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Impact of Stress on Prefrontal Glutamatergic, Monoaminergic and Cannabinoid Systems

  • M. Danet Lapiz-BluhmEmail author
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 18)

Abstract

Stress has been shown to have marked and divergent effects on learning and memory which involves specific brain regions, such as spatial and declarative memory involving the hippocampus, memory of emotional arousing experiences and fear involving the amygdala, and executive functions and fear extinction involving the prefrontal cortex or the PFC. Response to stress involves a coordinated activation of a constellation of physiological systems including the activation of the hypothalamic-pituitary-adrenal (HPA) axis and other modulatory neurotransmitters and signaling systems. This paper presents a concise review of the effects of stress and glucocorticoids on the glutamatergic and monoaminergic (including noradrenergic, dopaminergic, and serotonergic systems) neurotransmitter systems as well as endocannabinoid signaling. Because of the breadth of the scope of this topic, the review is limited to the effects of stress on these brain systems on the prefrontal cortex, and where relevant, the hippocampus and the amygdala.

Keywords

Stress Glucocorticoids Glutamatergic Noradrenergic Dopaminergic Serotonergic Endocannabinoid 

Notes

Acknowledgments

Dr. Lapiz-Bluhm receives funding from the Robert Wood Johnson Nurse Faculty Program. She sincerely thanks Dr. Carrie Jo Braden, Dr. James Michael Bluhm and Dr. Charles Marsden for taking the time to read the manuscript.

References

  1. Andolina D, Maran D, Valzania A, Conversi D, Puglisi-Allegra S (2013) Prefrontal/amygdalar system determines stress coping behavior through 5-HT/GABA connection. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 38(10):2057–2067Google Scholar
  2. Asan E, Steinke M, Lesch KP (2013) Serotonergic innervation of the amygdala: targets, receptors, and implications for stress and anxiety. Histochem Cell Biol 139(6):785–813PubMedGoogle Scholar
  3. Aso E, Ozaita A, Valdizan EM, Ledent C, Pazos A, Maldonado R, Valverde O (2008) BDNF impairment in the hippocampus is related to enhanced despair behavior in CB1 knockout mice. J Neurochem 105(2):565–572PubMedGoogle Scholar
  4. Atwood BK, Mackie K (2010) CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 160(3):467–479PubMedCentralPubMedGoogle Scholar
  5. Barik J, Marti F, Morel C, Fernandez SP, Lanteri C, Godeheu G, Tassin JP, Mombereau C, Faure P, Tronche F (2013) Chronic stress triggers social aversion via glucocorticoid receptor in dopaminoceptive neurons. Science (New York, N.Y.) 339(6117):332–335Google Scholar
  6. Barna I, Zelena D, Arszovszki AC, Ledent C (2004) The role of endogenous cannabinoids in the hypothalamo-pituitary-adrenal axis regulation: in vivo and in vitro studies in CB1 receptor knockout mice. Life Sci 75(24):2959–2970PubMedGoogle Scholar
  7. Baumeister D, Lightman SL, Pariante CM (2014) The interface of stress and the HPA axis in behavioural phenotypes of mental illness. In: Current topics in behavioral neurosciences. doi: 10.1007/7854_2014_304
  8. Bellocchio L, Cervino C, Pasquali R, Pagotto U (2008) The endocannabinoid system and energy metabolism. J Neuroendocrinol 20(6):850–857PubMedGoogle Scholar
  9. Berridge CW, Waterhouse BD (2003) The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42(1):33–84PubMedGoogle Scholar
  10. Beyer CE, Cremers TI (2008) Do selective serotonin reuptake inhibitors acutely increase frontal cortex levels of serotonin? Eur J Pharmacol 580(3):350–354PubMedGoogle Scholar
  11. Beylin AV, Shors TJ (2003) Glucocorticoids are necessary for enhancing the acquisition of associative memories after acute stressful experience. Horm Behav 43(1):124–131PubMedCentralPubMedGoogle Scholar
