Neurotoxicity Research

, Volume 6, Issue 1, pp 73–78

Effect of stress on prefrontal cortex function

Article

Abstract

Stress is the major epigenetic factor that contributes to the etiology, pathophysiology, and treatment out-come of most psychiatric disorders. Understanding the mechanisms by which stress contributes to these processes can have important implications for improving therapeutic outcome. Considering that a dysfunctional prefrontal cortex has been implicated in many psychiatric disorders, such as schizophrenia and mood disorders, delineating mechanisms by which stress affects prefrontal cortex (PFC) function is critical to our understanding of the role of stress in influencing the disease process. This paper will review recent mechanistic information about the effects of stress on dopamine and glutamate neurotransmission in the PFC.

Keywords

Dopamine Glutamate Prefrontal cortex Microdialysis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abercrombie ED, KA Keefe, DS DiFrischia and MJ Zigmond (1989) Differential effect of stress onin vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex.J. Neurochem. 52, 1655–1658.PubMedCrossRefGoogle Scholar
  2. Ahmed SH and GF Koob (1997) Cocaine- but not food- seeking behavior is reinstated by stress after extinction.Psychopharmacology 132, 289–295.PubMedCrossRefGoogle Scholar
  3. Axelrod J and TD Reisine (1984) Stress hormones: their interaction and regulation.Science 224, 452–459.PubMedCrossRefGoogle Scholar
  4. Bagley J and B Moghaddam (1997) Temporal dynamics of gluta-mate efflux in the prefrontal cortex and in the hippocampus following repeated stress: effects of pretreatment with saline or diazepam.Neuroscience 77, 65–73.PubMedCrossRefGoogle Scholar
  5. Berger B, AM Thierry, JP Tassin and MA Moyne (1976) Dopaminergic innervation of the rat prefrontal cortex: a fluorescence histochemical study.Brain Res. 106, 133–145.PubMedCrossRefGoogle Scholar
  6. Breiter HC, RL Gollub, RM Weisskoff, DN Kennedy, N Makris, JD Berke, JM Goodman, HL Kantor, DR Gastfriend, JP Riorden, RT Mathew, BR Rosen and SE Hyman (1997) Acute effects of cocaine on human brain activity and emotion.Neuron 19, 591–611.PubMedCrossRefGoogle Scholar
  7. Cabib S and S Puglisi-Allegra (1996) Different effects of repeated stressful experiences on mesocortical and mesolimbic dopamine metabolism.Neuroscience 73, 375–380.PubMedCrossRefGoogle Scholar
  8. Carlsson A (1978) Antipsychotic drugs, neurotransmitters, and schizophrenia.Am. J. Psychiatry 135, 164–173.Google Scholar
  9. Carr D and S Sesack (2000) Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synap-tic associations with mesoaccumbens and mesocortical neurons.J. Neurosci. 20, 3864–3873.PubMedGoogle Scholar
  10. Chergui K, P Charlety, H Akaoka, C Saunier, J-L Brunet, M Buda, T Svensson and G Chouvet (1993) Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neuronsin vivo.Eur. J. Neurosci. 5, 137–144.PubMedCrossRefGoogle Scholar
  11. Childress AR and CP O’Brien (2000) Dopamine receptor partial agonists could address the duality of cocaine craving.Trends Pharmacol. Sci. 21, 6–9.PubMedCrossRefGoogle Scholar
  12. Conde F, E Maire-Lepoivre and F Audinat, E Crepel (1995) Afferent connections of the medial frontal cortex of the rat. II. Cortical and subcortical afferents.J. Comp. Neurol. 352, 567–593.PubMedCrossRefGoogle Scholar
  13. Cuadra G, A Zurita, C Lacerra and V Molina (1999) Chronic stress sensitizes frontal cortex dopamine release in response to a subsequent novel stressor: reversal by naloxone.Brain Res. Bull. 48, 303–308.PubMedCrossRefGoogle Scholar
  14. Di Chiara G, P Loddo and G Tanda (1999) Reciprocal changes in prefrontal and limbic dopamine responsiveness to aversive and rewarding stimuli after chronic mild stress: implications for the psychobiology of depression.Biol. Psychiatry 46, 1624–1633.PubMedCrossRefGoogle Scholar
