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

Matter, John M.; Ronan, Patrick J.; Summers, Cliff H.

doi:10.1159/000006526

Cited by 79 publications

(46 citation statements)

References 25 publications

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“…Recent research conflicts with the prevailing view that 5-HT activity necessarily suppresses aggressive behavior. High 5-HT turnover in parts of the brain has been found in aggressive and dominant individuals (Korzan et al, 2000;Matter et al, 1998) and a "primed" serotonergic system may be necessary to enable an individual to produce an appropriate behavioral response in a complex social context (Sperry et al, 2005). These findings would help explain the apparent paradox we observed in our fish wherein 5-HT injections further masculinized the males' EODs (Stoddard et al, 2003).…”

Section: Discussionmentioning

confidence: 54%

Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus

Allee

Markham

Salazar

et al. 2008

Hormones and Behavior

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Serotonin (5-HT) is an indirect modulator of the electric organ discharge (EOD) in the weakly electric gymnotiform fish, Brachyhypopomus pinnicaudatus. Injections of 5-HT enhance EOD waveform "masculinity", increasing both waveform amplitude and the duration of the second phase. This study investigated the pharmacological identity of 5-HT receptors that regulate the electric waveform and their effects on EOD amplitude and duration. We present evidence that two sets of serotonin receptors modulate the EOD in opposite directions. We found that the 5HT 1A R agonist 8-OH-DPAT diminishes EOD duration and amplitude while the 5HT 1A R antagonist WAY100635 increases these parameters. In contrast, the 5HT 2 R agonist α-Me-5-HT increases EOD amplitude but not duration, yet 5-HT-induced increases in EOD duration can be inhibited by blocking 5HT 2A/2C -like receptors with ketanserin. These results show that 5-HT exerts bi-directional control of EOD modulations in B. pinnicaudatus via action at receptors similar to mammalian 5HT 1A and 5HT 2 receptors. The discordant amplitude and duration response suggests separate mechanisms for modulating these waveform parameters. KeywordsSerotonin; Electric organ discharge; Communication signal; 5HT 1A receptor; 5HT 2 receptor; Social interaction; Dominance hierarchy Serotonin (5-HT) is a neuromodulator so ubiquitous that hardly any physiological function or behavior is free from its direct or indirect effects. As a result, a full account of neuroendocrine control of behavior requires a thorough assessment of 5-HT's function across a wide range of circumstances, even as the pervasive presence of 5-HT in the nervous system complicates unambiguous assessment of its functions. Particularly, serotonin is involved in the regulation of diametrically opposed behaviors, aggression and subordinance (Summers and Winberg, 2006). Serotonin activity rises in both dominant and subordinate males but rapidly returns to baseline in dominants while it stays chronically high in subordinates (Overli et al., 1999;Summers and Winberg, 2006). Prior social defeat or success during aggressive interactions affects future aggressive behaviors and the activity of the serotonergic system (Winberg et al., 1992;Winberg et al., 1997b). Furthermore, social experience affects the regulatory effect of serotonin on dominant behaviors via serotonin receptors 1A and 2A (Yeh et al., 1996). Pharmaceutical 5HT 1A agonists inhibit aggression or induce submissive behaviors in a wide range of non-mammalian vertebrates including green anoles (Deckel and Fuqua, 1998), Arctic charr (Hoglund et al., 2002;Winberg and Nilsson, 1993) Bell et al., 2007). In addition, 5HT 1A receptors operate as both postsynaptic receptors and as pre-synaptic autoreceptors to either suppress or stimulate stress responses in teleosts as they do in mammals (Hoglund et al., 2002). Despite the functionally and anatomically conserved nature of the serotonin system in vertebrates (Parent et al., 1984) and the abundance of data indicating a role for 5HT ...

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Section: Discussionmentioning

confidence: 54%

Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus

Allee

Markham

Salazar

et al. 2008

Hormones and Behavior

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“…A variety of other evidence demonstrates a role for DA in aggression, including data from lizards (Matter et al, 1998) and mammals. In mammals, the A10 neurons in particular are known to influence agonistic behavior.…”

Section: Discussionmentioning

confidence: 99%

“…This finding should be interpreted cautiously, however, because the fighting in our tests was induced by mate competition, and may therefore be partly confounded with sexual motivation. Further studies in a territorial species would help to resolve this issue (e.g., using a resident-intruder paradigm).A variety of other evidence demonstrates a role for DA in aggression, including data from lizards (Matter et al, 1998) and mammals. In mammals, the A10 neurons in particular are known to influence agonistic behavior.…”