  12. Bubar MJ, Cunningham KA (2006) Serotonin 5-HT2A and 5-HT2C receptors as potential targets for modulation of psychostimulant use and dependence. Curr Top Med Chem 6(18):1971–1985PubMedGoogle Scholar
  13. Burghardt PR, Love TM, Stohler CS, Hodgkinson C, Shen PH, Enoch MA, Goldman D, Zubieta JK (2012) Leptin regulates dopamine responses to sustained stress in humans. J Neurosci: Off J Soc Neurosci 32(44):15369–15376Google Scholar
  14. Burke AR, Forster GL, Novick AM, Roberts CL, Watt MJ (2013) Effects of adolescent social defeat on adult amphetamine-induced locomotion and corticoaccumbal dopamine release in male rats. Neuropharmacology 67:359–369PubMedGoogle Scholar
  15. Burke AR, Renner KJ, Forster GL, Watt MJ (2010) Adolescent social defeat alters neural, endocrine and behavioral responses to amphetamine in adult male rats. Brain Res 1352:147–156PubMedCentralPubMedGoogle Scholar
  16. Burke AR, Watt MJ, Forster GL (2011) Adolescent social defeat increases adult amphetamine conditioned place preference and alters D2 dopamine receptor expression. Neuroscience 197:269–279PubMedCentralPubMedGoogle Scholar
  17. Butts KA, Weinberg J, Young AH, Phillips AG (2011) Glucocorticoid receptors in the prefrontal cortex regulate stress-evoked dopamine efflux and aspects of executive function. Proc Natl Acad Sci U S A 108(45):18459–18464PubMedCentralPubMedGoogle Scholar
  18. Carlson G, Wang Y, Alger BE (2002) Endocannabinoids facilitate the induction of LTP in the hippocampus. Nat Neurosci 5(8):723–724PubMedGoogle Scholar
  19. Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N (2007) The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci: Off J Soc Neurosci 27(11):2781–2787Google Scholar
  20. Chang MS, Sved AF, Zigmond MJ, Austin MC (2000) Increased transcription of the tyrosine hydroxylase gene in individual locus coeruleus neurons following footshock stress. Neuroscience 101(1):131–139PubMedGoogle Scholar
  21. Corchero J, Romero J, Berrendero F, Fernandez-Ruiz J, Ramos JA, Fuentes JA, Manzanares J (1999) Time-dependent differences of repeated administration with Delta9-tetrahydrocannabinol in proenkephalin and cannabinoid receptor gene expression and G-protein activation by mu-opioid and CB1-cannabinoid receptors in the caudate-putamen. Brain Res Mol Brain Res 67(1):148–157PubMedGoogle Scholar
  22. Deutsch DG, Ueda N, Yamamoto S (2002) The fatty acid amide hydrolase (FAAH). Prostaglandins Leukot Essent Fatty Acids 66(2–3):201–210PubMedGoogle Scholar
  23. Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, Gibson D, Mandelbaum A, Etinger A, Mechoulam R (1992) Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science (New York, N.Y.) 258(5090):1946–1949Google Scholar
  24. Diamond DM, Campbell AM, Park CR, Halonen J, Zoladz PR (2007) The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plast 2007:60803PubMedCentralPubMedGoogle Scholar
  25. Dinh TP, Freund TF, Piomelli D (2002) A role for monoglyceride lipase in 2-arachidonoylglycerol inactivation. Chem Phys Lipids 121(1–2):149–158PubMedGoogle Scholar
  26. Diorio D, Viau V, Meaney MJ (1993) The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress. J Neurosci: Off J Soc Neurosci 13(9):3839–3847Google Scholar
  27. Doppler W (1994) Regulation of gene expression by prolactin. Rev Physiol Biochem Pharmacol 124:93–130PubMedGoogle Scholar
  28. Doyon WM, Thomas AM, Ostroumov A, Dong Y, Dani JA (2013) Potential substrates for nicotine and alcohol interactions: a focus on the mesocorticolimbic dopamine system. Biochem Pharmacol 86(8):1181–1193PubMedCentralPubMedGoogle Scholar
  29. Ebner K, Bosch OJ, Kromer SA, Singewald N, Neumann ID (2005) Release of oxytocin in the rat central amygdala modulates stress-coping behavior and the release of excitatory amino acids. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 30(2):223–230Google Scholar
