Strain-Dependent variations in stress coping behavior are mediated by a 5-HT/GABA Interaction within the prefrontal corticolimbic system

International Journal of Neuropsychopharmacology

Volumn 18, Issue 3, 2015, Pages

  Andolina, Diego ^a,b   Maran, Dario ^c   Viscomi, Maria Teresa ^a   Puglisi Allegra, Stefano ^a,c  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY OF L'AQUILA   (Italy)

^c SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Basolateral amygdala; GABA; Medial prefrontal cortex; Serotonin; Strain

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; NEUROTRANSMITTER; SEROTONIN; SEROTONIN 1A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; 5,6 DIHYDROXYTRYPTAMINE; DOPAMINE; SEROTONIN RECEPTOR; SEROTONIN RECEPTOR AFFECTING AGENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BASOLATERAL AMYGDALA; C57BL 6 MOUSE; CONTROLLED STUDY; COPING BEHAVIOR; DBA 2 MOUSE; ELEVATED PLUS MAZE TEST; FORCED SWIM TEST; IMMOBILITY; IMMOBILIZATION STRESS; IMMUNOHISTOCHEMISTRY; INBRED MOUSE STRAIN; INFRALIMBIC CORTEX; LIMBIC SYSTEM; LOCOMOTION; MALE; MEDIAL PREFRONTAL CORTEX; MICRODIALYSIS; MOUSE; NEUROCHEMISTRY; NONHUMAN; PRELIMBIC CORTEX; PRIORITY JOURNAL; SEROTONIN RELEASE; SEROTONINERGIC TRANSMISSION; STRAIN DIFFERENCE; ADAPTIVE BEHAVIOR; ANIMAL; C57BL MOUSE; DBA MOUSE; GENETICS; MAZE TEST; MENTAL STRESS; METABOLISM; MOTOR ACTIVITY; PATHOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; PSYCHOLOGY; SPECIES DIFFERENCE;

5,6-DIHYDROXYTRYPTAMINE; ADAPTATION, PSYCHOLOGICAL; ANIMALS; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; LIMBIC SYSTEM; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICRODIALYSIS; MOTOR ACTIVITY; PREFRONTAL CORTEX; RECEPTORS, GABA-B; RECEPTORS, SEROTONIN; SEROTONIN; SEROTONIN AGENTS; SPECIES SPECIFICITY; STRESS, PSYCHOLOGICAL;

EID: 85005914676     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyu074     Document Type: Article

References (84)

