A field study of chemical senses in bottlenose dolphins and pilot whales.

For most marine vertebrates, chemical cues provide crucial information during navigation and foraging, but their use by cetaceans is still poorly understood. In contrast to baleen whales, toothed whales (odontocetes) are scarcely equipped for chemoreception: they lack the conventional anatomical structures (i.e., olfactory epithelium, nerves and bulbs) involved in olfaction and have reduced taste buds on the tongue. Several behavioral studies have however shown that captive dolphins can perceive chemical solutions, including odorants, in their oral cavity. To investigate whether odontocetes could use infochemicals in their foraging ecology, we implemented a behavioral response experiment in wild bottlenose dolphins and long-finned pilot whales. We tested dimethyl sulfide (DMS) as a potentially attractive stimulus since it is a chemical signature of highly productive marine areas, known to attract several marine predators including fishes and seabirds. We assessed cetacean responses to DMS exposure by analyzing their movements and surface behaviors recorded by onboard observers. In both species, results did not reveal any significant attraction or behavioral reaction toward DMS when compared to a control chemical stimulus, apart from a short-distance response in bottlenose dolphins. These results suggest that while odontocetes may perceive DMS in water, it apparently does not play a significant role in their foraging ecology. Testing potentially more attractive compounds such as prey extracts with the present method and analyzing surface, underwater and acoustic responses would provide further insights on odontocete feeding behavior. It would also provide valuable clues to studies on the anatomical structures involved in their chemosenses.

Acoustic behaviour of bottlenose dolphins under human care while performing synchronous aerial jumps.

Synchronous behaviours occur when two or more animals display the same behaviour at the same time. However, the mechanisms underlying this synchrony are not well understood. In this study, we carried out an experiment to determine whether or not Bottlenose dolphins use acoustic cues when performing a known synchronised exercise. For this, we recorded three dolphins while they performed requested aerial jumps both individually or synchronously in pairs, with a hydrophone array and a 360° underwater video camera allowing the identification of the subject emitting vocalisations. Results indicated that in pairs, dolphins synchronised their jumps 100% of the time. Whether they jumped alone or in pairs, they produced click trains before and after 92% of jumps. No whistles or burst-pulsed sounds were emitted by the animals during the exercise. The acoustic localisation process allowed the successful identification of the vocalising subject in 19.8% of all cases (N = 141). Our study showed that in all (n = 28) but one successful localisations, the click trains were produced by the same individual. It is worth noting that this individual was the oldest female of the group. This paper provides evidence suggesting that during synchronous behaviours, dolphins use acoustic cues, and more particularly click trains, to coordinate their movements; possibly by eavesdropping on the clicks or echoes produced by one individual leading the navigation.

Behavioural responses of humpback whales to food-related chemical stimuli.

Baleen whales face the challenge of finding patchily distributed food in the open ocean. Their relatively well-developed olfactory structures suggest that they could identify the specific odours given off by planktonic prey such as krill aggregations. Like other marine predators, they may also detect dimethyl sulfide (DMS), a chemical released in areas of high marine productivity. However, dedicated behavioural studies still have to be conducted in baleen whales in order to confirm the involvement of chemoreception in their feeding ecology. We implemented 56 behavioural response experiments in humpback whales using two food-related chemical stimuli, krill extract and DMS, as well as their respective controls (orange clay and vegetable oil) in their breeding (Madagascar) and feeding grounds (Iceland and Antarctic Peninsula). The whales approached the stimulus area and stayed longer in the trial zone during krill extract trials compared to control trials, suggesting that they were attracted to the chemical source and spent time exploring its surroundings, probably in search of prey. This response was observed in Iceland, and to a lesser extend in Madagascar, but not in Antarctica. Surface behaviours indicative of sensory exploration, such as diving under the stimulus area and stopping navigation, were also observed more often during krill extract trials than during control trials. Exposure to DMS did not elicit such exploration behaviours in any of the study areas. However, acoustic analyses suggest that DMS and krill extract both modified the whales' acoustic activity in Madagascar. Altogether, these results provide the first behavioural evidence that baleen whales actually perceive prey-derived chemical cues over distances of several hundred metres. Chemoreception, especially olfaction, could thus be used for locating prey aggregations and for navigation at sea, as it has been shown in other marine predators including seabirds.

Sight or smell: which senses do scavenging raptors use to find food?