  30. Ebner K, Singewald GM, Whittle N, Ferraguti F, Singewald N (2008) Neurokinin 1 receptor antagonism promotes active stress coping via enhanced septal 5-HT transmission. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 33(8):1929–1941Google Scholar
  31. Erecinska M, Silver IA (1990) Metabolism and role of glutamate in mammalian brain. Prog Neurobiol 35(4):245–296PubMedGoogle Scholar
  32. Evanson NK, Tasker JG, Hill MN, Hillard CJ, Herman JP (2010) Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology 151(10):4811–4819PubMedCentralPubMedGoogle Scholar
  33. Furay AR, Bruestle AE, Herman JP (2008) The role of the forebrain glucocorticoid receptor in acute and chronic stress. Endocrinology 149(11):5482–5490PubMedCentralPubMedGoogle Scholar
  34. Ganon-Elazar E, Akirav I (2009) Cannabinoid receptor activation in the basolateral amygdala blocks the effects of stress on the conditioning and extinction of inhibitory avoidance. J Neurosci: Off J Soc Neurosci 29(36):11078–11088Google Scholar
  35. Garrett JE, Wellman CL (2009) Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 162(1):195–207PubMedCentralPubMedGoogle Scholar
  36. Gasser PJ, Lowry CA, Orchinik M (2006) Corticosterone-sensitive monoamine transport in the rat dorsomedial hypothalamus: potential role for organic cation transporter 3 in stress-induced modulation of monoaminergic neurotransmission. J Neurosci: Off J Soc Neurosci 26(34):8758–8766Google Scholar
  37. Gasser PJ, Orchinik M, Raju I, Lowry CA (2009) Distribution of organic cation transporter 3, a corticosterone-sensitive monoamine transporter, in the rat brain. J Comp Neurol 512(4):529–555PubMedGoogle Scholar
  38. Gorzalka BB, Hill MN (2011) Putative role of endocannabinoid signaling in the etiology of depression and actions of antidepressants. Prog Neuropsychopharmacol Biol Psychiatry 35(7):1575–1585PubMedGoogle Scholar
  39. Gorzalka BB, Hill MN, Hillard CJ (2008) Regulation of endocannabinoid signaling by stress: implications for stress-related affective disorders. Neurosci Biobehav Rev 32(6):1152–1160PubMedGoogle Scholar
  40. Grace AA, Floresco SB, Goto Y, Lodge DJ (2007) Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30(5):220–227PubMedGoogle Scholar
  41. Guptan P, Dhingra A, Panicker MM (1997) Multiple transcripts encode the 5-HT1F receptor in rodent brain. Neuroreport 8(15):3317–3321PubMedGoogle Scholar
  42. Hale MW, Shekhar A, Lowry CA (2012) Stress-related serotonergic systems: implications for symptomatology of anxiety and affective disorders. Cell Mol Neurobiol 32(5):695–708PubMedCentralPubMedGoogle Scholar
  43. Haller J, Varga B, Ledent C, Barna I, Freund TF (2004) Context-dependent effects of CB1 cannabinoid gene disruption on anxiety-like and social behaviour in mice. Eur J Neurosci 19(7):1906–1912PubMedGoogle Scholar
  44. Harro J, Oreland L, Vasar E, Bradwejn J (1995) Impaired exploratory behaviour after DSP-4 treatment in rats: implications for the increased anxiety after noradrenergic denervation. Eur Neuropsychopharmacol: J Eur Coll Neuropsychopharmacol 5(4):447–455Google Scholar
  45. Herkenham M, Lynn AB, Johnson MR, Melvin LS, de Costa BR, Rice KC (1991) Characterization and localization of cannabinoid receptors in rat brain: a quantitative in vitro autoradiographic study. J Neurosci: Off J Soc Neurosci 11(2):563–583Google Scholar
  46. Herman JP, Mueller NK (2006) Role of the ventral subiculum in stress integration. Behav Brain Res 174(2):215–224PubMedGoogle Scholar
  47. Hill MN, Hillard CJ, MCEwen BS (2011) Alterations in corticolimbic dendritic morphology and emotional behavior in cannabinoid CB1 receptor-deficient mice parallel the effects of chronic stress. Cereb cortex (New York, N.Y.: 1991) 21(9):2056–2064Google Scholar
