maintaining neutral buoyancy by means of an independently beating tail filament. The feeding mechanism of larval Phyllomedusa trinitatis was studied morphologically and experimentally. The primary feeding mechanism involves a buccal rasp which may in some circumstances render food into small particles, a pumping mechanism which forces water through the buccal cavity and the gill filters, an entanglement system which traps particles in mucous strings produced in special organs, and the formation of mucous cords which transport particles to the oesophagus. In mid-water feeding and surface feeding the buccal rasp serves only its other function in preventing backflow of the respiratory stream. The primary feeding mechanism is discussed and compared with schemes proposed for Rana temporaria and R. agilis. Little agreement exists between these schemes and that which is here proposed. It is concluded that the primary feeding mechanism is the same in the three forms but that there are behavioural differences in feeding generally. Some comment is made on the primary feeding mechanism in the Microhylidae.     

Alarm reaction in the crucian carp is mediated by the medial bundle of the medial olfactory tract

Experiments were performed to determine which bundles of the olfactory tracts were essential for mediating alarm reaction in crucian carp (Carassius carassius L.). The fish were maintained in physiological saline after surgery to preserve the remaining tracts and postoperative inspections revealed the functionality of the intact tracts. Operations on the tracts were performed symmetrically on both sides. Sham-operated and non-operated fish showed the typical alarm behaviour of fast swimming to the bottom, dashing movements and aggregation when exposed to skin extract which contain alarm substance. Fish with only the medial bundle of the medial olfactory tract intact also displayed the alarm behaviour upon exposure; however, these fish did not react to the amino acid, L-alanine with either feeding response or alarm reaction. Crucian carp which had the medial bundle of the medial olfactory tract cut, leaving both the lateral bundle of the medial olfactory tract and the lateral olfactory tract intact, did not display any alarm reaction to skin extract; however, these fish reacted to exposure to L-alanine with feeding behaviour. There were statistically significant differences between the behaviour scores for the fish subject to different treatments. The present study demonstrates that the medial bundle of the medial olfactory tract appears to be both necessary and sufficient for mediation of the alarm reaction. The results also show that the sensory neurons which respond to alarm substance terminate and make synaptic connections with the secondary neurons that make up the medial bundle of the medial olfactory tract; thereby demonstrating the specificity of the spatial aspect of olfactory processing. The results are discussed with respect to the spatial aspect of organization within the olfactory system, the pattern of generalization across orders of fish, and the functional implications of the spatial arrangement of information transmission between the peripheral olfactory organ and the brain.     

Projection of sensory neurons with microvilli to the lateral olfactory tract indicates their participation in feeding behaviour in crucian carp.

In the olfactory system of vertebrates, a large number of primary sensory neurons terminate in glomeruli in the olfactory bulb, where they make synapses with a significantly smaller number of secondary neurons. We applied small amounts of a lipophilic neural tracer (Dil) in the glomerular regions of the lateral olfactory bulb in crucian carp, and investigated the centrifugal migration of this stain through the secondary neurons towards the brain and peripherally to the sensory neurons of the olfactory epithelium. In preparations where only the secondary neurons of the lateral olfactory tract (LOT) were stained, the majority (76%) of sensory neurons had cell bodies in the intermediate layer of the olfactory epithelium. Scanning electron microscopy revealed that most of the sensory neurons with cell bodies in the intermediate layers of the olfactory epithelium feature microvilli. Based on observations that the secondary neurons of the LOT mediate feeding behaviour, we feel that there is strong evidence to indicate that the sensory neurons that exhibit microvilli are responsible for mediating the behavioural patterns related to feeding. These results are discussed in relation to physiological experiments on the properties of the sensory neurons and to studies of the innervation pattern of sensory neurons.     

Variation in genetic architecture of olfactory behaviour among wild-derived populations of Drosophila melanogaster

Odour-guided behaviour is a quantitative trait determined by many genes that are sensitive to gene-environment interactions. Different natural populations are likely to experience different selection pressures on the genetic underpinnings of chemosensory behaviour. However, few studies have reported comparisons of the quantitative genetic basis of olfactory behaviour in geographically distinct populations. We generated isofemale lines of Drosophila melanogaster from six populations in Argentina and measured larval and adult responses to benzaldehyde. There was significant variation within populations for both larval and adult olfactory behaviour and a significant genotype x sex interaction (GSI) for adult olfactory behaviour. However, there is substantial variation in the contribution of GSI to the total phenotypic variance among populations. Estimates of evolvability are orders of magnitude higher for larvae than for adults. Our results suggest that the potential for evolutionary adaptation to the chemosensory environment is greater at the larval feeding stage than at the adult reproductive stage.