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confidence: 99%

Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches

2006

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Dopamine (DA) is produced in numerous brain areas and influences a wide variety of social behaviors, but very few data are available to establish the socially-relevant response properties of most DA populations, which comprise eight cell groups numbered A8-A15. Anatomically, these DA populations are evolutionarily conserved, and all have been identified in both birds and mammals. We now report the Fos responses of tyrosine hydroxylase-immunoreactive (TH-ir; putatively dopaminergic) neurons in the A8-A15 cell groups of male zebra finches following exposure to a control condition or one of six different social stimuli: A heterospecific male, conspecific male, fighting in a mate competition paradigm (which includes both male and female stimuli), a courtship interaction without physical contact, a courtship interaction with physical contact but no mounting, and a courtship interaction with mounting. We found that the DA cell groups exhibit distinctive profiles of responsiveness to social stimuli. Fos induction in A8, A9, A10 and midbrain A11 neurons increased significantly in response to a variety of conspecific stimuli, but not heterospecific stimuli. In contrast, Fos induction in the preoptic A14 neurons was observed specifically in response to sexual interactions, and Fos induction in hypothalamic A11 neurons appears to primarily reflect the performance of courtship singing. Infundibular A12 neurons, which may be involved in stress-related processes, showed the highest level of TH+Fos colocalization in control subjects. This colocalization decreased in response to all conspecific stimuli except fighting, and did not decrease following exposure to a heterospecific male. Keywords dopamine; forebrain; aggression; sexual behavior; tyrosine hydroxylase; Fos Dopamine (DA) is known to influence a variety of social behaviors, particularly male sexual behavior, in multiple vertebrate groups (Warner et al., 1991;Pomerantz, 1992;Absil et al., 1994;Hull et al., 1995;Dominguez et al., 2001;Woolley et al., 2001;Melis et al., 2003;Charlier et al., 2005), and DA cells are distributed in homologous groups across the vertebrate classes (Bailhache and Balthazart, 1993;Bottjer, 1993;Gonzalez and Smeets, 1994;Reiner et al., 1994;Tillet, 1994;Appeltants et al., 2001;Adrio et al., 2002). This similarity across vertebrates is particularly clear when comparing mammals and birds, which each have dopaminergic neurons (immunopositive for tyrosine hydroxylase, TH, and immunonegative for dopamine β-hydroxylase) localized to eight populations of the basal forebrain and brainstem numbered A8 through A15 (Reiner et al., 1994;Tillet, 1994). However, it is largely unknown how these various DA populations respond to a broad range of social stimuli, so we have here examined DA neuronal responses to a variety of interactions with heterospecific and conspecific animals. Extensive data suggest that the release of DA into the preoptic area (POA) controls male sexual behavior. Administrations of the DA agonist apomorphine into the medial POA faci...

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“…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].…”

Section: Discussionmentioning

confidence: 88%

“…Following centrifugation, 2 μl of a 1 mg/ml ascorbate oxidase solution (Sigma, St. Louis, MO) was added to each sample. The supernatant was removed and 40 μl was injected into a chromatographic system (Waters Associates, Inc.) and analyzed with an ESA 5200 Coulochem II liquid chromatography system with electrochemical detection (ESA, Bedford, MA) using two electrodes at reducing, then oxidizing potentials of −40 and +320 mV [49]. The sodium phosphate-10% acetonitrile mobile phase was brought to a final pH of 2.9.…”

Section: Analysis Of Central Monoaminesmentioning

confidence: 99%

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

Korzan

Höglund²,

Watt

et al. 2007

Behavioural Brain Research

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During agonistic interactions between male Anolis carolinensis, perception of a visual sign stimulus (darkened eyespots) not only inhibits aggression and promotes initial attainment of dominant social status, but also evokes distinct neuroendocrine responses in each opponent. This study was designed to examine the effect of eyespot manipulation on behavior and social rank during a second interaction between opponents that had previously established a natural dyadic social hierarchy. Prior to a second interaction, eyespots of familiar size-matched combatants were manipulated to reverse information conveyed by this visual signal. Eyespots on the previously dominant male were masked with green paint to indicate low aggression and social status. Previously subordinate males had their eyespots permanently marked with black paint to convey high aggression and status. Opponents were then repaired for a second 10 min interaction following either one or three days of separation. Aggression was generally decreased and social status between pairs remained reasonably consistent. Unlike rapidly activated monoaminergic activity that occurs following the initial pairing, most brain areas sampled were not affected when animals were re-introduced, regardless of visual signal reversal or length of separation between interactions. However in males with "normal" eyespot color, dominant males had reduced serotonergic activity in CA 3 and raphé, while subordinate males exhibited elevated CA 3 dopaminergic activity. Reversing eyespot color also reversed serotonergic activity in raphé and dopaminergic activity in CA 3 after three days of separation. The results suggest that males remember previous opponents, and respond appropriately to their previous social rank in spite of eyespot color.

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

Cited by 79 publications

References 25 publications

Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus

Opposing actions of 5HT1A and 5HT2-like serotonin receptors on modulations of the electric signal waveform in the electric fish Brachyhypopomus pinnicaudatus

Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches

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

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