Elsevier

Hormones and Behavior

Volume 43, Issue 1, January 2003, Pages 245-253
Hormones and Behavior

Regular article
Rapid glucocorticoid stimulation and GABAergic inhibition of hippocampal serotonergic response: in vivo dialysis in the lizard anolis carolinensis

https://doi.org/10.1016/S0018-506X(02)00014-4Get rights and content

Abstract

Central serotonin (5-HT) is activated during stressful situations and aggressive interactions in a number of species. Glucocorticoids secreted peripherally during stressful events feed back on central systems and may affect 5-HT mediation of stress-induced behavioral events. To test the neuromodulatory effect of stress hormone secretion, serotonin overflow was measured from the hippocampus of the lizard Anolis carolinensis. Microdialysis was used to collect repeated samples from anesthetized lizards, with perfusate measured by HPLC with electrochemical analysis. Following initially high levels of 5-HT, concentrations stabilized to basal levels after approximately 2 h. Intracortical infusion of 200 ng/ml corticosterone evoked transient increases in 5-HT release of approximately 400%. The effect of corticosterone on 5-HT overflow appears to be dose dependent as 20 ng/ml stimulated an increase of 200%, whereas 2 ng/ml stimulated a 50% increase. Administration of 0.1 and 1 ng/ml GABA via the dialysis probe significantly inhibited 5-HT overflow by 20 and 40%, respectively. The duration of GABA inhibition is greater than the stimulatory response for glucocorticoids. Short-lived glucocorticoid stimulation of 5-HT release suggests a possible mechanism for endocrine mediation of continuously changing social behavioral events.

Section snippets

Animals

Adult male lizards, A. carolinensis, were purchased from a commercial supplier (Buck’s Live Animals, La Place, LA) then housed individually in 25 × 25 × 25-cm terraria with a 14L32°C:10D20°C photothermal regimen. Surgical implantation of microdialysis probes and dialysis perfusion throughout the experiment were implemented with lizards exposed to methoxyflurane anesthesia (Mallinckrodt). Body temperature (32°C) was maintained with a heating pad. The stereotaxic coordinates for probe

Basal levels

Serotonergic overflow stabilized approximately 2 h following probe placement (Fig. 1B). Position of the probe in the hippocampal cortex was verified histologically for each animal. Stable unstimulated levels of 5-HT in dialysate from lizard hippocampus were ∼500 fg.

TTx verification

The majority (F = 18.7, P < 0.003; two-way rm compared with baseline control) of the 5-HT measured from the medial cortex of the lizard A. carolinensis was inhibited by the Na+ channel blocker tetrodotoxin (Fig. 1C). Approximately

Discussion

Serotonergic activity in the hippocampus of the lizard A. carolinensis is rapidly and dynamically influenced by local changes in hormone or transmitter concentrations (Fig. 2, Fig. 3). Local rapid stimulation or inhibition of hippocampal 5-HT release supplies the basis for behavioral adaptations during stressful conditions. Corticosterone and GABA modify hippocampal release of 5-HT in a dose- and time-sensitive manner. Extracellular 5-HT overflow in the hippocampus was markedly decreased by

Acknowledgements

This work was supported by NIH Grant P20 RR15567, NSF Grant IBN-9596009, and a grant from the South Dakota Health Research Foundation. We thank David Kappenman for technical support.

References (75)

  • T.G. Dinan

    Serotonin and the regulation of hypothalamic–pituitary–adrenal axis function

    Life Sci.

    (1996)
  • A.J. Emerson et al.

    Stress induces rapid changes in serotonergic activityRestraint and exertion

    Behav. Brain Res.

    (2000)
  • N. Greenberg et al.

    Social status, gonadal state, and the adrenal stress response in the lizard, Anolis carolinensis

    Horm. Behav.

    (1984)
  • T. Inoue et al.

    Effects of acute and chronic administration of high-dose corticosterone and dexamethasone on regional brain dopamine and serotonin metabolism in rats

    Prog. Neuropsychopharmacol. Biol. Psychiatry

    (1996)
  • B.L. Jacobs et al.

