Svante Winberg

Short-Term Effects of Fights for Social Dominance and the Establishment of Dominant-Subordinate Relationships on Brain Monoamines and Cortisol in Rainbow Trout

We report changes in brain serotonergic, noradrenergic and dopaminergic activity, along with plasma cortisol concentrations, occurring during the initial 24-h period following the establishment of dominant-subordinate relationships in pairs of rainbow trout. Immediately (within 5 min) after the termination of staged fights for social dominance, a large increase in blood plasma cortisol was observed in both fight losers (future subordinate fish) and winners (future dominant fish). In dominant fish, cortisol decreased rapidly (within 3 h) to the level of unstressed controls, while continuing to increase in subordinate fish. At 3 h following fights, the brain serotonergic system was activated in both dominant fish and subordinate fish, at least in some brain regions (telencephalon). This effect was reversed in dominant individuals within 24 h of social interaction, whereas in subordinate fish a substantial activation of the serotonergic system was manifest in all brain regions by 24 h. Similarly, a strong increase in brain catecholaminergic activation was indicated after 24 h of social interaction in subordinate fish, but not in dominant fish. Relationships between plasma cortisol and brain serotonergic and noradrenergic activity in the various experimental groups suggest that these systems influence cortisol secretion under normal conditions and during moderate or short-term stress.

Behavioral and Neuroendocrine Correlates of Selection for Stress Responsiveness in Rainbow Trout—a Review

Abstract In rainbow trout the magnitude of the cortisol response to stress shows both consistency over time and a moderate to high degree of heritability, and high responding (HR) and low responding (LR) lines of rainbow trout have been generated by individual selection for consistently high or low post-stress cortisol values. Using 2nd and 3rd generation fish, we tested the hypothesis that differential stress responsiveness is associated with behavioral alterations in the HR-LR trout model. LR fish showed a tendency to become socially dominant, a rapid recovery of food intake after transfer to a novel environment, and a reduced locomotor response in a territorial intrusion test. Furthermore, stress induced elevation of brain stem and optic tectum concentrations of the monoamine neurotransmitters serotonin, dopamine, and norepinephrine and their metabolites suggests that both synthesis and metabolism of these transmitters were elevated after stress to a larger degree in HR than in LR trout. A divergent pattern was seen in the hypothalamus, where LR fish displayed elevated levels of 5-hydroxyindoleacetic acid (a serotonin metabolite) and 3-methoxy-4-hydroxyphenylglycol (a norepinephrine metabolite). Thus, selection for a single trait, cortisol responsiveness, in rainbow trout is associated with concurrent changes in both behavior and central signaling systems. The apparent parallel to genetically determined stress coping styles in mammals, and the existence of similar trait associations in unselected populations of rainbow trout, suggests an evolutionarily conserved correlation between multiple traits. Continuing studies on the HR and LR trout lines are aimed at providing the physiological and genetic basis for new marker-assisted selection strategies in the rapidly developing finfish aquaculture industry, as well as increased knowledge of the function and evolution of central neuroendocrine signaling systems.

Roles of brain monoamine neurotransmitters in agonistic behaviour and stress reactions, with particular reference to fish

Abstract 1. Experimental results on the involvement of brain monoamines in agonistic behaviour and stress in fish are reviewed and discussed in relation to available data from other vertebrates. 2. In fish as well as mammals, stress induces increased brain serotonergic activity, and a similar increase in serotonergic activity is seen in subordinate individuals in a dominance hierarchy. 3. The brain serotonergic system appears to inhibit aggression and spontaneous locomotor activity in both fish and mammals. 4. Subordinate fish show several behavioural characteristics, notably inhibition of aggressive behaviour, low spontaneous locomotor activity and decreased food intake, that are likely to be related to their increased brain serotonergic activity. 5. By contrast, the brain dopaminergic system appears to stimulate aggressive behaviour in both fish and mammals, and dominant fish show signs of elevated dopaminergic activity in telencephalon. 6. The similarities between fish and mammalian monoaminergic functions suggest that these are phylogenetically very old mechanisms that have been conserved during the last 400 million years of vertebrate evolution.

Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout

Agonistic behavior, brain concentrations of serotonin (5-hydroxytryptamine, 5-HT), and 5-hydroxyindoleacetic acid (5-HIAA, the main 5-HT metabolite), plasma cortisol levels, and the pituitary expression of pro-opiomelanocortin (POMC) A and B mRNA were determined in socially dominant and subordinate rainbow trout after 1 or 7 days of social interaction. Telencephalic and brain stem 5-HIAA/5-HT ratios, plasma cortisol levels, and pituitary POMC mRNA concentrations were elevated in fish being subordinate for 1 day. Furthermore, neither telencephalic 5-HIAA/5-HT ratios nor pituitary POMC A or POMC B mRNA expression showed any decline after 7 days of social interaction. By contrast, plasma cortisol concentrations of subordinate fish declined after 7 days but were still significantly higher than in dominant fish. Furthermore, in subordinate fish, hypothalamic 5-HIAA/5-HT ratios and plasma cortisol levels were highly correlated, suggesting an important role of hypothalamic 5-HT in the regulation of the teleost hypothalamic-pituitary-interrenal (HPI) axis. The number of aggressive acts received and plasma cortisol levels were highly correlated in 1-day subordinates, a relationship not seen in fish subjected to 1 wk of subordination. Thus the chronic stress experienced by subordinates in established dominance hierarchies appears to be more closely related to the threat imposed by the presence of the dominant fish than to actual aggressive encounters. The sustained elevation of pituitary POMC mRNA expression, an effect mainly related to an increase of melanotropic POMC expression, in subordinates could be a mechanism serving to maintain HPI axis excitability and promote acclimation in these individuals.

Serotonin as a regulator of hypothalamic-pituitary-interrenal activity in teleost fish

Evidence for the presence of a serotonin1A (5-HT1A) receptor subtype in the salmonid fish brain has recently been presented. In the present study the potent 5-HT1A receptor agonist, 8-hydroxy-2-(di-n-propylamino)-tetralin (8-OH-DPAT) was tested for its effect on plasma cortisol concentrations in rainbow trout (Oncorhynchus mykiss). Blood was sampled and 8-OH-DPAT administered through a catheter in the dorsal aorta. Thirty minutes after the injection of 40 microg of 8-OH-DPAT/kg, plasma cortisol levels had increased from 12 to 149 ng/ml, whereupon they fell, reaching baseline levels after 4 h. The effect of 1-40 microg 8-OH-DPAT/kg on plasma cortisol concentrations was dose-dependent. The results lends further support to the hypothesis that the brain serotonergic system plays a key role in integrating autonomic, behavioral and neuroendocrine stress-responses in fish as well as mammals, suggesting that not only the structural and biochemical organization, but also the function of the serotonergic system has been conserved during vertebrate evolution.

Stress coping style predicts aggression and social dominance in rainbow trout

Social stress is frequently used as a model for studying the neuroendocrine mechanisms underlying stress-induced behavioral inhibition, depression, and fear conditioning. It has previously been shown that social subordination may result in increased glucocorticoid release and changes in brain signaling systems. However, it is still an open question which neuroendocrine and behavioral differences are causes, and which are consequences of social status. Using juvenile rainbow trout of similar size and with no apparent differences in social history, we demonstrate that the ability to win fights for social dominance can be predicted from the duration of a behavioral response to stress, in this case appetite inhibition after transfer to a new environment. Moreover, stress responsiveness in terms of confinement-induced changes in plasma cortisol was negatively correlated to aggressive behavior. Fish that exhibited lower cortisol responses to a standardized confinement test were markedly more aggressive when being placed in a dominant social position later in the study. These findings support the view that distinct behavioral-physiological stress coping styles are present in teleost fish, and these coping characteristics influence both social rank and levels of aggression.

Effects of cortisol on aggression and locomotor activity in rainbow trout.

Noninvasive administration of cortisol through the diet resulted in relatively rapid (<1.5 h) and highly reproducible increases in plasma cortisol in rainbow trout, comparable to changes seen in fish subjected to substantial stress. Juvenile rainbow trout were reared in isolation for 1 week, before their daily food ration was replaced by a meal of cortisol-treated food corresponding to 6 mg cortisol kg(-1). All fish were observed for 30 min, beginning at 1 or 48 h following the introduction of cortisol-treated food. Additional cortisol (75% of the original dose on Day 2, and 50% on Day 3) was administered to the long-term cortisol-treated group. The resulting blood plasma concentrations of cortisol were similar in short- and long-term treated fish, and corresponded to those previously seen in stressed rainbow trout. Controls were fed similar food without cortisol. Half of the fish from each treatment group (controls and short- and long-term cortisol) were subjected to an intruder test (a smaller conspecific introduced into the aquarium), while half of the fish were observed in isolation. In fish challenged by a conspecific intruder, short-term cortisol treatment stimulated locomotor activity, while long-term treatment inhibited locomotion. Aggressive behavior was also inhibited by long-term cortisol treatment, but not by short-term exposure to cortisol. Cortisol treatment had no effect on locomotor activity in undisturbed fish, indicating that the behavioral effects of cortisol were mediated through interaction with other signal systems activated during the simulated territorial intrusion test. This study demonstrates for the first time that cortisol has time- and context-dependent effects on behavior in teleost fish.