Raptors are usually considered to be mainly visually dependent, and the use of other sensory modalities has rarely been studied in these birds. Here, we investigated experimentally which senses (vision and/or olfaction) Turkey vultures (Cathartes aura) and Southern caracaras (Caracara plancus) use to find hidden food. First, two identical stainless-steel perforated balls, one containing a putrefied piece of meat and the other an odorless control, were presented to birds in binary choice experiments. Both species interacted more with the smelling ball than with the control, suggesting that they were attracted by the odor of the hidden meat. In a second experiment, individuals were accustomed to eat in one specifically colored ball (blue or green). In the test phase, the meat was hidden in the opposite color with respect to the one each bird had become accustomed to. Vultures still interacted more with the smelly ball disregarding the color, while caracaras interacted equally with the two balls. The prevalence of olfaction in Turkey vultures may partly explain why they are the first raptors to find carcasses in tropical forests. In contrast, caracaras forage on the ground opportunistically, a strategy where both olfaction and sight may be involved. Our experiments suggest that both species are able to use olfactory cues for foraging. However, olfaction could be the predominant sense in Turkey vultures while olfaction and sight could play an equivalent role in Southern caracaras.

Olfactory foraging in temperate waters: sensitivity to dimethylsulphide of shearwaters in the Atlantic Ocean and Mediterranean Sea.

Many procellariiforms use olfactory cues to locate food patches over the seemingly featureless ocean surface. In particular, some of them are able to detect and are attracted by dimethylsulphide (DMS), a volatile compound naturally occurring over worldwide oceans in correspondence with productive feeding areas. However, current knowledge is restricted to sub-Antarctic species and to only one study realized under natural conditions at sea. Here, for the first time, we investigated the response to DMS in parallel in two different environments in temperate waters, the Atlantic Ocean and the Mediterranean Sea, employing Cory's (Calonectris borealis) and Scopoli's (Calonectris diomedea) shearwaters as models. To test whether these birds can detect and respond to DMS, we presented them with this substance in a Y-maze. Then, to determine whether they use this molecule in natural conditions, we tested the response to DMS at sea. The number of birds that chose DMS in the Y-maze and that were recruited at DMS-scented slicks at sea suggests that these shearwaters are attracted to DMS in both non-foraging and natural contexts. Our findings show that the use of DMS as a foraging cue may be a strategy adopted by procellariiforms across oceans but that regional differences may exist, giving a worldwide perspective to previous hypotheses concerning the use of DMS as a chemical cue.

Potential semiochemical molecules from birds: a practical and comprehensive compilation of the last 20 years studies.

During the past 2 decades, considerable progress has been made in the study of bird semiochemistry, and our goal was to review and evaluate this literature with particular emphasis on the volatile organic constituents. Indeed, since the importance of social chemosignaling in birds is becoming more and more apparent, the search for molecules involved in chemical communication is of critical interest. These molecules can be found in different sources that include uropygial gland secretions, feather-surface compounds, and molecules from feces and skin. Although many studies have examined the chemical substances secreted by birds, research on bird chemical communication is still at the start, so new strategies for collecting samples and development of new methods of analysis are urgently required. As a first step, we built a database that brings together potential semiochemicals, using a unique chemical nomenclature for comparing different bird species and also for referencing the different classes of substances that can be found in order to adapt future parameters of analysis. The most important patterns of the wax fraction of preen secretions are highlighted and organized in an ordered table. We also draw up a list of various combinations of sampling and analytical techniques, so that each method can be compared at a glance.

Chemical kin label in seabirds.

Chemical signals yield critical socio-ecological information in many animals, such as species, identity, social status or sex, but have been poorly investigated in birds. Recent results showed that chemical signals are used to recognize their nest and partner by some petrel seabirds whose olfactory anatomy is well developed and which possess a life-history propitious to olfactory-mediated behaviours. Here, we investigate whether blue petrels (Halobaena caerulea) produce some chemical labels potentially involved in kin recognition and inbreeding avoidance. To overcome methodological constraints of chemical analysis and field behavioural experiments, we used an indirect behavioural approach, based on mice olfactory abilities in discriminating odours. We showed that mice (i) can detect odour differences between individual petrels, (ii) perceive a high odour similarity between a chick and its parents, and (iii) perceive this similarity only before fledging but not during the nestling developmental stage. Our results confirm the existence of an individual olfactory signature in blue petrels and show for the first time, to our knowledge, that birds may exhibit an olfactory kin label, which may have strong implications for inbreeding avoidance.

Detective mice assess relatedness in baboons using olfactory cues.

