Heart rate measures in blind cave crayfish during environmental disturbances and social interactions

Most animals continually assess the environment in which they live and alter their behavior according to various stimuli. As an observer, one looks for changes in a behavior indicating that an animal responded to a particular event. When the animal does not make significant behavioral changes as measured by bodily movements, the animal may be characterized as unresponsive to a given stimulus. This study demonstrates that when behavioral body movements can not be observed an internal physiological measure of heart rate (HR) shows dramatic changes following presentation of defined stimuli. This study used the blind cave crayfish and examined their responsiveness to the following stimuli: light (infrared, dim red, and white), water-borne vibrations, removal of water, olfactory cues, and social interaction with partners. This study demonstrates that there is substantial individual variation of HR at basal levels and with the intensity of an social interaction. We find HR is a reasonable measure of the responsiveness of blind cave crayfish to given stimuli even in the absence of observable behavioral changes. This enables the observer to determine if an individual is responsive to and making an assessment of particular cues.     

Heart and ventilatory measures in crayfish during environmental disturbances and social interactions

Most animals assess the environment in which they live and alter their behavior according to various stimuli. When the animal does not make significant behavioral changes, as measured by bodily movements, the animal may be characterized as unresponsive to a given stimulus. This study demonstrates that when behavioral movements of crayfish cannot be observed, physiological measures of heart rate (HR) and ventilatory rate (VR) show dramatic changes in response to defined sensory stimuli. In the majority of cases, upon anticipation of a social interaction with another crayfish both HR and VR will increase. During an agonistic encounter between two crayfish, the level of HR and VR correlate with the intensity of the interaction. Such rapid responses in cardiac and respiratory systems to environmental disturbances and anticipation of a social interaction suggest an autonomic-like regulation associated with fear, flight or fight. Since behavioral observations do not allow an internal status to be readily assessed, we suggest that HR and VR may serve as a useful bioindex in crustaceans to their internal drive or possibly an awareness level to environmental cues.     

Heart rate and breathing pattern: interactions and sex differences

Ten subjects (five males, five females) were studied in resting conditions. Ventilation (VT, f, TI, TE), heart rate (HR) and RR interval were recorded or measured. Each subject voluntarily breathed with spontaneous frequency at different ratios of his spontaneous tidal volume (VrT). The results show that sinus arrhythmia increases with lung volume but without effect on mean heart rate. When VT is increased by two times its spontaneous value, the ventilatory drive (VT/TI) is raised in both sexes; the relative duration of inspiration (TI/Ttot) is modified (+20%) in females only. Thus with the cardiac effects of increasing lung volume being similar in both sexes, we conclude that sinus arrhythmia is not generated by sensory inputs from pulmonary structures, but that its origin is at the CNS level. Moreover, there may be a sex difference in the control of voluntary ventilation, a suggestion requiring further investigation.     

The social consequences of honey bee polyandry: the effects of kinship on worker interactions within colonies

Honey bees, Apis mellifera L., are polyandrous and several males simultaneously father offspring within a single colony. The relatedness of female colony members therefore varies with their paternity: workers encounter both patrilineal full sister (r¯=0·75) and non-patrilineal half-sister (r¯=0·25) nestmates. The impact of this intra-colony genetic variation on social grooming and trophallaxis (liquid food exchange) among workers in colonies consisting of two phenotypically-distinct worker patrilines was examined. Workers in these colonies groomed and fed a disproportionately large number of full sisters despite a tendency to encounter a disproportionately large number of half-sisters. Thus, workers actively discriminated between full and half-sisters. This patrilineal discrimination occurred both in colonies with laying queens and in a queenless colony rearing replacement queens. These results suggest that intracolony genetic variation may have a major effect on colony social organization.     

The effects of 5-HT on sensory, central and motor neurons driving the abdominal superficial flexor muscles in the crayfish

Serotonin (5-HT) induces a variety of physiological and behavioral effects in crustaceans. However, the mechanisms employed by 5-HT to effect behavorial changes are not fully understood. Among the mechanisms by which these changes might occur are alterations in synaptic drive and efficacy of sensory, interneurons and motor neurons, as well as direct effects on muscles. We investigated these aspects with the use of a defined sensory-motor system, which is entirely contained within a single abdominal segment and consists of a ‘cuticular sensory neurons–segmental ganglia–abdominal superficial flexor motor neurons–muscles’ circuit. Our studies address the role of 5-HT in altering (1) the activity of motor neurons induced by sensory stimulation; (2) the inherent excitability of superficial flexor motor neurons; (3) transmitter release properties of the motor nerve terminal and (4) input resistance of the muscle. Using en passant recordings from the motor nerve, with and without sensory stimulation, and intracellular recordings from the muscle, we show that 5-HT enhances sensory drive and output from the ventral nerve cord resulting in an increase in the firing frequency of the motor neurons. Also, 5-HT increases transmitter release at the neuromuscular junction, and alters input resistance of the muscle fibers     