  48. Hill MN, Hunter RG, McEwen BS (2009) Chronic stress differentially regulates cannabinoid CB1 receptor binding in distinct hippocampal subfields. Eur J Pharmacol 614(1–3):66–69PubMedCentralPubMedGoogle Scholar
  49. Hill MN, Patel S, Campolongo P, Tasker JG, Wotjak CT, Bains JS (2010) Functional interactions between stress and the endocannabinoid system: from synaptic signaling to behavioral output. J Neurosci: Off J Soc Neurosci 30(45):14980–14986Google Scholar
  50. Hill MN, Tasker JG (2012) Endocannabinoid signaling, glucocorticoid-mediated negative feedback, and regulation of the hypothalamic-pituitary-adrenal axis. Neuroscience 204:5–16PubMedCentralPubMedGoogle Scholar
  51. Itoi K, Jiang YQ, Iwasaki Y, Watson SJ (2004) Regulatory mechanisms of corticotropin-releasing hormone and vasopressin gene expression in the hypothalamus. J Neuroendocrinol 16(4):348–355PubMedGoogle Scholar
  52. Itoi K, Sugimoto N (2010) The brainstem noradrenergic systems in stress, anxiety and depression. J Neuroendocrinol 22(5):355–361PubMedGoogle Scholar
  53. Jacobs BL, Fornal CA (1999) Activity of serotonergic neurons in behaving animals. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 21(2 Suppl):9S–15SGoogle Scholar
  54. Jaferi A, Bhatnagar S (2006) Corticosterone can act at the posterior paraventricular thalamus to inhibit hypothalamic-pituitary-adrenal activity in animals that habituate to repeated stress. Endocrinology 147(10):4917–4930PubMedGoogle Scholar
  55. Jaferi A, Nowak N, Bhatnagar S (2003) Negative feedback functions in chronically stressed rats: role of the posterior paraventricular thalamus. Physiol Behav 78(3):365–373PubMedGoogle Scholar
  56. Jedema HP, Grace AA (2004) Corticotropin-releasing hormone directly activates noradrenergic neurons of the locus ceruleus recorded in vitro. J Neurosci: Off J Soc Neurosci 24(43):9703–9713Google Scholar
  57. Joels M, Baram TZ (2009) The neuro-symphony of stress. Nat Rev Neurosci 10(6):459–466PubMedCentralPubMedGoogle Scholar
  58. Karst H, Berger S, Turiault M, Tronche F, Schutz G, Joels M (2005) Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci U S A 102(52):19204–19207PubMedCentralPubMedGoogle Scholar
  59. 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(3):279–286PubMedGoogle Scholar
  60. Kim CH, Lee J, Lee JY, Roche KW (2008) Metabotropic glutamate receptors: phosphorylation and receptor signaling. J Neurosci Res 86(1):1–10PubMedGoogle Scholar
  61. Klink R, Robichaud M, Debonnel G (2002) Gender and gonadal status modulation of dorsal raphe nucleus serotonergic neurons. Part II. Regulatory mechanisms. Neuropharmacology 43(7):1129–1138Google Scholar
  62. Lang T, Jahn R (2008) Core proteins of the secretory machinery. Handb Exp Pharmacol 184:107–127Google Scholar
  63. Lapiz MD, Mateo Y, Durkin S, Parker T, Marsden CA (2001) Effects of central noradrenaline depletion by the selective neurotoxin DSP-4 on the behaviour of the isolated rat in the elevated plus maze and water maze. Psychopharmacology 155(3):251–259PubMedGoogle Scholar
  64. Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, Morrison JH, McEwen BS (2006) Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci: Off J Soc Neurosci 26(30):7870–7874Google Scholar
  65. Lowry CA, Hale MW, Evans AK, Heerkens J, Staub DR, Gasser PJ, Shekhar A (2008) Serotonergic systems, anxiety, and affective disorder: focus on the dorsomedial part of the dorsal raphe nucleus. Ann N Y Acad Sci 1148:86–94PubMedGoogle Scholar
  66. Lowther S, de Paermentier F, Crompton MR, Horton RW (1992) The distribution of 5-HT1D and 5-HT1E binding sites in human brain. Eur J Pharmacol 222(1):137–142PubMedGoogle Scholar
  67. Lupien SJ (2009) Brains under stress. Can J Psychiatry Revue Can Psychiatr 54(1):4–5Google Scholar
