Abstract
Although stress is an extensively investigated phenomenon, the effects of specific stressors on the pharmacologic activity of routinely administered drugs are less well characterized. We designed the present study to investigate the effect of handling stress on catecholaminergic responsivity following an acute methylphenidate (MP, Ritalin) challenge in the medial prefrontal cortex (mPFC). Norepinephrine (NE) and dopamine (DA) levels were simultaneously measured in 15-min samples of PFC dialysate using HPLC coupled with electrochemical detection. Sprague-Dawley rats were handled for 15 min, which produced an increase from basal extracellular DA and NE levels. Handling stress attenuates the DA response when administered 2 h prior to IP MP, whereas handling stress enhances the DA response when administered simultaneously with IG MP. These findings suggest that persistent alterations in mesocorticolimbic DA-ergic activity are induced by a short exposure to restraint stress as evidenced by the altered response to MP challenge.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Abercrombie ED, Keefe KA, DiFrischia DS, Zigmond MJ . (1989): Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52: 1655–1658
Carrizo E, Cano G, Suarez-Roca H, Bonilla E . (1997): Motor activity and quantitative autoradiographic analysis of muscarinic receptors in the brain of rats subjected to the forced swimming test. Brain Res Bull 42: 133–139
Doherty MD, Gratton A . (1999): Effects of medial prefrontal cortical injections of GABA receptor agonists and antagonists on the local and nucleus accumbens dopamine responses to stress. Synapse 32: 288–300
Enrico P, Bouma M, de Vries JB, Westerink BH . (1998): The role of afferents to the ventral tegmental area in the handling stress-induced increase in the release of dopamine in the medial prefrontal cortex: a dual-probe microdialysis study in the rat brain. Brain Res 779: 205–213
Feenstra MG, Botterblom MH, van Uum JF . (1995): Novelty-induced increase in dopamine release in the rat prefrontal cortex in vivo: inhibition by diazepam. Neurosci Lett 189: 81–84
Feenstra MG, Botterblom MH, van Uum JF . (1998): Local activation of metabotropic glutamate receptors inhibits the handling-induced increased release of dopamine in the nucleus accumbens but not that of dopamine or noradrenaline in the prefrontal cortex: comparison with inhibition of ionotropic receptors. J Neurochem 70: 1104–1113
Feenstra MG, Teske G, Botterblom MH, De Bruin JP . (1999): Dopamine and noradrenaline release in the prefrontal cortex of rats during classical aversive and appetitive conditioning to a contextual stimulus: interference by novelty effects. Neurosci Lett 272: 179–182
Gatley SJ, Pan D, Chen R, Chaturvedi G, Ding YS . (1996): Affinities of methylphenidate derivatives for dopamine, norepinephrine and serotonin transporters. Life Sci 58: 231–239
Gerasimov MR, Franceschi M, Volkow ND, Gifford A, Gatley SJ, Marsteller D, Molina PE, Dewey SL . (2000): Comparison between intraperitoneal and oral methylphenidate administration: A microdialysis and locomotor activity study. J Pharmacol Exp Ther 295: 51–57
Grace AA . (2000): The tonic/phasic model of dopamine system regulation and its implications for understanding alcohol and psychostimulant craving. Addiction 95(Suppl 2): S119–S128
Gresch PJ, Sved AF, Zigmond MJ, Finlay JM . (1995): Local influence of endogenous norepinephrine on extracellular dopamine in rat medial prefrontal cortex. J Neurochem 65: 111–116
Horger BA, Roth RH . (1996): The role of mesoprefrontal dopamine neurons in stress. Crit Rev Neurobiol 10: 395–418
Ihalainen JA, Riekkinen P Jr, Feenstra MG . (1999): Comparison of dopamine and noradrenaline release in mouse prefrontal cortex, striatum and hippocampus using microdialysis. Neurosci Lett 277: 71–74
Imperato A, Puglisi-Allegra S, Casolini P, Angelucci L . (1991): Changes in brain dopamine and acetylcholine release during and following stress are independent of the pituitary-adrenocortical axis. Brain Res 538: 111–117