Role of 5-HT in the regulation of the brain-pituitary-adrenal axis: effects of 5-HT on adrenocortical cells

Serotonin (5-HT) plays a pivotal role in the regulation of the brain-pituitary-adrenal axis. In particular, 5-HT has been shown to control the activity of hypothalamic CRF neurons and pituitary corticotrope cells through activation of 5-HT1A and (or) 5-HT(2A/2C) receptor subtypes. 5-HT, acting through 5-HT2 receptors, can also trigger the renin-angiotensin system by stimulating renin secretion and consequently can enhance aldosterone production. At the adrenal level, 5-HT produced locally stimulates the secretory activity of adrenocortical cells through a paracrine mode of communication. The presence of 5-HT in the adrenal gland has been demonstrated immunohistochemically and biochemically in various species. In the frog, rat, and pig adrenal gland, 5-HT is synthesized by chromaffin cells, while in the mouse adrenal cortex, 5-HT is contained in nerve fibers. In man, 5-HT is present in perivascular mast cells. In vivo and in vitro studies have shown that 5-HT stimulates corticosteroid secretion in various species (including human). The type of receptor involved in the mechanism of action of 5-HT differs between the various species. In frogs and humans, the stimulatory effect of 5-HT on adrenocortical cells is mediated through a 5-HT4 receptor subtype positively coupled to adenylyl cyclase and calcium influx. In the rat, the effect of 5-HT on aldosterone secretion is mediated via activation of 5-HT7 receptors. Clinical studies indicate that 5-HT4 receptor agonists stimulate aldosterone secretion in healthy volunteers and in patients with corticotropic insufficiency and primary hyperaldosteronism. Local serotonergic control of corticosteroid production may be involved in the physiological control of the activity of the adrenal cortex as well as in the pathophysiology of cortisol and aldosterone disorders.     

Density and function of central serotonin (5-HT) transporters, 5-HT1A and 5-HT2A receptors, and effects of their targeting on BTBR T+tf/J mouse social behavior

BTBR mice are potentially useful tools for autism research because their behavior parallels core social interaction impairments and restricted-repetitive behaviors. Altered regulation of central serotonin (5-HT) neurotransmission may underlie such behavioral deficits. To test this, we compared 5-HT transporter (SERT), 5-HT(1A) and 5-HT(2A) receptor densities among BTBR and C57 strains. Autoradiographic [(3) H] cyanoimipramine (1 nM) binding to SERT was 20-30% lower throughout the adult BTBR brain as compared to C57BL/10J mice. In hippocampal membrane homogenates, [(3) H] citalopram maximal binding (B(max) ) to SERT was 95 ± 13 fmol/mg protein in BTBR and 171 ± 20 fmol/mg protein in C57BL/6J mice, and the BTBR dissociation constant (K(D) ) was 2.0 ± 0.3 nM versus 1.1 ± 0.2 in C57BL/6J mice. Hippocampal 5-HT(1A) and 5-HT(2A) receptor binding was similar among strains. However, 8-OH-DPAT-stimulated [(35) S] GTPγS binding in the BTBR hippocampal CA(1) region was 28% higher, indicating elevated 5-HT(1A) capacity to activate G-proteins. In BTBR mice, the SERT blocker, fluoxetine (10 mg/kg) and the 5-HT(1A) receptor partial-agonist, buspirone (2 mg/kg) enhanced social interactions. The D(2) /5-HT(2) receptor antagonist, risperidone (0.1 mg/kg) reduced marble burying, but failed to improve sociability. Overall, altered SERT and/or 5-HT(1A) functionality in hippocampus could contribute to the relatively low sociability of BTBR mice.     

Behavioral and neuroendocrine response to psychosocial stress in male rats: the effects of the 5-HT 1A agonist ipsapirone

The effect of the 5-HT 1A agonist ipsapirone on the behavior, plasma catecholamine, and corticosterone levels was studied in male Wistar rats during the psychosocial stress of confrontation with a confined dominant opponent 24 hr after defeat. The effect of the drug was also studied during a predefeat confrontation with the confined (would-be dominant) rat. Blood samples were withdrawn via a permanent heart catheter. The drug (5 mg/kg, ip) or vehicle was given 30 min before transportation to the experimental room. Ipsapirone had no major effects on the plasma hormone concentrations and had no influence upon the behavioral response to the confined rat. At the postdefeat test ipsapirone led to a significant increase of immobility, whereas both rearing and time spent sniffing the cage were diminished. Postdefeat psychosocial stress resulted in an increase of the hormone, particularly catecholamine levels. These responses were further elevated by the drug. The presence of high corticosterone levels in the home cage after postdefeat ipsapirone treatment leads to the hypothesis that postsynaptic 5-HT 1A receptor hypersensitivity develops after the social stress of defeat.     

