Abstract
Rationale
The medial prefrontal cortex (PFC) receives stress-sensitive dopamine (DA) and noradrenergic (NE) projections from the ventral tegmental area and locus coeruleus, respectively, and evidence from various sources point to a complex functional interaction between these two systems. Stress will also stimulate DA transmission in the nucleus accumbens (NAcc), and our previous work has shown that this response is under the indirect inhibitory control of a DA-sensitive mechanism in PFC.
Objective
We examined the possibility that the NAcc DA stress response is also modulated by prefrontal cortical NE.
Materials and methods
We used voltammetry to study in freely behaving rats the effects of local applications of alpha1 (benoxathian 0.1, 1, 10 nmol), alpha2 (SKF86466), and beta1/2 (alprenolol) receptor selective antagonists into the PFC on the NAcc DA response to tail-pinch stress.
Results
The NAcc DA stress response was dose-dependently inhibited by local PFC blockade of alpha1 receptors. Additional tests revealed, however, that the DA stress response in NAcc is unaffected after local alpha1 receptor activation with cirazoline. Furthermore, at equivalent doses, neither alpha2 nor beta1/2 receptor blockade significantly affected the NAcc DA stress response.
Conclusions
These data indicate that stress-induced activation of subcortical DA transmission is modulated by the NE input to PFC acting at alpha1 receptors. They suggest that, under normal circumstances, this system exerts a facilitatory or enabling influence on the NAcc DA stress response.
Similar content being viewed by others
References
Abercrombie ED, Keefe KA, DiFrischia DS, Zigmond MJ (1989) Differential effects of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial prefrontal cortex. J Neurochem 52:1655–1658
Blanc G, Trovero F, Vezina P, Hervé D, Godeheu A-M, Glowinski J, Tassin J-P (1994) Blockade of prefronto-cortical alpha1-adrenergic receptors prevents locomotor hyperactivity induced by subcortical d-amphetamine injection. Eur J Neurosci 6:293–298
Capella P, Ghasemzadeh B, Mitchell K, Adams RN (1990) Nafion-coated carbon fiber electrodes for neurochemical studies in brain tissue. Electroanalysis 2:175–182
Carboni E, Tanda L, Frau R, Di Chiara G (1990) Blockade of the noradrenaline carrier increases extracellular dopamine concentrations in the prefrontal cortex: evidence that dopamine is taken up in vivo by noradrenergic terminals. J Neurochem 55:1067–1070
Carr DB, Sesack SR (2000) Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesocortical and mesoaccumbens neurons. J Neurosci 20:3864–3873
Carr DB, O’Donnell P, Card JP, Sesack SR (1999) Dopamine terminals in the rat prefrontal cortex synapse on pyramidal sells that project to the nucleus accumbens. J Neurosci 19:11049–11060
Christie MJ, Bridge S, James LB, Beart PM (1985a) Excitotoxic lesions suggest an aspartatergic projection from rat medial prefrontal cortex to ventral tegmental area. Brain Res 333:169–172
Christie MJ, James LB, Beart PM (1985b) An excitatory amino acid projection from medial prefrontal cortex to anterior part of nucleus accumbens in the rat. J Neurochem 45:477–482
Crespi F, Moebius C (1992) In vivo selective monitoring of basal levels of cerebral dopamine using voltammetry with Nafion modified (NA-CRO) carbon fiber micro-electrodes. J Neurosci Methods 42:149–161
Darracq L, Blanc G, Glowinski J, Tassin J-P (1998) Importance of the noradrenaline-dopamine coupling in the locomotor activating effects of d-amphetamine. J Neurosci 18:2729–2739
Deutch AY, Clark WA, Roth RH (1990) Prefrontal cortical dopamine depletion enhances the responsiveness of mesolimbic dopamine neurons to stress. Brain Res 521:311–315
Doherty MD, Gratton A (1992) High-speed chronoamperometric measurements of mesolimbic and nigrostriatal dopamine release associated with repeated daily stress. Brain Res 586:295–302
Doherty MD, Gratton A (1996) Medial prefrontal cortical D1 receptor modulation of the meso-accumbens dopamine response to stress: an electrochemical study in freely-behaving rats. Brain Res 715:86–97
Doherty MD, Gratton A (1997) NMDA receptors in nucleus accumbens modulate stress-induced dopamine release in nucleus accumbens and ventral tegmental area. Synapse 26:225–234
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
Doherty MD, Gratton A (2007) Differential involvement of ventral tegmental GABAA and GABAB receptors in the regulation of the nucleus accumbens dopamine response to stress. Brain Res (in press)
Finlay JM, Zigmond MJ, Abercrombie ED (1995) Increased dopamine and norepinephrine release in medial prefrontal cortex induced by acute and chronic stress: effects of diazepam. Neurosci 64:619–928
Gerhardt GA, Oke AF, Nagy G, Moghaddam B, Adams RN (1984) Nafion-coated electrodes with high sensitivity for CNS electrochemistry. Brain Res 290:390–394