  68. Makino S, Smith MA, Gold PW (2002) Regulatory role of glucocorticoids and glucocorticoid receptor mRNA levels on tyrosine hydroxylase gene expression in the locus coeruleus during repeated immobilization stress. Brain Res 943(2):216–223PubMedGoogle Scholar
  69. Marazziti D, Baroni S, Borsini F, Picchetti M, Vatteroni E, Falaschi V, Catena-Dell’Osso M (2013) Serotonin receptors of type 6 (5-HT6): from neuroscience to clinical pharmacology. Curr Med Chem 20(3):371–377PubMedGoogle Scholar
  70. Marchetti E, Dumuis A, Bockaert J, Soumireu-Mourat B, Roman FS (2000) Differential modulation of the 5-HT(4) receptor agonists and antagonist on rat learning and memory. Neuropharmacology 39(11):2017–2027PubMedGoogle Scholar
  71. Marquez C, Poirier GL, Cordero MI, Larsen MH, Groner A, Marquis J, Magistretti PJ, Trono D, Sandi C (2013) Peripuberty stress leads to abnormal aggression, altered amygdala and orbitofrontal reactivity and increased prefrontal MAOA gene expression. Transl Psychiatry 3:e216PubMedCentralPubMedGoogle Scholar
  72. Mason ST, Fibiger HC (1979) Current concepts. I. Anxiety: the locus coeruleus disconnection. Life Sci 25(26):2141–2147PubMedGoogle Scholar
  73. Matsuda LA, Bonner TI, Lolait SJ (1992) Cannabinoid receptors: which cells, where, how, and why? NIDA Res Monogr 126:48–56PubMedGoogle Scholar
  74. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346(6284):561–564PubMedGoogle Scholar
  75. McEwen B (1999) Development of the cerebral cortex: XIII. Stress and brain development: II. J Am Acad Child Adolesc Psychiatry 38(1):101–103PubMedGoogle Scholar
  76. McEwen BS, Gianaros PJ (2011) Stress- and allostasis-induced brain plasticity. Annu Rev Med 62:431–445PubMedCentralPubMedGoogle Scholar
  77. Miederer I, Maus S, Zwiener I, Podoprygorina G, Meshcheryakov D, Lutz B, Schreckenberger M (2013) Evaluation of cannabinoid type 1 receptor expression in the rat brain using [(1)(8)F]MK-9470 microPET. Eur J Nucl Med Mol Imag 40(11):1739–1747Google Scholar
  78. Milad MR, Quirk GJ (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature 420(6911):70–74PubMedGoogle Scholar
  79. Milad MR, Rauch SL, Pitman RK, Quirk GJ (2006) Fear extinction in rats: implications for human brain imaging and anxiety disorders. Biol Psychol 73(1):61–71PubMedGoogle Scholar
  80. Morsink MC, Joels M, Sarabdjitsingh RA, Meijer OC, de Kloet ER, Datson NA (2006) The dynamic pattern of glucocorticoid receptor-mediated transcriptional responses in neuronal PC12 cells. J Neurochem 99(4):1282–1298PubMedGoogle Scholar
  81. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365(6441):61–65PubMedGoogle Scholar
  82. Nagano-Saito A, Dagher A, Booij L, Gravel P, Welfeld K, Casey KF, Leyton M, Benkelfat C (2013) Stress-induced dopamine release in human medial prefrontal cortex–18F-fallypride/PET study in healthy volunteers. Synapse (New York, N.Y.) 67(12):821–830Google Scholar
  83. Niciu MJ, Ionescu DF, Richards EM, Zarate CA Jr (2013) Glutamate and its receptors in the pathophysiology and treatment of major depressive disorder. J Neural Transm. doi: 10.1007/s00702-013-1130-x
  84. Oliver KR, Kinsey AM, Wainwright A, Sirinathsinghji DJ (2000) Localization of 5-ht(5A) receptor-like immunoreactivity in the rat brain. Brain Res 867(1–2):131–142PubMedGoogle Scholar
  85. O’Shea RD (2002) Roles and regulation of glutamate transporters in the central nervous system. Clin Exp Pharmacol Physiol 29(11):1018–1023PubMedGoogle Scholar
  86. Ossewaarde L, Qin S, van Marle HJ, van Wingen GA, Fernandez G, Hermans EJ (2011) Stress-induced reduction in reward-related prefrontal cortex function. NeuroImage 55(1):345–352PubMedGoogle Scholar
  87. Pacak K, Palkovits M (2001) Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr Rev 22(4):502–548PubMedGoogle Scholar