  15. Divac I, A Kosmal, A Bjorklund and O Lindvall (1978) Subcortical projections to the prefrontal cortex in the rat as revealed by the horseradish peroxidase technique.Neuroscience 3, 785–796.PubMedCrossRefGoogle Scholar
  16. Domesick V (1981) Further observation on the anatomy of the nucleus accumbens and caudatoputamen in the rat: similarities and contrasts, inNeurobiology of the Nucleus Accumbens (Chronister RB and JF DeFrance, Eds.) (Haer Inst. Electrophysiological Res., Brunswick, ME), pp 7–39.Google Scholar
  17. Drevets WC (2001) Neuroimaging and neuropathological studies of depression: implications for the cognitive-emotional features of mood disorders.Curr. Opin. Neurobiol. 11, 240–249.PubMedCrossRefGoogle Scholar
  18. Enrico P, M Bouma and J de Vries (1998) The role of afferents to the ventral tegmental area in the handling stress-induced in the release of dopamine in the medial prefrontal cortex: a dual-probe microdialysis study in the rat brain.Brain Res. 779, 205–213.PubMedCrossRefGoogle Scholar
  19. Erb S, Y Shaham and J Stewart (1996) Stress reinstates cocaine-seeking behavior after prolonged extinction and a drug-free period.Psychopharmacology 128, 408–412.PubMedCrossRefGoogle Scholar
  20. Feenstra M, M Botterblom and JF Uum (1998) Local activation of metabolic 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.PubMedGoogle Scholar
  21. Feenstra MG, M Vogel, MH Botterblom, RN Joosten and JP de Bruin (2001) Dopamine and noradrenaline efflux in the rat pre-frontal cortex after classical aversive conditioning to an auditory cue.Eur. J. Neurosci. 13, 1051–1054.PubMedCrossRefGoogle Scholar
  22. Gambarana C, F Masi, A Tagliamonte, S Scheggi, O Ghiglieri and MG De Montis (1999) A chronic stress that impairs reactivity in rats also decreases dopaminergic transmission in the nucleus accumbens: a microdialysis study.J. Neurochem. 72, 2039–2046.PubMedCrossRefGoogle Scholar
  23. Grace AA (2000) Gating of information flow within the limbic system and the pathophysiology of schizophrenia.Brain Res. Rev. 31, 330–341.PubMedCrossRefGoogle Scholar
  24. Herbert H, A Klepper and J Ostwald (1997) Afferent and efferent connections of the ventrolateral tegmental area in the rat.Anat. Embryol. 196, 235–259.PubMedCrossRefGoogle Scholar
  25. Imperato A, S Cabib and S Puglisi-Allegra (1993) Repeated stressful experiences differently affect the time-dependent responses of the mesolimbic dopamine system to the stressor.Brain Res. 601, 333–336.PubMedCrossRefGoogle Scholar
  26. Jackson ME and B Moghaddam (2000) Basolateral amygdala regulation of dopamine release in the nucleus accumbens is governed by the prefrontal cortex.Soc. Neurosci. Abstr. 26, 764.769.Google Scholar
  27. Jedema H and B Moghaddam (1994) Glutamatergic control of dopamine release during stress in rat prefrontal cortex.J. Neurosci. 63, 785–788.Google Scholar
  28. Jedema H and B Moghaddam (1996) Characterization of excitatory amino acid modulation of dopamine release in the prefrontal cortex of conscious rats.J. Neurosci. 66, 1448–1453.Google Scholar
  29. Kalivas PW, P Duffy and J Barrow (1989) Regulation of the meso-corticolimbic dopamine system by glutamic acid receptor subtypes.J. Pharm. Exp. Ther. 251, 378–387.Google Scholar
  30. Karreman M and B Moghaddam (1996a) The prefrontal cortex regulates the basal release of dopamine in the limbic striatum: an effect mediated by ventral tegmental area.J. Neurosci. 66, 589–598.Google Scholar
  31. Karreman M and B Moghaddam (1996b) Effect of a pharmacological stressor on glutamate efflux in the prefrontal cortex.Brain Res. 716, 180–182.PubMedCrossRefGoogle Scholar
  32. Keefe K, M Zigmond and E Abercrombie (1993a)In vivo regulation of extracellular dopamine in the neostriatum influence of impulse activity and local excitatory amino acids.J. Neural Transm. 91, 223–240.CrossRefGoogle Scholar
  33. Keefe K, A Sved, M Zigmond and E Abercrombie (1993b) Stress-induced dopamine release in the neostriatum: evaluation of the role of action potentials in nigrostriatal dopamine neurons or local initiation by endrogenous excitatory amino acids.J. Neurochem. 61, 1943–1952.PubMedCrossRefGoogle Scholar