Kawahara H, Kawahara Y, Westerink BH . (2000): The role of afferents to the locus coeruleus in the handling stress-induced increase in the release of noradrenaline in the medial prefrontal cortex: a dual-probe microdialysis study in the rat brain. Eur J Pharmacol 387: 279–286
Kawahara Y, Kawahara H, Westerink BH . (1999): Comparison of effects of hypotension and handling stress on the release of noradrenaline and dopamine in the locus coeruleus and medial prefrontal cortex of the rat. Naunyn Schmiedebergs Arch Pharmacol 360: 42–49
Kuczenski R, Segal DS . (1997): Effects of methylphenidate on extracellular dopamine, serotonin, and norepinephrine: comparison with amphetamine. J Neurochem 68: 2032–2037
Kuczenski R, Segal DS . (2001): Locomotor effects of acute and repeated threshold doses of amphetamine and methylphenidate: relative roles of dopamine and norepinephrine. J Pharmacol Exp Ther 296: 876–883
Mathe JM, Nomikos GG, Blakeman KH, Svensson TH . (1999): Differential actions of dizocilpine (MK-801) on the mesolimbic and mesocortical dopamine systems: role of neuronal activity. Neuropharmacology 38: 121–128
Nakane H, Shimizu N, Hori T . (1994): Stress-induced norepinephrine release in the rat prefrontal cortex measured by microdialysis. Am J Physiol 267: R1559–R1566
Raiteri M, Del Carmine R, Bertollini A, Levi G . (1977): Effect of sympathomimetic amines on the synaptosomal transport of noradrenaline, dopamine and 5-hydroxytryptamine. Eur J Pharmacol 41: 133–143
Shimizu N, Nakane H, Hori T, Hayashi Y . (1994): CRF receptor antagonist attenuates stress-induced noradrenaline release in the medial prefrontal cortex of rats. Brain Res 654: 145–148
Suaud-Chagny MF, Chergui K, Chouvet G, Gonon F . (1992): Relationship between dopamine release in the rat nucleus accumbens and the discharge activity of dopaminergic neurons during local in vivo application of amino acids in the ventral tegmental area. Neuroscience 49: 63–72
Svensson L, Ahlenius S . (1983): Suppression of exploratory locomotor activity by the local application of dopamine or l-noradrenaline to the nucleus accumbens of the rat. Pharmacol Biochem Behav 19: 693–699
Van Gaalen M, Kawahara H, Kawahara Y, Westerink BH . (1997): The locus coeruleus noradrenergic system in the rat brain studied by dual-probe microdialysis. Brain Res 763: 56–62
Volkow ND, Wang G, Fowler JS, Logan J, Gerasimov M, Maynard L, Ding Y, Gatley SJ, Gifford A, Franceschi D . (2001): Therapeutic doses of oral methylphenidate significantly increase extracellular dopamine in the human brain. J Neurosci 21: RC121
Acknowledgements
This research was carried out at Brookhaven National Laboratory under contract with the U.S. Department of Energy Office of Biological and Environmental Research (USDOE/OBER DE-AC02-98CH10886), and by the National Institutes of Mental Health (NIMH MH49165 and NIMH R2955155) and the National Institute on Drug Abuse (5RO-DA06278 and DA09490).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marsteller, D., Gerasimov, M., Schiffer, W. et al. Acute Handling Stress Modulates Methylphenidate-induced Catecholamine Overflow in the Medial Prefrontal Cortex. Neuropsychopharmacol 27, 163–170 (2002). https://doi.org/10.1016/S0893-133X(02)00288-9
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1016/S0893-133X(02)00288-9
Keywords
This article is cited by
-
Chronic Methylphenidate Alters Tonic and Phasic Glutamate Signaling in the Frontal Cortex of a Freely-Moving Rat Model of ADHD
Neurochemical Research (2019)
-
Ventral tegmental area dopamine revisited: effects of acute and repeated stress
Psychopharmacology (2016)
-
Selective solid-phase extraction of catecholamines from plasma using nanofibers doped with crown ether and their quantitation by HPLC with electrochemical detection
Analytical and Bioanalytical Chemistry (2016)
-
Analysis of epinephrine, norepinephrine, and dopamine in urine samples of hospital patients by micellar liquid chromatography
Analytical and Bioanalytical Chemistry (2015)
-
Pharmacotherapy for Attention-Deficit/Hyperactivity Disorder: From Cells to Circuits
Neurotherapeutics (2012)