Gioanni Y, Thierry AM, Glowinski J, Tassin JP (1998) Alpha-1 adrenergic, D1, and D2 receptor interactions in the prefrontal cortex: implications for the modality of action of different types of neuroleptics. Synapse 30:362–370
Gobert A, Rivet JM, Audinot V, Newman-Tancredi A, Cistarelli L, Millan MJ (1998) Simultaneous quantification of serotonin, dopamine and noreadrenaline levels in single frontal cortex dialysates of freely-moving rats reveals complex pattern of reciprocal auto- and heteroreceptor-mediated control of release. Neurosci 84:413–429
Grace AA, Bunney BS (1985) Opposing effects of striatonigral feedback pathways on midbrain dopamine cell activity. Brain Res 333:271–284
Gresch PJ, Sved AF, Zigmond MJ, Finley JM (1995) Local influence of endogenous norepinephrine on extracellular dopamine in rat medial prefrontal cortex. J Neurochem 65:111–116
Jodo E, Chiang C, Aston-Jones G (1998) Potent excitatory influence of prefrontal cortex activity on noradrenergic locus coeruleus neurons. Neurosci 83:63–79
Kalivas PW, Duffy P, Eberhardt H (1990) Modulation of A10 dopamine neurons by g-aminobutyric acid agonists. J Pharmacol Exp Ther 253:858–866
Kalivas PW, Churchill L, Klitenick MA (1993) GABA and enkephalin projections from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neurosci 57:1047–1060
Keefe KA, Zved AF, Zigmond MJ, Abercrombie ED (1993) Stress-induced dopamine release in the neostriatum: evaluation of the role of action potentials in nigrostriatal dopamine neurons or local initiation by endogenous excitatory amino acids. J Neurochem 61:1943–1952
Kiyatkin EA (1988) Functional properties of presumed dopamine-containing and other ventral tegmental area neurons in conscious rats. Int J Neurosci 42:21–43
Louilot A, LeMoal M, Simon H (1989) Opposite influences of dopaminergic pathways to the prefrontal cortex or the septum on the dopaminergic transmission in the nucleus accumbens: an in vivo voltammetric study. Neurosci 29:45–56
Mitchell JB, Gratton A (1992) Partial dopamine depletion of the prefrontal cortex leads to enhanced mesolimbic dopamine release elicited by repeated exposure to naturally reinforcing stimuli. J Neurosci 12:3609–3618
Moghaddam B (1993) Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 60:1650–1657
Morari M, O’Connor WT, Ungerstedt U, Bianchi C, Fuxe K (1996) Functional neuroanatomy of the nigrostriatal and striatonigral pathways as studied with dual probe microdialysis in the awake rat—II. Evidence for striatal N-Methyl-d-Aspartate receptor regulation of striatonigral GABAergic transmission and motor function. Neurosci 72:89–97
Pan WHT, Yang S-Y, Lin S-K (2004) Neurochemical interaction between dopaminergic and noradrenergic neurons in the medial prefrontal cortex. Synapse 53:44–52
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic, New York
Raiteri M, Del Carmine R, Bertollinin A, Levi G (1977) Effect of sympathomimetic amines on the synaptosomal transport of noradrenaline, dopamine and 5-hydroxytryptamine. Eur J Pharmacol 41:133–143
Santiago M, Machado A, Cano J (1993) Regulation of the prefrontal cortical dopamine release by GABAA and GABAB receptor agonists and antagonists. Brain Res 630:28–31
Saulskaya N, Marsden CA (1995) Conditioned dopamine release: dependence upon N-methyl-d-aspartate receptors. Neurosci 67:57–63
Sesack SR, Pickel VM (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320:145–160
Sesack SR, Snyder CL, Lewis DA (1995) Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex. J Comp Neurol 363:264–280
Smythe JW, Gratton A (1994) Effects of stress on ventral tegmental unit activity in freely-behaving rat. Soc Neurosci Abstr 20:821
Vezina P, Blanc G, Glowinski J, Tassin JP (1991) Opposed behavioral outputs of increased dopamine transmission in prefrontocortical and subcortical areas: a role for cortical D1 receptor. Eur J Neurosci 3:1001–1007
Wayment HK, Schenk JO, Sorg BA (2001) Characterization of extracellular dopamine clearance in the medial prefrontal cortex: role of monoamine uptake and monoamine oxidase inhibition. J Neurosci 21:35–44
Wheeler D, Boutelle MG, Fillenz M (1995) The role of N-methyl-d-aspartate receptors in the regulation of physiologically released dopamine. Neurosci 65:767–774
Yamamoto BK, Novotney S (1998) Regulation of extracellular dopamine by the norepinephrine transporter. J Neurochem 71:274–280
Acknowledgment
This research was funded by a Canadian Institutes of Health Research grant to A.G.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
NicNiocaill, B., Gratton, A. Medial prefrontal cortical alpha1 adrenoreceptor modulation of the nucleus accumbens dopamine response to stress in Long–Evans rats. Psychopharmacology 191, 835–842 (2007). https://doi.org/10.1007/s00213-007-0723-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00213-007-0723-1