Activation of Central Biogenic Amines Following Aggressive Interaction in Male Lizards, <i>Anolis carolinensis</i>

Abstract

Many stimuli, including social aggression, activate endocrine stress mechanisms, presumably mediated or modulated by central neurotransmitters. To determine the effects of aggression on central neurochemistry, reproductively active male Anolis carolinensis were paired and allowed to establish social dominance relationships. While combatants cohabited, the fight losers invariably became socially subordinate and displayed darker color, selection of lower perch sites, and lower body posture than the winners. After one hour, one day, one week, or one month of cohabitation animals were sacrificed. Each member of a pair was killed at approximately the same time, along with animals kept isolated as controls. Diencephalon, non-optic lobe midbrain and hindbrain were analyzed for indoleamines, catecholamines and metabolites by coulochem electrode array HPLC. Early activation (by one hour) of the serotonergic system in subordinate male lizards was indicated by decreased serotonin (5-HT), increased 5-hydroxy-indoleacetic acid (5-HIAA) levels and 5-HIAA/5-HT ratio. Substrate 5-hydroxy-tryptophan (5-HTP) also increased in losing males, suggesting enhanced production as well as turnover. Significant 5-HTP and 5-HIAA/5-HT increases for subordinate males, compared with levels in control and dominant males, were greatest at one hour and diminished thereafter. This pattern of indoleamine system activation is consistent with stress-induced stimulation of the serotonergic system and prolonged activation of the stress response in subordinate animals, as well as serotonergic inhibition of aggression. In contrast with serotonin, subordinate males did not have increased catecholamine system activation following one hour of interaction. The ratio of DOPAC/dopamine was lower following one hour of interaction in subordinate males. Adrenergic system activation, indicated by metanephrine/epinephrine ratio, increased with time in losing males, except that after one month of cohabitation, turnover returned to levels that equaled those of control animals. Noradrenergic metabolite MHPG, as well as MHPG/NE ratio, were significantly reduced in dominant males at one hour and one week. Changes in adrenergic system activation, not seen in or registered by noradrenergic systems, indicate a possible role for central epinephrine in social stress accommodation.

Neuromodulation of the agonistic behavior in two species of weakly electric fish that display different types of aggression

“…In several species in which the serotonergic system has been analyzed during agonistic interactions, serotonergic activity increases consistently in subordinates (Yodyingyuad et al, 1985;Blanchard et al, 1991;Summers and Greenberg, 1995;Overli et al, 1999;Summers et al, 2005b) and decreases or remains unchanged in dominants (van Erp and Miczek, 2000;Ferrari et al, 2003;Summers et al, 2003). The activation of 5-HT 1A receptors has been involved in the inhibitory effect of 5-HT on aggression in all vertebrate classes (Deckel and Fuqua, 1998;Sperry et al, 2003;Miczek and Fish, 2006;Clotfelter et al, 2007;Allee et al, 2008;Ten Eyck, 2008).…”

Central Monoamines in Free-Ranging Lizards: Differences Associated with Social Roles and Territoriality

“…Increased 5-hydroxyindoleacetic acid (5-HIAA), indicative of serotonin (5-HT) catabolism, is associated with subordinate social roles in vertebrates as taxonomically diverse as fishes [Winberg et al, 1992a; and primates [Yodyingyuad et al, 1985]. Increased serotonergic activity is coincident with subordinate behavior, such as decreased feeding rates and locomotor activity and increased receipt of aggressive attacks in salmonid fish [Winberg et al, 1992b], reptiles [Summers and Greenberg, 1995] and mammals [Yodyingyuad et al, 1985]. Staged agonistic encounters between pairs of lizards, Anolis carolinensis, lead to significant increases in serotonin turnover in subordinates (losers), lasting for up to a day, compared to winners (dominant) and isolated controls [Summers and Greenberg, 1995].…”

“…Increased serotonergic activity is coincident with subordinate behavior, such as decreased feeding rates and locomotor activity and increased receipt of aggressive attacks in salmonid fish [Winberg et al, 1992b], reptiles [Summers and Greenberg, 1995] and mammals [Yodyingyuad et al, 1985]. Staged agonistic encounters between pairs of lizards, Anolis carolinensis, lead to significant increases in serotonin turnover in subordinates (losers), lasting for up to a day, compared to winners (dominant) and isolated controls [Summers and Greenberg, 1995]. In addition, activation of catecholaminergic systems appears to be associated with increased levels of aggression [Eichelman, 1987;Zebrowska-Lupina et al, 1991].…”

Memory of opponents is more potent than visual sign stimuli after social hierarchy has been established

“…What is more, the memory of opponents and their status is more important for determining subsequent social behavior and rank than the social sign stimuli presented by the eyespots. We also believe that firmly established of rank relationships, not greatly affected by eyespot color change, nor aggressively disputed, constrained stimulation of serotonergic activity that is usually evident following social antagonism in specific regions of the aggression neurocircuitry [35,37,39,49,68,70,72,73,[75][76][77][78][79].…”

“…Unlike previous studies that have repeatedly demonstrated specifically activated serotonergic systems in centers of aggression neurocircuitry, in the study reported here we measured no change in any serotonergic parameter nucleus accumbens, medial amygdala, lateral amygdala or anterior hypothalamus. These regions particularly, but also other regions, have been demonstrated to rapidly, or for some regions more slowly, increase serotonergic output and/or metabolism [35,37,39,49,68,70,72,73,[75][76][77][78][79]. Aggressive social interactions that determine social status produce different hormonal and central neurochemical patterns, particularly of serotonergic and dopaminergic activity, dependent on status of each individual [33,35,40,[68][69][70]73,[75][76][77][78].…”