  88. Pascucci T, Andolina D, Mela IL, Conversi D, Latagliata C, Ventura R, Puglisi-Allegra S, Cabib S (2009) 5-Hydroxytryptophan rescues serotonin response to stress in prefrontal cortex of hyperphenylalaninaemic mice. Int J Neuropsychopharmacol/official scientific journal of the Collegium Internationale Neuropsychopharmacologicum (CINP) 12(8):1067–1079Google Scholar
  89. Pasqualetti M, Ori M, Castagna M, Marazziti D, Cassano GB, Nardi I (1999) Distribution and cellular localization of the serotonin type 2C receptor messenger RNA in human brain. Neuroscience 92(2):601–611PubMedGoogle Scholar
  90. Passerin AM, Cano G, Rabin BS, Delano BA, Napier JL, Sved AF (2000) Role of locus coeruleus in foot shock-evoked Fos expression in rat brain. Neuroscience 101(4):1071–1082PubMedGoogle Scholar
  91. Patel KD, Davison JS, Pittman QJ, Sharkey KA (2010) Cannabinoid CB(2) receptors in health and disease. Curr Med Chem 17(14):1393–1410PubMedGoogle Scholar
  92. Pazos A, Probst A, Palacios JM (1987a) Serotonin receptors in the human brain—III. Autoradiographic mapping of serotonin-1 receptors. Neuroscience 21(1):97–122PubMedGoogle Scholar
  93. Pazos A, Probst A, Palacios JM (1987b) Serotonin receptors in the human brain—IV. Autoradiographic mapping of serotonin-2 receptors. Neuroscience 21(1):123–139PubMedGoogle Scholar
  94. Pecoraro N, Dallman MF, Warne JP, Ginsberg AB, Laugero KD, la Fleur SE, Houshyar H, Gomez F, Bhargava A, Akana SF (2006) From Malthus to motive: how the HPA axis engineers the phenotype, yoking needs to wants. Prog Neurobiol 79(5–6):247–340PubMedGoogle Scholar
  95. Pertovaara A (2013) The noradrenergic pain regulation system: a potential target for pain therapy. Eur J Pharmacol 716(1–3):2–7PubMedGoogle Scholar
  96. Pertwee RG (2008) Ligands that target cannabinoid receptors in the brain: from THC to anandamide and beyond. Addict Biol 13(2):147–159PubMedGoogle Scholar
  97. Pirnik Z, Mravec B, Kiss A (2004) Fos protein expression in mouse hypothalamic paraventricular (PVN) and supraoptic (SON) nuclei upon osmotic stimulus: colocalization with vasopressin, oxytocin, and tyrosine hydroxylase. Neurochem Int 45(5):597–607PubMedGoogle Scholar
  98. Popoli M, Yan Z, McEwen BS, Sanacora G (2011) The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 13(1):22–37PubMedCentralPubMedGoogle Scholar
  99. Pruessner JC, Champagne F, Meaney MJ, Dagher A (2004) Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. J Neurosci: Off J Soc Neurosci 24(11):2825–2831Google Scholar
  100. Qin S, Hermans EJ, van Marle HJ, Luo J, Fernandez G (2009) Acute psychological stress reduces working memory-related activity in the dorsolateral prefrontal cortex. Biol Psychiatry 66(1):25–32PubMedGoogle Scholar
  101. Rademacher DJ, Meier SE, Shi L, Ho WS, Jarrahian A, Hillard CJ (2008) Effects of acute and repeated restraint stress on endocannabinoid content in the amygdala, ventral striatum, and medial prefrontal cortex in mice. Neuropharmacology 54(1):108–116PubMedGoogle Scholar
  102. Radley JJ, Sawchenko PE (2011) A common substrate for prefrontal and hippocampal inhibition of the neuroendocrine stress response. J Neurosci: Off J Soc Neurosci 31(26):9683–9695Google Scholar
  103. Radley JJ, Williams B, Sawchenko PE (2008) Noradrenergic innervation of the dorsal medial prefrontal cortex modulates hypothalamo-pituitary-adrenal responses to acute emotional stress. J Neurosci: Off J Soc Neurosci 28(22):5806–5816Google Scholar
  104. Rasmussen K, Morilak DA, Jacobs BL (1986a) Single unit activity of locus coeruleus neurons in the freely moving cat. I. During naturalistic behaviors and in response to simple and complex stimuli. Brain Res 371(2):324–334PubMedGoogle Scholar