  34. Kelley AE (1999) Neural integrative activities of nucleus accum-bens subregions in relation to learning and motivation.Psychobiology 27, 198–213.Google Scholar
  35. Koob GF and EJ Nestler (1997) The neurobiology of drug addiction.J. Neuropsychiatry Clin. Neurosci. 9, 482–497.PubMedGoogle Scholar
  36. LeMoal M, Simon H (1991) Mesocorticolimbic dopaminergic network: functional and regulatory roles.Physiol. Rev. 71, 155–234.Google Scholar
  37. Lowy M, L Gault and B Yammamato (1993) Adrenolectomy attenuates stress induced elevation in extracellular glutamate concentration in hippocampus.J. Neurosci. 61, 1957–1960.Google Scholar
  38. Lu W, LM Monteggia and ME Wolf (1999) Withdrawal from repeated amphetamine administration reduces NMDAR1 expression in the rat substantia nigra, nucleus accumbens and medial prefrontal cortex.Eur. J. Neurosci. 11, 3167–3177.PubMedCrossRefGoogle Scholar
  39. Mogensen GL, LW Swanson and M Wu (1983) Neural projections from nucleus accumbens to globus pallidus, substantia innomi-nata, and lateral preoptic-lateral hypothalamic area: an anatomical and electrophysiological investigation in the rat.J. Neurosci. 3, 189–202.Google Scholar
  40. Moghaddam B (1993) Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia.J. Neurosci. 60, 1650–1657.Google Scholar
  41. Moore H, HJ Rose and AA Grace (2001) Chronic cold stress reduces the spontaneous activity of ventral tegmental dopamine neurons.Neuropsychopharmacology 24, 410–419.PubMedCrossRefGoogle Scholar
  42. Morrow BA, RH Roth and JD Elsworth (2000) TMT, a predator odor, elevates mesoprefrontal dopamine metabolic activity and disrupts short-term working memory in the rat.Brain Res. Bull. 52, 519–523.PubMedCrossRefGoogle Scholar
  43. Morrow BA, AW Clark and RH Roth (1993) Stress activation of mesocorticolimbic dopamine neurons: effects of a glycine/NMDA receptor antagonist.Eur. J. Pharmacol. 238, 255–262.PubMedCrossRefGoogle Scholar
  44. Nauta WJH, GP Smith, RLM Faull and VB Domesick (1978) Efferent connections and nigral afferents of the nucleus accum-bens septi in the rat.Neuroscience 3, 385–401.PubMedCrossRefGoogle Scholar
  45. Oades RD and GM Halliday (1987) Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity.Brain Res. 434, 117–165.PubMedGoogle Scholar
  46. O’Donnell P and AA Grace (1995) Synaptic interactions amoung excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J. Neurosci.15, 3622–3639.PubMedGoogle Scholar
  47. Paquet M, M Tremblay, JJ Soghomonian and Y Smith (1997) AMPA and NMDA glutamate receptor subunits in midbrain dopaminergic neurons in the squirrel monkey: an immunohisto-chemical andin situ hybridization study.J. Neurosci. 17, 1377–1396.PubMedGoogle Scholar
  48. Phillipson OT (1979) Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat.J. Comp. Neurol. 187, 117–143.PubMedCrossRefGoogle Scholar
  49. Piazza PV and M Le Moal (1998) The role of stress in drug self-administration.Trends Pharmacol. Sci. 19, 67–74.PubMedCrossRefGoogle Scholar
  50. Piazza P, M Barrot, F Rouge-Pont, M Marinelli, S Maccari, D Abrous, H Simon and M Le Moal (1996) Suppression of gluto-corticoid secretion and antipsychotic drugs have similar effects on the mesolimbic dopaminergic transmission.Proc. Natl. Acad. Sci. USA 93, 15445–15450.PubMedCrossRefGoogle Scholar
  51. Rajkowska G, JJ Miguel-Hidalgo, J Wei, G Dilley, SD Pittman, HY Meltzer, JC Overholser, BL Roth and CA Stockmeier (1999) Morphometric evidence for neuronal and glial prefrontal cell pathology in major depression.Biol. Psychiatry 45, 1085–1098.PubMedCrossRefGoogle Scholar
  52. Rossetti ZL and RA Wise (1996) Stress increases extracellular glu-tamate and dopamine in the ventral tegmental area.Soc. Neurosci. Abstr. #38, 4.Google Scholar
  53. Salamone J (1991) Behavioral pharmachology of dopamine systems: a new synthesis, inThe Mesolimbic Dopamine System: From Motivation to Action (Wilner P and J Scheel-Kruger, Eds.) (J Wiley & Sons, New York, NY).Google Scholar