1. Ago Y, Koyama Y, Baba A, Matsuda T (2003) Regulation by 5-HT1A receptors of the in vivo release of 5-HT and DA in mouse frontal cortex. Neuropharmacology 45:1050-1056.
2. Akirav I, Maroun M (2007) The role of the medial prefrontal cortex- Amygdala circuit in stress effects on the extinction of fear. Neural Plast 2007:30873.
3. Albert PR, Zhou QY, Van Tol HH, Bunzow JR, Civelli O (1990) Cloning, functional expression, and mRNA tissue distribution of the rat 5-hydroxytryptamine1A receptor gene. J Biol Chem 265:5825-5832.
4. Alcaro A, Cabib S, Ventura R, Puglisi-Allegra S (2002) Genotype and experience dependent susceptibility to depressive-like responses in the forced-swimming test. Psychopharmacology (Berl) 164:138-143.
5. Amat J, Matus-Amat P, Watkins LR, Maier SF (1998) Escapable and inescapable stress differentially alter extracellular levels of 5-HT in the basolateral amygdala of the rat. Brain Res 812:113-120.
6. Amat J, Baratta MV, Paul E, Bland ST, Watkins LR Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365-371.
7. Andolina D, Maran D, Valzania A, Conversi D Puglisi-Allegra S (2013) Prefrontal/amygdalar system determines stress coping behavior through 5-HT/GABA connection. Neuropsychopharmacology 38:2057-2067.
8. Beique JC, Campbell B, Perring P, Walker P, Mladenovic L Andrade R (2004) Serotonergic regulation of membrane potential in developing rat prefrontal cortex: coordinated expression of 5-hydroxytryptamine (5-HT)1A, 5-HT2A, and 5- HT7 receptors. J Neurosci 24:4807-4817.
9. Berger SM, Weber T, Perreau-Lenz S, Vogt MA, Gartside SE, Maser- Gluth C, Lanfumey L, Gass P, Spanagel R, Bartsch D (2012). A functional Tph2 C1473G polymorphism causes an anxiety phenotype via compensatory changes in the serotonergic system. Neuropsychopharmacology 37:1986-1998.
10. Blier P, de Montigny C (1990) Electrophysiological investigation of the adaptiveresponse of the 5-HT system to the administration of 5-HT1A receptor agonists. J Cardiovasc Pharmacol 15:S42-S48.
11. Bolser DC, Blythin DJ, Chapman RW, Egan RW, Hey JA, Rizzo C, Kuo SC, Kreutner W (1995) The pharmacology of SCH 50911: A novel, orally active GABA-B receptor antagonist. J Pharmacol Exp Ther. 274:1393-1398.
12. Brambilla P, Harenski K, Nicoletti M, Sassi RB, Mallinger AG, Frank E, Kupfer DJ, Keshavan MS, Soares JC (2003) MRI investigation of temporal lobe structures in bipolar patients. J Psychiatr Res 37:287-295.
13. Cabib S, Ventura R, Puglisi-Allegra S (2002) Opposite imbalances between mesocortical and mesoaccumbens dopamine responses to stress by the same genotype depending on living conditions. Behav Brain Res 129:179-185.
14. Cabib S, Pascucci T, Ventura R, Romano V, Puglisi-Allegra S (2003) The behavioral profile of severe mental retardation in a genetic mouse model of phenylketonuria. Behav Genet 33:301-310.
15. Cabib S, Puglisi-Allegra S (1991) Genotype-dependent effects of chronic stress on apomorphine-induced alterations of striatal and mesolimbic dopamine metabolism. Brain Res 542:91-96.
16. Cabib S, Puglisi-Allegra S (1996) Stress, depression and the mesolimbic dopamine system. Psychopharmacology (Berl) 128:331-342.
17. Calcagno E, Canetta A, Guzzetti S, Cervo L Invernizzi RW (2007) Strain differences in basal and post-citalopram extracellular 5-HT in the mouse medial prefrontal cortex and dorsal hippocampus: Relation with tryptophan hydroxylase-2 activity. J Neurochem 103:1111-1120.
18. Canli T, Omura K, Haas BW, Fallgatter A, Constable RT, Lesch KP (2005) Beyond affect: A role for genetic variation of the serotonin transporter in neural activation during a cognitive attention task. Proc Natl Acad Sci USA 102:12224-12229.
19. Car H, Wisniewska RJ (2006) Antidepressant-like effects of baclofen and LY367385 in the forced swim test in rats. Pharmacol Rep 58:758-764.
20. Cervo L, Canetta A, Calcagno E, Burbassi S, Sacchetti G, Caccia S, Fracasso C, Albani D, Forloni G, Invernizzi RW (2005) Genotype-dependent activity of tryptophan hydroxylase-2 determines the response to citalopram in a mouse model of depression. J Neurosci 25:8165-8172.