Interactions between the neural regulation of stress and aggression

SUMMARY Socially aggressive interaction is stressful. What is more, social aggression is stressful for both dominant and subordinate animals. Much of the neurocircuitry for stress and aggression overlap. The pattern of neurochemical and hormonal events stimulated by social interaction make it clear that subtle differences in this pattern of response distinguish social rank. The neurotransmitter serotonin (5-HT) responds rapidly to stress, and also appears to play the most important role for inhibitory regulation of aggressive interactions. In addition, the adrenocortical/interrenal steroid hormones corticosterone and cortisol are responsive to stress and influence aggression. However, while 5-HT and glucocorticoids can both be inhibitory to aggression, the relationship between 5-HT and glucocorticoids is not straightforward, and much of the distinctions in function depend upon timing. Neither is inhibitory during the early stressful phase of aggression. This transmitter-hormone combination follows and influences a four-stage functional pattern of effect: (1) predisposed (positively or negatively) toward aggression, (2) motivated toward behavior, (3) responsive to stress (including aggression) and passively allowing aggression, and finally (4) chronically applied 5-HT and glucocorticoids inhibit aggression.

Social rank and brain levels of monoamines and monoamine metabolites in Arctic charr, Salvelinus alpinus (L.)

SummaryDominance hierarchy was determined in 5 groups of juvenile Arctic charr (Salvelinus alpinus), each group consisting of 4 fish. Telencephalon and brain stem (remaining parts of the brain) were analyzed with regard to their content of monoamines and monoamine metabolites. No significant differences were observed in the concentrations of norepinephrine (NE), dopamine (DA), or serotonin (5-hydroxytryptamine, 5-HT) between fish with different social rank. However, the concentration of 5-hydroxyindoleacetic acid (5-HIAA), the principle metabolite of 5-HT, was significantly higher in subordinate fish, and a significant inverse linear correlation was found between 5-HIAA concentration and social rank (as measured by dominance index) in the brain stem. In the telencephalon the dominant fish had a significantly higher level of homovanillic acid (HVA), a major DA metabolite. These findings indicate a greater serotonergic activity, possibly associated with increased stress, as well as a lower dopaminergic activity, possibly associated with reduced aggression, in subordinate charr. The differences between dominant and subordinate fish could either be caused by social interactions or reflect innate individual differences in monoamine utilization, predisposing individuals for dominant or subordinate positions in the dominance hierarchy.

Changes in brain serotonergic activity during hierarchic behavior in Arctic charr (Salvelinus alpinus L.) are socially induced

SummaryThe experiment was performed in two phases. During the first phase (phase 1) the dominance hierarchy was determined in 4 groups of Arctic charr (Salvelinus alpinus L.), each group consisting of 4 fish. Phase 2 was started by rearranging phase 1 fish into 4 new groups. Group 1 consisted of previously dominant fish and groups 2, 3 and 4 of fish that previously held rank 2, 3 and 4, respectively. After phase 2 telencephalon and brain stem were analyzed with regard to their contents of serotonin (5-hydroxytryptamine, 5-HT) and 5-hydroxyindoleacetic acid (5-HIAA), the principle metabolite of 5-HT. No correlation was found between the social rank (measured as dominance index) during phase 1 and the brain serotonergic activity (measured as the ratio 5-HIAA/5-HT) determined after phase 2. However, most important, the 5-HIAA/5-HT ratio was significantly correlated with the last experienced social rank, i.e. that acquired during phase 2. These results shows that the difference in brain serotonergic activity between dominant and subordinate fish develops through social interactions. Further, we found that previous subordinate experience inhibited aggressive behavior, an effect which, in the light of available information on stress and 5-HT, could be related to the increase in brain serotonergic activity. We hypothesize that stress induces an increased serotonergic activity which in turn inhibits the neuronal circuitry which mediates aggressive behavior.