  105. Rasmussen K, Strecker RE, Jacobs BL (1986b) Single unit response of noradrenergic, serotonergic and dopaminergic neurons in freely moving cats to simple sensory stimuli. Brain Res 369(1–2):336–340PubMedGoogle Scholar
  106. Redmond DE Jr, Huang YH, Snyder DR, Maas JW (1976) Behavioral effects of stimulation of the nucleus locus coeruleus in the stump-tailed monkey Macaca arctoides. Brain Res 116(3):502–510PubMedGoogle Scholar
  107. Reznikov LR, Reagan LP, Fadel JR (2009) Effects of acute and repeated restraint stress on GABA efflux in the rat basolateral and central amygdala. Brain Res 1256:61–68PubMedGoogle Scholar
  108. Ruffolo RR Jr, Hieble JP (1994) Alpha-adrenoceptors. Pharmacol Ther 61(1–2):1–64PubMedGoogle Scholar
  109. Russell GM, Henley DE, Leendertz J, Douthwaite JA, Wood SA, Stevens A, Woltersdorf WW, Peeters BW, Ruigt GS, White A, Veldhuis JD, Lightman SL (2010) Rapid glucocorticoid receptor-mediated inhibition of hypothalamic-pituitary-adrenal ultradian activity in healthy males. J Neurosci: Off J Soc Neurosci 30(17):6106–6115Google Scholar
  110. Sakai K, Crochet S (2001) Differentiation of presumed serotonergic dorsal raphe neurons in relation to behavior and wake-sleep states. Neuroscience 104(4):1141–1155PubMedGoogle Scholar
  111. Samuels ER, Szabadi E (2008) Functional neuroanatomy of the noradrenergic locus coeruleus: its roles in the regulation of arousal and autonomic function part I: principles of functional organisation. Curr Neuropharmacol 6(3):235–253PubMedCentralPubMedGoogle Scholar
  112. Sapolsky RM, Krey LC, McEwen BS, Rainbow TC (1984) Do vasopressin-related peptides induce hippocampal corticosterone receptors? Implications for aging. J Neurosci: Off J Soc Neurosci 4(6):1479–1485Google Scholar
  113. Sara SJ (2009) The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10(3):211–223PubMedGoogle Scholar
  114. Schoofs D, Pabst S, Brand M, Wolf OT (2013) Working memory is differentially affected by stress in men and women. Behav Brain Res 241:144–153PubMedGoogle Scholar
  115. Schultz W (2007) Behavioral dopamine signals. Trends Neurosci 30(5):203–210PubMedGoogle Scholar
  116. Selye H (1936) A syndrome produced by diverse nocuous agents. Nature 138:32Google Scholar
  117. Shors TJ, Weiss C, Thompson RF (1992) Stress-induced facilitation of classical conditioning. Science (New York, N.Y.) 257(5069):537–539Google Scholar
  118. Sinclair D, Purves-Tyson TD, Allen KM, Weickert CS (2014) Impacts of stress and sex hormones on dopamine neurotransmission in the adolescent brain. Psychopharmacology 231(8):1581–1599PubMedCentralPubMedGoogle Scholar
  119. Singewald GM, Rjabokon A, Singewald N, Ebner K (2011) The modulatory role of the lateral septum on neuroendocrine and behavioral stress responses. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 36(4):793–804Google Scholar
  120. Stasi C, Bellini M, Bassotti G, Blandizzi C, Milani S (2014) Serotonin receptors and their role in the pathophysiology and therapy of irritable bowel syndrome. Tech Coloproctol 18(17):613–621Google Scholar
  121. Sudhof TC, Rothman JE (2009) Membrane fusion: grappling with SNARE and SM proteins. Science (New York, N.Y.) 323(5913):474–477Google Scholar
  122. Sugiura T, Kishimoto S, Oka S, Gokoh M (2006) Biochemistry, pharmacology and physiology of 2-arachidonoylglycerol, an endogenous cannabinoid receptor ligand. Prog Lipid Res 45(5):405–446PubMedGoogle Scholar
  123. Sugiura T, Waku K (2000) 2-Arachidonoylglycerol and the cannabinoid receptors. Chem Phys Lipids 108(1–2):89–106PubMedGoogle Scholar
  124. Summers RJ, McMartin LR (1993) Adrenoceptors and their second messenger systems. J Neurochem 60(1):10–23PubMedGoogle Scholar
  125. Taghzouti K, le Moal M, Simon H (1991) Suppression of noradrenergic innervation compensates for behavioral deficits induced by lesion of dopaminergic terminals in the lateral septum. Brain Res 552(1):124–128PubMedGoogle Scholar