21. Chessell IP, Francis PT, Pangalos MN, Pearson RC, Bowen DM (1993) Localisation of muscarinic (m1) and other neurotransmitter receptors on corticofugal-projecting pyramidal neurones. Brain Res 632:86-94.
22. Cousins MS, Seiden LS (2000) The serotonin-1A receptor antagonist WAY-100635 modifies fluoxetine's antidepressant-like profile on the differential reinforcement of low rates 72-s schedule in rats. Psychopharmacology (Berl) 148:438-442.
23. Cryan JF, Kaupmann K (2005) Don't worry 'B' happy!: A role for GABA(B) receptors in anxiety and depression. Trends Pharmacol Sci. 26:36-43.
24. Drevets WC, Videen TO, Price JL, Preskorn SH, Carmichael ST, Raichle ME (1992) A functional anatomical study of unipolar depression. J Neurosci. 12:3628-3641.
25. DuBois DW, Perlegas A, Floyd DW, Weiner JL, McCool BA (2006) Distinct functional characteristics of the lateral/basolateral amygdala GABAergic system in C57BL/6J and DBA/2J mice. J Pharmacol Exp Ther 318:629-640.
26. Ebner K, Bosch JO, Kromer SA, Singewald N, Neumann ID (2005) Release of oxytocin in the rat central amygdala modulates stress coping behavior and the release of excitator amino acids. Neuropsychopharmacology 30:223-230.
27. Etkin A, Klemenhagen KC, Dudman JT, Rogan MT, Hen R, Kandel ER, Hirsch J (2004) Individual differences in trait anxiety predict the response of the basolateral amygdala to unconsciously processed fearful faces. Neuron 44:1043-1055.
28. Fakra E, Hyde LW, Gorka A, Fisher PM, Munoz KE, Kimak M, Halder I, Ferrell RE, Manuck SB, Hariri AR (2009) Effects of HTR1A C(-1019)G on amygdala reactivity and trait anxiety. Arch Gen Psychiatry 66:33-40.
29. Firk C, Markus CR (2007) Review: Serotonin by stress interaction: A susceptibility factor for the development of depression? J Psychopharmacol 21:538-544.
30. Fisher PM, Meltzer CC, Price JC, Coleman RL, Ziolko SK, Becker C, Moses-Kolko EL, Berga SL Hariri AR (2009) Medial prefrontal cortex 5-HT(2A) density is correlated with amygdala reactivity, response habituation, and functional coupling. Cereb Cortex 19:2499-2507.
31. Fisher PM, Price JC, Meltzer CC, Moses-Kolko EL, Becker C, Berga SL, Hariri AR (2011) Medial prefrontal cortex serotonin 1A and 2A receptor binding interacts to predict threatrelated amygdala reactivity. Biol Mood Anxiety Disord 1:2.
32. Franklin KBJ, Paxinos G (1997) The Mouse Brain: In Stereotaxic Coordinates (Academic, San Diego).
33. Frankowska M, Filip M, Przegalinski E (2007) Effects of GABAB receptor ligands in animal tests of depression and anxiety. Pharmacol Rep 59:645-655.
34. Goodfellow NM, Benekareddy M, Vaidya VA, Lambe EK (2009) Layer II/III of the prefrontal cortex: inhibition by the serotonin 5-HT1A receptor in development and stress. J Neurosci 29:10094-10103.
35. Hall FS, Devries AC, Fong GW, Huang S, Pert A (1999) Effects of 5, 7-dihydroxytryptamine depletion of tissue serotonin levels on extracellular serotonin in the striatum assessed with in vivo microdialysis: Relationship to behavior. Synapse 33:16-25.
36. Hariri AR, Mattay VS, Tessitore A, Kolachana B, Fera F, Goldman D, Egan MF, Weinberger DR (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297:400-403.
37. Heinz A, Braus DF, Smolka MN, Wrase J, Puls I, Hermann D, Klein S, Grusser SM, Flor H, Schumann G, Mann K, Buchel C (2005) Amygdala-prefrontal coupling depends on a genetic variation of the serotonin transporter. Nat Neurosci 8:20-21.
38. Heisler LK, Chu HM, Brennan TJ, Danao JA, Bajwa P, Parsons LH, Tecott LH (1998) Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc Natl Acad Sci USA 95:15049-15054.
39. Holmes A (2009) Genetic variation in cortico- Amygdala serotonin function and risk for stressrelated disease. Neurosci Biobehav Rev 32:1293-1314.
40. Homberg JR (2012) The stress-coping (mis)match hypothesis for nature x nurture interactions. Brain Res 1432:114-121.
41. Kirby LG, Kreiss DS, Singh A, Lucki I (1995) Effect of destruction of serotonin neurons on basal and fenfluramine-induced serotonin release in striatum. Synapse 20:99-105.