The assessment of relatedness may be crucial in the evolution of socio-sexual behaviour, because it can be associated with fitness benefits mediated by both nepotism and inbreeding avoidance. In this context, one proposed mechanism for kin recognition is 'phenotype matching'; animals might compare phenotypic similarities between themselves and others in order to assess the probability that they are related. Among cues potentially used for kin discrimination, body odours constitute interesting candidates that have been poorly investigated in anthropoid primates so far, because of a mixture of theoretical considerations and methodological/experimental constraints. In this study, we used an indirect approach to examine the similarity in odour signals emitted by related individuals from a natural population of chacma baboons (Papio ursinus). For that purpose, we designed an innovative behavioural tool using mice olfactory abilities in a habituation-discrimination paradigm. We show that: (i) mice can detect odour differences between individuals of same sex and age class in another mammal species, and (ii) mice perceive a higher odour similarity between related baboons than between unrelated baboons. These results suggest that odours may play a role in both the signalling of individual characteristics and of relatedness among individuals in an anthropoid primate. The 'biological olfactometer' developed in this study offers new perspectives to the exploration of olfactory signals from a range of species.

Mediodorsal thalamic lesions block the stress-induced inversion of serial memory retrieval pattern in mice.

This study examines the effects of ibotenic acid lesions of the mediodorsal nucleus of the thalamus (MD) on serial contextual memory retrieval in non-stress and stress conditions. Independent groups of mice learned two successive contextual serial discriminations (D1 and D2) in a four-hole board. The discriminations differed each by the color and texture of the floor. Twenty-four hours later, memory testing occurred in independent groups of mice on one of the two floors of the initial acquisition session. Half of the subjects received three electric footschocks (0.9mA, 2s) 5min prior to testing. Results showed that (i) stress induced a plasma corticosterone rise of same magnitude in sham-operated and MD-lesioned mice; (ii) non-stressed sham-operated mice accurately remembered D1 but not D2, whereas stressed sham-operated animals remembered D2 but not D1; (iii) non-stressed MD-lesioned mice exhibited a memory retrieval pattern similar to that observed in non-stressed sham-operated mice; (iv) however, the stress-induced inversion of the memory retrieval pattern was not observed in MD animals. The effects of MD lesions on memory retrieval in this task are similar to those observed in earlier studies in prefrontal cortex or amygdala-lesioned mice [Chauveau F, Piérard C, Coutan M, Drouet I, Liscia P, Béracochéa D. Prefrontal cortex or basolateral amygdala lesions blocked the stress-induced inversion of serial memory pattern in mice. Neurobiol Learn Mem 2008;90:395-403]; they are however in sharp contrast with mice exhibiting hippocampal lesions [Chauveau F, Pierard C, Tronche C, Coutan M, Drouet I, Liscia P, et al. The hippocampus and prefrontal cortex are differentially involved in serial memory retrieval in non-stress and stress condition. Neurobiol Learn Mem; in press; Chauveau F, Pierard C, Tronche C, Coutan M, Drouet I, Liscia P, et al. Rapid stress-induced corticosterone rise in the hippocampus reverses serial memory retrieval pattern. Hippocampus; in press]. Overall, the present findings highlight the involvement of the MD in an AMG/PFC system mediating the rapid effects of stress on serial memory retrieval.

Altered memory capacities and response to stress in p300/CBP-associated factor (PCAF) histone acetylase knockout mice.

Chromatin remodeling by posttranslational modification of histones plays an important role in brain plasticity, including memory, response to stress and depression. The importance of H3/4 histones acetylation by CREB-binding protein (CBP) or related histone acetyltransferase, including p300, was specifically demonstrated using knockout (KO) mouse models. The physiological role of a related protein that also acts as a transcriptional coactivator with intrinsic histone acetylase activity, the p300/CBP-associated factor (PCAF), is poorly documented. We analyzed the behavioral phenotype of homozygous male and female PCAF KO mice and report a marked impact of PCAF deletion on memory processes and stress response. PCAF KO animals showed short-term memory deficits at 2 months of age, measured using spontaneous alternation, object recognition, or acquisition of a daily changing platform position in the water maze. Acquisition of a fixed platform location was delayed, but preserved, and no passive avoidance deficit was noted. No gender-related difference was observed. These deficits were associated with hippocampal alterations in pyramidal cell layer organization, basal levels of Fos immunoreactivity, and MAP kinase activation. PCAF KO mice also showed an exaggerated response to acute stress, forced swimming, and conditioned fear, associated with increased plasma corticosterone levels. Moreover, learning and memory impairments worsened at 6 and 12 months of age, when animals failed to acquire the fixed platform location in the water maze and showed passive avoidance deficits. These observations demonstrate that PCAF histone acetylase is involved lifelong in the chromatin remodeling necessary for memory formation and response to stress.