Heart rate biofeedback and cold pressor pain: effects of expectancy

The study investigated the effects of expectancy on the reduction of cold pressor test pain using heart rate biofeedback training. Thirty-six male subjects were given an initial 45-sec cold pressor test, 25 heart rate decrease feedback training trials, and a final cold pressor test in which they were told to decrease their heart rate, but without the aid of feedback. Two levels of outcome expectancy (increase pain, decrease pain) and two levels of cold pressor water temperature (0 degrees C, 5 degrees C), resulting in four groups (N = 9 per group), were used to assess the interaction between expectancy and aversive stimulus intensity. Immediately prior to the final cold pressor test, the increase pain expectancy subjects were told that decreasing their heart rate during the ice water immersion would cause more pain. Decrease pain subjects were told that decreasing their heart rate would cause less pain. Expectancy was found to be the major determinant of pain reports. The decrease pain subjects consistently reported less pain on the final cold pressor, whereas the increase pain subjects consistently reported more pain. Contrary to prediction, expectancy effects were greater for the colder water. The findings indicate the importance of expectancy in the clinical use of biofeedback to control pain.     

Novelty stress and reproductive state alters responsiveness to sensory stimuli and 5-HT neuromodulation in crayfish

Sensory stimuli can produce varied responses depending on the physiological state of an animal. Stressors and reproductive stage can result in altered biochemical status that changes the responsiveness of an animal to hormones and neuromodulators, which affects whole animal behavior in relation to sensory stimuli. Crayfish serve as a model for examining the effects of neuromodulators at the neuromuscular junctions (NMJs) and for alterations in stereotypic behaviors for particular stimuli. Thus, we used crayfish to examine the effect of novelty stressors in males and the effect of being gravid in female crayfish to exogenous application of serotonin (5-HT). The responsiveness of neuromuscular junctions to 5-HT revealed that stressed as well as gravid crayfish have a reduced response to 5-HT at NMJs. The stressed crayfish were not fatigued since the basal synaptic responses are large and still showed a pronounced response to 5-HT. Using intact animals to examine a tail flip behavior, we showed that the rate of habituation in tail flipping to a strong repetitive stimulus on the telson is reduced in stressed males. Gravid females show no tail flipping behavior upon telson stimulation.     

The effects of Trichinella spiralis infection on social interactions in mixed groups of infected and uninfected male mice

The presence of Trichinella spiralis infection in groups of male mice caused behavioural changes in both infected and uninfected mice. Also, for some behaviours, the extent of behavioural change in infected mice appeared to be determined by the number of muscle larvae they harboured. Infected mice showed a reduced frequency of exploratory and social behaviours compared with uninfected mice while uninfected mice performed more social investigatory activities towards those that were infected. Social interactions between infected and uninfected mice were also affected by familiarity. Behavioural differences shown to result from infection in mice familiar with each other were similar but more pronounced when the mice were unfamiliar. These results suggest that other factors may influence the behavioural effects of parasites on their hosts. For some behaviours, the greatest alterations in behaviour apparently caused by infection coincided with the period of infectivity to another host. The significance of this in relation to parasite transmission is considered.     

Cyclic AMP, 5-HT, and the modulation of transmitter release at the crayfish neuromuscular junction

In this study it was found that several agents which elevate cAMP levels in cells also increase dramatically the quantity of transmitter released from crayfish excitatory nerve terminals in response to a stimulus. With respect to time course and magnitude, the increase produced by one of these agents, the cyclic nucleotide phosphodiesterase inhibitor Squibb 20,009 (SQ 20,009), is unlike any reported for such a drug at a synapse. Additionally, SQ 20,009 potentiated the facilitation of transmitter release produced by serotonin (5-HT) at this synapse. These results establish a possible role for cAMP in the control and modulation of transmitter release at the crayfish neuromuscular junction (NMJ). They further suggest that 5-HT functions here by activation of a presynaptically located adenylate cyclase.     