42. Krystal JH, Sanacora G, Blumberg H, Anand A, Charney DS, Marek G, Epperson CN, Goddard A, Mason GF (2002) Glutamate and GABA systems as targets for novel antidepressant and mood stabilizing treatments. Mol Psychiatry 1:S71-S80.
43. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155-184.
44. Lehner M, Taracha E, Skorzewska A, Maciejak P, Wislowska- Stanek A, Zienowicz M, Szyndler J, Bidzinski A, Płaznik A (2006) Behavioral, immunocytochemical and biochemical studies in rats differing in their sensitivity to pain. Behav Brain Res 171:189-198.
45. Likhtik E, Pelletier JG, Paz R, Pare D (2005) Prefrontal control of the amygdala. J Neurosci 25:7429-7437.
46. Lloyd KG, Thuret F, Pilc A (1985) Upregulation of gamma- Aminobutyric acid (GABA) B binding sites in rat frontal cortex: A common action of repeated administration of different classes of antidepressants and electroshock. J Pharmacol Exp Ther 235:191-199.
47. Lucki I, Dalvi A, Mayorga AJ (2001) Sensitivity to the effects of pharmacologically selective antidepressants in different strains of mice. Psychopharmacology (Berl) 155:315-322.
48. Maier SF, Watkins LR (2010) Role of the medial prefrontal cortex in coping and resilience. Brain Res 1355:52-60.
49. Martin-Ruiz R, Puig MV, Celada P, Shapiro DA, Roth BL, Mengod G, Artigas F (2001) Control of serotonergic function in medial prefrontal cortex by serotonin-2A receptors through a glutamatedependent mechanism. J Neurosci 21:9856-9866.
50. Mathews TA, Fedele DE, Coppelli FM, Avila AM, Murphy DL, Andrews AM (2004) Gene dose-dependent alterations in extraneuronal serotonin but not dopamine in mice with reduced serotonin transporter expression. J Neurosci Methods 140:169-181.
51. McDonald AJ, Mascagni F, Muller JF (2004) Immunocytochemical localization of GABABR1 receptor subunits in the basolateral amygdala. Brain Res 1018:147-158.
52. Mozhui K, Karlsson RM, Kash TL, Ihne J, Norcross M, Patel S, Farrell MR, Hill EE, Graybeal C, Martin KP, Camp M, Fitzgerald PJ, Ciobanu DC, Sprengel R, Mishina M, Wellman CL, Winder DG, Williams RW, Holmes A (2010) Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 30:5357-5367.
53. Pascucci T, Andolina D, La Mela I, 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 14:479-489.
54. Pezawas L, Meyer-Lindenberg A, Drabant EM, Verchinski BA, Munoz KE, Kolachana BS, Egan MF, Mattay VS, Hariri AR, Weinberger DR (2005) 5-HTTLPR polymorphism impacts human cingulate- Amygdala interactions: A genetic susceptibility mechanism for depression. Nat Neurosci 8:828-834.
55. Phelps EA, Delgado MR, Nearing KI, LeDoux JE (2004) Extinction learning in humans: Role of the amygdala and vmPFC. Neuron 43:897-905.
56. Phillips ML, Drevets WC, Rauch SL, Lane R (2003) Neurobiology of emotion perception II: implications for major psychiatric disorders. Biol Psychiatry 54:515-528.
57. Pilc A, Lloyd KG (1984) Chronic antidepressants and GABA "B" receptors: A GABA hypothesis of antidepressant drug action. Life Sci 35:2149-2154.
58. Pompeiano M, Palacios JM, Mengod G (1992) Distribution and cellular localization of mRNA coding for 5-HT1A receptor in the rat brain: correlation with receptor binding. J Neurosci 12:440-453.
59. Popova NK, Naumenko VS, Tibeikina MA, Kulikov AV (2009) Serotonin transporter, 5-HT1A receptor, and behavior in DBA/2J mice incomparison with four inbred mouse strains. J Neurosci Res 87:3649-3657.
60. Puig MV, Gulledge AT (2011) Serotonin and prefrontal cortex function: neurons, networks, and circuits. Mol Neurobiol 44:449-464.
61. Puglisi-Allegra S, Cabib S, Pascucci T, Ventura R, Cali F, Romano V (2000) Dramatic brain aminergic deficits in a genetic mouse model of phenyketonuria. Neuroreport 11:1361-1364.
62. Qi X, Lin W, Li J, Li H, Wang W, Wang D, Sun M (2008) Fluoxetine increases the activity of the ERK-CREB signal system and alleviates the depressive-like behavior in rats exposed to chronic forced swim stress. Neurobiol Dis 31:278-285.
63. Quirk GJ, Likhtik E, Pelletier JG, Pare D (2003) Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 23:8800-8807.