Compensatory effect by sigma1 (sigma1) receptor stimulation during alcohol withdrawal in mice performing an object recognition task.

Chronic alcohol consumption (CAC) provokes intense neurobiological alterations, which lead, notably, to an important abstinence syndrome upon withdrawal with deleterious cognitive consequences. We here examined the effect of activation or inactivation of the sigma(1) receptor during CAC withdrawal on the cognitive abilities of Swiss mice. Animals consumed an alcohol 10%/sucrose 30 g/l solution during 4 months. Control groups consumed only the sucrose vehicle solution. Then, animals experienced a progressive, 16 days long, CAC withdrawal, during which they were administered once daily with saline, igmesine (10 mg/kg i.p.), a sigma(1) receptor agonist, or BD1047 (10 mg/kg i.p.), a sigma(1) antagonist. Mice were then tested using an object exploration task, to evaluate their locomotor and exploratory activities and reactions to object habituation, spatial change or novel object presentation. CAC-treated animals showed augmentation of locomotion, anxiety and object exploration, which impeded correct reaction to object habituation, spatial change or novelty. Treatment with the sigma(1) ligands, ineffective in control groups, resulted in decrease of the hyper-responsiveness and restored habituation. However, correct reactions to spatial change and novelty were only produced by the sigma(1) agonist treatment. Moreover, the sigma(1) receptor hippocampal expression was increased in CAC-treated mice. Treatments with both sigma(1) ligands regulated its expression, but subcellular fractionation experiments revealed that the agonist treatment increased [(3)H](+)-pentazocine binding to sigma(1) sites in the plasma membrane fraction, while the antagonist maintained it only in the microsomal, putatively endoplasmic reticulum, fraction. In conclusion, CAC increased the sigma(1) receptor expression in the hippocampus of mice. Regulation of its expression during withdrawal, notably using a selective agonist, allowed not only to attenuate the CAC-induced hyper-responsiveness, but also to restore correct cognitive abilities.

Effects of ibotenic acid lesions of the mediodorsal thalamus on memory: relationship with emotional processes in mice.

The effects of ibotenic acid lesions of the mediodorsal nucleus of the thalamus (MD) on memory and fear reactivity in mice were studied. In the first experiment, MD subjects were submitted to a behavioral design allowing to study the relationship between memory and anxiety [Krazem A, Borde N, Beracochea D. Effects of diazepam and beta-CCM on working memory in mice: relationship with emotional reactivity. Pharmacol Biochem Behav 2001;68:235-44; Beracochea D, Krazem A, Jaffard R. Methyl beta carboline-3-carboxylate reverses the working memory deficits induced either by chronic alcohol consumption or mammillary body lesions in mice. Psychobiology 1995;23:52-8]. In a second experiment, MD-lesioned subjects were submitted to a GO/NOGO temporal alternation task involving two intertrial intervals (ITIs: 0 and 30 s). Lesioned subjects exhibited large bilateral mediodorsal thalamic lesions with small damage into the centromedial thalamic nucleus. In the first experiment, MD-lesioned animals performed normally a sequential alternation task involving fixed ITIs over seven successive trials (5 or 30 s); in contrast, MD-lesioned subjects exhibited deficits in the sequential task involving the same but mixed ITIs (30-5 s versus 5-30 s) the deficit being observed for the last trials of the series, regardless the ITIs used. MD lesions increased fear reactivity in an elevated-plus maze, and scores of anxiety were negatively correlated with performance in the mixed alternation schedule. The second experiment involving non spatial information extended results of the first experiment in showing that the deficit of MD-lesioned animals was not dependent on the ITIs separating trials. Overall, our data show that MD-lesioned subjects exhibit a cognitive impairment characterized by a difficulty to maintain an alternation rule in situations involving procedural variance, and this deficit could stem primarily from an increase of fear reactivity.

Effects of ibotenic acid lesions of the dorsal hippocampus on contextual fear conditioning in mice: comparison with mammillary body lesions.

The goals of the present study were to determine if ibotenic acid lesions of the dorsal hippocampus (dHPC) or of mammillary body (MB) of the hypothalamus would induce similar contextual conditioning deficit in a fear-conditioning paradigm, previously developed in mice [Eur. J. Neurosci. 12 (2000) 2575]. Results showed that ibotenic acid lesions of the dHPC or of the MB both induced severe deficits on contextual conditioning but spared auditory conditioning, as compared to controls. This study provides direct evidence for an involvement of dHPC neurones in contextual fear conditioning and is first to demonstrate an involvement of the MB in the mediation of contextual fear conditioning.