    Activity of serotonergic neurons in behaving animals

    Neuropsychopharmacology

    (1999)
  • W.J. Korzan et al.

    Monoaminergic activities of limbic regions are elevated during aggressionInfluence of sympathetic social signaling

    Brain Res.

    (2000)
  • Y. Kuroda et al.

    Effects of adrenalectomy and type I or type II glucocorticoid receptor activation on 5-HT1A and 5-HT2 receptor binding and 5-HT transporter mRNA expression in rat brain

    Brain Res.

    (1994)
  • E.T. Larson et al.

    Serotonin reverses dominant social status

    Behav. Brain Res.

    (2001)
  • V.N. Luine et al.

    Effects of chronic corticosterone ingestion on spatial memory performance and hippocampal serotonergic function

    Brain Res.

    (1993)
  • C.R. McKittrick et al.

    Serotonin receptor binding in a colony model of chronic social stress

    Biol. Psychiatry

    (1995)
  • S.A. Millard et al.

    On the control of brain serotonin turnover rate by end product inhibition

    Brain Res.

    (1972)
  • L. Neckers et al.

    Regulation of 5-hydroxytryptamine metabolism in mousebrain by adrenal glucocorticoids

    Brain Res.

    (1975)
  • M. Orchinik et al.

    Chronic exposure to stress levels of corticosterone alters GABAA receptor subunit mRNA levels in rat hippocampus

    Brain Res. Mol. Brain Res.

    (1995)
  • M.J. Raleigh et al.

    Serotonergic mechanisms promote dominance acquisition in adult male vervet monkeys

    Brain Res.

    (1991)
  • J. Ravindran et al.

    High extracellular GABA levels in hippocampus—as a mechanism of neuronal protection in cerebral ischemia in adrenalectomized gerbils

    Neurosci. Lett.

    (1994)
  • C.H. Summers et al.

    Somatic correlates of adrenergic activity during aggression in the lizard, Anolis. carolinensis

    Horm. Behav.

    (1994)
  • C.H. Summers et al.

    Serotonergic responses to corticosterone and testosterone in the limbic system

    Gen. Comp. Endocrinol.

    (2000)
  • C.H. Summers et al.

    Regional and temporal separation of serotonergic activity mediating social stress

    Neuroscience

    (1998)
  • S. Winberg et al.

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

    Neurosci. Lett.

    (1997)
  • J.L. Yau et al.

    Impact of adrenalectomy on 5-HT6 and 5-HT7 receptor gene expression in the rat hippocampus

    Brain Res. Mol. Brain Res.

    (1997)
  • U. Yodyingyuad et al.

    Relationship between dominance hierarchy, cerebrospinal fluid levels of amine transmitter metabolites (5-hydroxyindole acetic acid and homovanillic acid) and plasma cortisol in monkeys

    Neuroscience

    (1985)
  • E.C. Azmitia et al.

    Corticosterone regulation of tryptophan hydroxylase in midbrain of the rat

    Science

    (1969)
  • L.R. Baxter et al.

    Brain mediation of Anolis social dominance displays. II. Differential forebrain serotonin turnover, and effects of specific 5-HT receptor agonists

    Brain Behav. Evol.

    (2001)
  • C.W. Bradberry et al.

    Sub-picogram determination of serotonin using HPLC with electrochemical detection for microdialysis studies of serotonin release

    Adv. Exp. Med. Biol.

    (1991)
  • C.W. Breuner et al.

    Seasonal regulation of membrane and intracellular corticosteroid receptors in the house sparrow brain

    J. Neuroendocrinol.

    (2001)
  • D. De Maio

    Influence of adrenalectomy and hypophysectomy on cerebral serotonin

    Science

    (1959)
  • A.W. Deckel

    Behavioral changes in Anolis carolinensis following injection with fluoxetine

    Behav. Brain Res.

    (1996)

    • Cited by (0)

    View full text
    Copyright © 2002 Elsevier Science (USA). All rights reserved.