64. Rainnie DG (1999) Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82:69-85.
65. Rea K, Cremers TI, Westerink BH (2005) HPLC conditions are critical for the detection of GABA by microdialysis. J Neurochem 94:672-679.
66. 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 1256:61-68.
67. Shin LM, Liberzon I (2010) The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology. 35:169-191.
68. Shin LM, Wright CI, Cannistraro PA, Wedig MM, McMullin K, Martis B, Macklin ML, Lasko NB, Cavanagh SR, Krangel TS, Orr SP, Pitman RK, Whalen PJ, Rauch SL (2005) A functional magnetic resonance imaging study of amygdala and medial prefrontal cortex responses to overtly presented fearful faces in posttraumatic stress disorder. Arch Gen Psychiatry 62:273-281.
69. Shishkina GT, Kalinina TS, Dygalo NN (2012) Effects of swim stress and fluoxetine on 5-HT1A receptor gene expression and monoamine metabolism in the rat brain regions. Cell Mol Neurobiol 32:787-794.
70. Siegle GJ, Steinhauer SR, Thase ME, Stenger VA, Carter CS (2002) Can't shake that feeling: Event-related fMRI assessment of sustained amygdala activity in response to emotional information in depressed individuals. Biol Psychiatry 51:693-707.
71. Slattery DA, Desrayaud S, and Cryan JF (2005) GABAB receptor antagonist-mediated antidepressant-like behavior is serotonin- dependent. J Pharmacol Exp Ther 312:290-296.
72. Sprouse JS, Aghajanian GK (1988) Responses of hippocampal pyramidal cells to putative serotonin 5-HT1A and 5-HT1B agonists: A comparative study with dorsal raphe neurons. Neuropharmacology 27:707-715.
73. Sugimoto Y, Kajiwara Y, Hirano K, Yamada S, Tagawa N, Kobayashi Y, Hotta Y, Yamada J (2008) Mouse strain differences in immobility and sensitivity to fluvoxamine and desipramine in the forced swimming test: Analysis of serotonin and noradrenaline transporter binding. Eur J Pharmacol 592: 116-122.
74. Tanaka E, North RA (1993) Actions of 5-hydroxytryptamine on neurons of the rat cingulate cortex. J Neurophysiol 69:1749-1757.
75. Ventura R, Cabib S, Puglisi-Allegra S (2002) Genetic susceptibility of mesocortical dopamine to stress determines liability to inhibition of mesoaccumbens dopamine and to behavioral 'despair' in a mouse model of depression. Neuroscience 115:999-1007.
76. Ventura R, Morrone C, Puglisi-Allegra S (2007) Prefrontal/accumbal catecholamine system determines motivational salience attribution to both reward- And aversion-related stimuli. Proc Natl Acad Sci USA 104:5181-5186.
77. Voikar V, Polus A, Vasar E, Rauvala H (2005) Long-term individual housing in C57BL/6J and DBA/2 mice: Assessment of behavioral consequences. Genes Brain Behav 4:240-252.
78. Yang RJ, Mozhui K, Karlsson RM, Cameron HA, Williams RW, Holmes A (2008) Variation in mouse basolateral amygdala volume is associated with differences in stress reactivity and fear learning. Neuropsychopharmacology 33:2595-2604.
79. Waddell J, Dunnett C, Falls WA (2004) C57BL/6J and DBA/2J mice differ in extinction and renewal of extinguished conditioned fear. Behav Brain Res 154:567-576.
80. Wedzony K, Chocyk A, Kolasiewicz W, Mackowiak M (2007) Glutamatergic neurons of rat medial prefrontal cortex innervating the ventral tegmental area are positive for serotonin 5- HT1A receptor protein. J Physiol Pharmacol 58:611-624.
81. Wellman CL, Izquierdo A, Garrett JE, Martin KP, Carroll J, Millstein R, Lesch KP, Murphy DL, Holmes A (2007). Impaired stresscoping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knock-out mice. J Neurosci. 27:684-691.
82. Zhang X, Beaulieu JM, Sotnikova TD, Gainetdinov RR, Caron MG (2004) Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science 305:217.
83. Zhang ZW, Arsenault D (2005) Gain modulation by serotonin in pyramidal neurones of the rat prefrontal cortex. J Physiol 566:379-394.
84. Zhong P, Yan Z (2011) Differential regulation of the excitability of prefrontal cortical fastspiking interneurons and pyramidal neurons by serotonin and fluoxetine. PLoS One 6:e16970.