BetaCCM but not physostigmine enhancement of memory retrieval depends on emotional processes in mice.

RATIONALE: The effects of methyl beta-carboline-3-carboxylate (betaCCM, an inverse agonists of GABA/benzodiazepine receptors) or physostigmine (a cholinesterase inhibitor) on retrieval processes and relationships with anxiety have been only marginally studied. OBJECTIVE: This study investigates in mice the effects of acute betaCCM or physostigmine injections on retrieval of previously acquired discriminations involving distinct contextual cues (serial contextual discrimination; SCD) in a four-hole-board. Animals submitted to SCD were also evaluated for emotional reactivity in an elevated-plus maze. METHODS: Mice were injected before the learning session began with a saline solution. Twenty-four hours later, mice were replaced on the context of the initial acquisition and a single dose of saline or betaCCM (0.5 or 1.5 mg/kg) or physostigmine (0.05 and 1.0 mg/kg) was injected 20 min before testing. RESULTS: The highest dose of either betaCCM or physostigmine improved performance of the first discrimination in the SCD task. The higher dose of betaCCM produced anxiety-like reactivity in the plus maze, and scores of "anxiety" were significantly correlated with memory scores; in contrast, memory performance of physostigmine-treated subjects were totally independent of emotional reactivity. CONCLUSION: These results show that, as opposed to physostigmine, betaCCM acts on retrieval processes specifically through its emotional component.

Contextual and serial discriminations: a new learning paradigm to assess simultaneously the effects of acute stress on retrieval of flexible or stable information in mice.

The present study was aimed at simultaneously determining on the same subject, the effects of stress on retrieval of flexible (contextual or temporal) or stable (spatial) information. Three behavioral paradigms carried out in a four-hole board were designed as follows: (1) Simple Discrimination (SD), in which mice learned a single discrimination; (2) Contextual and Serial Discriminations (CSD), in which mice learned two successive discriminations on two different internal contexts; (3) Spatial Serial Discriminations (SSD), in which mice learned two successive discriminations on an identical internal context. The stressor (three inescapable electric footshocks) was delivered 5 min before retention, occurring 5 min or 24 h after acquisition. Results showed that this stressor increased plasmatic corticosterone levels and fear reactivity in an elevated-plus-maze, as compared with nonstressed mice. The stressor reversed the normal pattern of retrieval observed in nonstressed controls in the CSD task, this effect being context dependent, as it was not observed in the SSD task. Overall, our study shows that stress affected the retrieval of flexible and old information, but spared the retrieval of stable or recent ones. Therefore, these behavioral paradigms allow us to study simultaneously, on the same animal, the effects of stress on distinct forms of memory retrieval.

Enhancement of learning processes following an acute modafinil injection in mice.

Modafinil is a wakeness-promoting drug, which is effective in the treatment of narcolepsy; its effects on learning processes are however little studied. Thus, the present study was aimed at determining the effects of an acute modafinil injection on a serial reversal discrimination task performed in a T-maze in mice. Independent groups of mice varying by the level of pretest training (either 1 or 4 days of training) were used. Mice were injected each day with a gum arabic solution before each session began. On the second or the fifth day of training, a single dose of modafinil was injected before testing. Modafinil at 64 mg/kg but not at 32 mg/kg dramatically improved performance as compared to controls in subjects being trained 4 days, but not in subjects being trained 1 day. This improvement of learning was due to the more rapid emergence of a win-stay strategy in modafinil-treated subjects as compare to controls. Thus, our data show that an acute modafinil injection enhances learning processes.

Improvement of learning processes following chronic systemic administration of modafinil in mice.

This study was aimed at determining the effects of a chronic modafinil intraperitoneal administration on the rate of learning in a series of five serial spatial discrimination reversals (SSDR) in a T-maze. Results showed that a daily modafinil administration at 64 mg/kg but not at 32 mg/kg induced a faster learning rate as compared to controls. This learning improvement in experimental mice was due to the faster emergence of a win-stay rule over days of testing. In contrast, a second experiment showed that the same modafinil treatment had no significant effect on contingently reinforced alternation rates over five successive days of testing, as compared to controls. Thus, the results show that modafinil spared the ability to shift responses over trials and consequently, that the use of the win-stay rule to solve the SSDR task observed in modafinil-treated animals is due to an improvement of learning processes.