  54. Sepping P, W Wood, C Bellamy, PK Bridges, P O’Gormann, JR Bartlett and VK Patel (1977) Studies of endocrine activity, plasma tryptophan and catecholamine excretion on psychosurgical patients.Acta Psychiatrica Scand. 56, 1–14.CrossRefGoogle Scholar
  55. Serrano A, M D’Angio and B Scatton (1989) NMDA antagonists block restraint-induced increase in extracellular DOPAC in rat nucleus accumbens.Eur. J. Pharm. 162, 157–166.CrossRefGoogle Scholar
  56. Sesack SR, AY Deutch, RH Roth and BS Bunney (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study withPhaseolus vulgaris leucoagglutinin.J. Comp. Neurol. 290, 213–242.PubMedCrossRefGoogle Scholar
  57. Shaham Y and J Stewart (1995) Stress reinstates heroin-seeking in drug-free animals: an effect mimicking heroin, not withdrawl.Psychopharmacology 119, 334–341.PubMedCrossRefGoogle Scholar
  58. Sorg BA and PW Kalivas (1991) Effects of cocaine and footshock stress on extracellular dopamine levels in the ventral striatum.Brain Res. 559, 29–36.PubMedCrossRefGoogle Scholar
  59. Stoll AL, PF Renshaw, DA Yurgelun-Todd and BM Cohen (2000) Neuroimaging in bipolar disorder: What have we learned.Biol. Psychiatry 48, 505–517.PubMedCrossRefGoogle Scholar
  60. Taber M and H Fibiger (1995) Electrical stimulation of the pre-frontal cortex increases dopamine release in the nucleus accumbens of the rat: modulation by metabotropic glutamate receptors.J. Neurosci. 15, 3896–3904.PubMedGoogle Scholar
  61. Takahata R and B Moghaddam (1998) Glutamatergic regulation of basal and stimulus-activated dopamine release in the prefrontal cortex.J. Neurochem. 71, 1443–1449.PubMedGoogle Scholar
  62. Takahata R and B Moghaddam (2000) Target-specific glutamater-gic regulation of dopamine neurons in the ventral tegmental area.J. Neurochem. 75, 1775–1778.PubMedCrossRefGoogle Scholar
  63. Taylor J and T Robbins (1986) 6-Hydroxydopamine lesions of the nucleus accumbens but not the caudate nucleus attenuate responding with reward-related stimuli produced by intra-accumbens D-amphetamine.Psychopharmacology 90, 390–397.PubMedCrossRefGoogle Scholar
  64. Van Eden C, EMD Hoorneman, RM Buijs, MAH Matthijssun, M Geffard and HBM Uylings (1987) Immunocytochemical localization of dopamine in the prefrontal cortex of the rat at the light electron microscopical level.Neuroscience 22, 849–862.PubMedCrossRefGoogle Scholar
  65. Volkow ND and JS Fowler (2000) Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex.Cereb. Cortex 10, 318–325.PubMedCrossRefGoogle Scholar
  66. Volkow ND, JS Fowler and GJ Wang (1999) Imaging studies on the role of dopamine in cocaine reinforcement and addiction in humans.J. Psychopharmacol. 13, 337–345.PubMedCrossRefGoogle Scholar
  67. Wang T and ED French (1993) Electrophysiological evidence for the existence of NMDA and non-NMDA receptors on rat ventral tegmental dopamine neurons.Synapse 13, 270–277.PubMedCrossRefGoogle Scholar
  68. Wang T and E French (1995) NMDA, kainate and AMPA depolarize non-dopamine neurons in the rat ventral tegmentum.Brain Res. Bull. 36, 39–43.PubMedCrossRefGoogle Scholar
  69. Weinberger D, K Berman and R Zec (1986) Physiological dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow (rCBF) evidence.Arch. Gen. Psychiatr. 43, 114–125.PubMedGoogle Scholar
  70. Westerink BHC, HF Kwint and JB de Vries (1997) Eating-induced dopamine release from mesolimbic neurons is mediated by NMDA receptors in the ventral tegmental area: a dual-probe microdialysis study.J. Neurochem. 69, 662–668.PubMedCrossRefGoogle Scholar
  71. White F (1996) Synaptic regulation of mesocorticolimbic dopamine neurons.Annu. Rev. Neurosci. 19, 405–436.PubMedCrossRefGoogle Scholar
  72. Wise RA and PP Rompre PP (1989) Brain dopamine and reward.Annu. Rev. Psychol. 40, 191–225.PubMedCrossRefGoogle Scholar

Copyright information

© FP Graham Publishing Co 2004

Authors and Affiliations

  1. 1.Department of NeurosciencePittsburghUSA

Personalised recommendations