Prosocial effects of prolactin in male rats: Social recognition,social approach and social learning

Prolactin (PRL) and oxytocin (OT) are pituitary hormones essential for lactation, but also promote sexual behavior. OT stimulates social behaviors, such as recognition, approach, and learning, but less is known about PRL in these behaviors. Since PRL and OT have complementary functions in reproduction, we hypothesized that PRL increases social recognition, approach, and learning. Male Long-Evans rats received ovine PRL (oPRL; 0.5, 2.0 or 5.0 mg/kg), the PRL antagonist bromocriptine (0.1, 3.0 or 5.0 mg/kg) or saline 20 mins before testing for recognition of familiar vs. unfamiliar stimulus males. Saline controls preferred the unfamiliar male (p < 0.05), while bromocriptine blocked this preference. oPRL did not increase preference. To measure social approach, we determined if PRL restores approach 2 h after defeat by an aggressive male. Defeated rats avoided the aggressive male. 2 mg/kg oPRL, before or after defeat, restored approach towards the aggressive male (p < 0.05). In non-defeated rats, oPRL or 3 mg/kg bromocriptine had no effect. To determine if PRL increases social learning, we tested social transmission of food preference. Rats choose between two unfamiliar flavors, one of which they have previously been exposed to through interaction with a demonstrator rat. Vehicle controls preferred chow with the demonstrated flavor over the novel flavor. oPRL-treated rats were similar. Bromocriptine-treated rats failed to show a preference. When tested one week later, only oPRL-treated rats preferred the demonstrated flavor. The results suggest that PRL is required for social recognition and learning, and that increasing PRL enhances social memory and approach, similar to OT.     

Heart rate modulation in bystanding geese watching social and non-social events

Simply observing other individuals interacting has been shown to affect subsequent behaviour and also hormones in 'bystander' individuals. However, immediate physiological responses of an observer have been hardly investigated. Here we present results on individuals' heart rate (HR) responses during various situations, which occur regularly in a flock of greylag geese (Anser anser, e.g. agonistic encounters, vehicles passing by). We recorded simultaneously HR and behaviour of 21 semi-tame free-roaming geese, equipped with fully implanted transmitters. We considered 304 social and 81 non-social events during which the focal individuals did not respond behaviourally. Independent of the spatial distance to the event, these HR responses were significantly greater in social contexts (e.g. departing or landing geese, agonistic interactions) than in non-social situations (e.g. vehicles passing by, thunder). Focal individuals showed a significantly higher maximum HR as well as a greater HR increase in response to agonistic interactions, in which the pair partner or a family member was involved, as compared with a non-affiliated goose. Also, HR was significantly higher when the bystander watched non-affiliated geese interacting, which were higher ranking than the focal. We conclude that these differences are due to different relevance of the recorded events for the focal individual, depending on the individuals involved in the observed interaction.     

Innervation of holothurian body wall muscle: inhibitory effects and localization of 5-HT

We investigated innervation to body wall muscles as well as distribution of 5-HT (serotonin) and its effects on longitudinal muscles of body wall (LMBW) of the sea cucumber Apostichopus japonicus. With serial sections we found neural branches and fibers extending from hyponeural part of radial nerve towards LMBW and circular muscles of body wall. With the aqueous aldehyde (Faglu) method yellow fluorescence indicating indolamines was observed in LMBW and in the mesentery connecting LMBW to the body wall. With indirect immunohistochemistry 5-HT-like immunoreactivity was observed in LMBW and in mesentery. These results strongly suggested that both LMBW and mesentery contained 5-HT. The effects of monoamine neurotransmitters were studied in LMBW. Putative neurotransmitters tested were 5-HT, adrenaline, noradrenaline, dopamine, and DOPA at the concentration of 10(-6) M. The application of 5-HT caused no contraction or relaxation, but it inhibited the contraction induced by 10(-6)-10(-5) M acetylcholine (ACh). Catecholamines were ineffective by themselves and had no effects on the contraction induced by ACh. The present histological, histochemical, and pharmacological studies strongly suggested that holothurian LMBW was innervated by inhibitory serotonergic neurons of the hyponeural nervous system.     

The influence of male dominance on social interactions in black ducks and mallards

The influence of male dominance on male-female social interactions was examined in black ducks, Anas rubripes, and mallards, A. platyrhynchos, that were raised from hatch in four different groups (male and female mallards; male and female black ducks; male mallards and female black ducks; male black ducks and female mallards). The mate preference of females, independent of the influence of male dominance, was determined by exposing females to four caged, isolated males, one from each different group. All females preferred the type of male they had been raised with since hatch. Females were then exposed to the same four males, now free-swimming, to determine how male dominance influenced the initial preference. Under these conditions, each female associated primarily with the most dominant of the four males, regardless of her initial mate preference. Mallards were the most dominant males in all tests. These results demonstrate that male dominance influences social interactions and is one factor contributing to hybridization between these two species.