  126. Tasker JG, Herman JP (2011) Mechanisms of rapid glucocorticoid feedback inhibition of the hypothalamic-pituitary-adrenal axis. Stress (Amsterdam, Netherlands) 14(4):398–406Google Scholar
  127. Tepper SJ, Rapoport AM, Sheftell FD (2002) Mechanisms of action of the 5-HT1B/1D receptor agonists. Arch Neurol 59(7):1084–1088PubMedGoogle Scholar
  128. Thomas DR, Hagan JJ (2004) 5-HT7 receptors. Curr Drug Targets CNS Neurol Disord 3(1):81–90Google Scholar
  129. Thompson AJ, Lummis SC (2007) The 5-HT3 receptor as a therapeutic target. Expert Opin Ther Targets 11(4):527–540PubMedCentralPubMedGoogle Scholar
  130. Ueda N, Katayama K, Goparaju SK, Kurahashi Y, Yamanaka K, Suzuki H, Yamamoto S (2002) Catalytic properties of purified recombinant anandamide amidohydrolase. Adv Exp Med Biol 507:251–256PubMedGoogle Scholar
  131. Ulrich-Lai YM, Herman JP (2009) Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 10(6):397–409PubMedCentralPubMedGoogle Scholar
  132. Uriguen L, Perez-Rial S, Ledent C, Palomo T, Manzanares J (2004) Impaired action of anxiolytic drugs in mice deficient in cannabinoid CB1 receptors. Neuropharmacology 46(7):966–973PubMedGoogle Scholar
  133. Vallone D, Picetti R, Borrelli E (2000) Structure and function of dopamine receptors. Neurosci Biobehav Rev 24(1):125–132PubMedGoogle Scholar
  134. van Sickle MD, Duncan M, Kingsley PJ, Mouihate A, Urbani P, Mackie K, Stella N, Makriyannis A, Piomelli D, Davison JS, Marnett LJ, di Marzo V, Pittman QJ, Patel KD, Sharkey KA (2005) Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science (New York, N.Y.) 310(5746):329–332Google Scholar
  135. Varnas K, Halldin C, Hall H (2004) Autoradiographic distribution of serotonin transporters and receptor subtypes in human brain. Hum Brain Mapp 22(3):246–260PubMedGoogle Scholar
  136. Wade MR, Degroot A, Nomikos GG (2006) Cannabinoid CB1 receptor antagonism modulates plasma corticosterone in rodents. Eur J Pharmacol 551(1–3):162–167PubMedGoogle Scholar
  137. Wand GS, Oswald LM, McCaul ME, Wong DF, Johnson E, Zhou Y, Kuwabara H, Kumar A (2007) Association of amphetamine-induced striatal dopamine release and cortisol responses to psychological stress. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 32(11):2310–2320Google Scholar
  138. Watt MJ, Burke AR, Renner KJ, Forster GL (2009) Adolescent male rats exposed to social defeat exhibit altered anxiety behavior and limbic monoamines as adults. Behav Neurosci 123(3):564–576PubMedCentralPubMedGoogle Scholar
  139. Wellman CL, Izquierdo A, Garrett JE, Martin KP, Carroll J, Millstein R, Lesch KP, Murphy DL, Holmes A (2007) Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci: Off J Soc Neurosci 27(3):684–691Google Scholar
  140. Wilson RI, Nicoll RA (2002) Endocannabinoid signaling in the brain. Science (New York, N.Y.) 296(5568):678–682Google Scholar
  141. Xi ZX, Peng XQ, Li X, Song R, Zhang HY, Liu QR, Yang HJ, Bi GH, Li J, Gardner EL (2011) Brain cannabinoid CB(2) receptors modulate cocaine’s actions in mice. Nat Neurosci 14(9):1160–1166PubMedCentralPubMedGoogle Scholar
  142. Yuen EY, Liu W, Karatsoreos IN, Feng J, McEwen BS, Yan Z (2009) Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proc Natl Acad Sci U S A 106(33):14075–14079PubMedCentralPubMedGoogle Scholar
  143. Ziegler DR, Cass WA, Herman JP (1999) Excitatory influence of the locus coeruleus in hypothalamic-pituitary-adrenocortical axis responses to stress. J Neuroendocrinol 11(5):361–369PubMedGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Department of Family and Community Health Systems, School of NursingUniversity of Texas Health Science Center at San AntonioSan AntonioUSA

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