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Seasonal effects of the monoamine oxidase inhibitor deprenyl but not the tricyclic antidepressant imipramine in rats bred for helplessness

Year 2016, , 312 - 6, 15.08.2016
https://doi.org/10.17546/msd.19700

Abstract

Objective:  Seasonal variations in monoaminergic function may underlie seasonal affective disorder, a subtype of major depression.  Here, we examined whether antidepressant drugs which regulate monoaminergic function exhibit seasonal effects in an animal model of depression, congenital helplessness.

Material and Method:  Rats selectively bred for helplessness were required to press a lever to turn off a foot-shock before and after chronic treatment with the tricyclic antidepressant imipramine (10 mg/kg) or the monoamine oxidase inhibitor deprenyl (10 mg/kg).  Control rats received saline.  Different groups of rats were tested in summer-fall and spring over the course of two years.

Results: Congenitally helpless (cH) rats that were treated with imipramine pressed the lever more often than controls in fall and in spring, indicative of antidepressant effects regardless of season.  By contrast, cH rats treated with deprenyl pressed the lever more often in summer-fall than in spring, suggestive of seasonal drug effects on helplessness behavior.  Deprenyl significantly attenuated the lever-pressing deficit in both seasons when compared to saline controls.  Moreover, cH rats treated with deprenyl but not imipramine increased the number of lever presses over trials, indicative of negative reinforcement learning.

Conclusion: The present data are the first to show seasonal variations in antidepressant drug effects that are possibly linked to changes in dopamine neurotransmission.  The data support the view that we must take seasonality into account when evaluating the efficacy of antidepressant compounds.

 

References

  • Otsuka T, Kawai M, Togo Y, Goda R, Kawase T, Matsuo H, et al. Photoperiodic responses of depression-like behavior, the brain serotonergic system, and peripheral metabolism in laboratory mice. Psychoneuroendocrinology. 2014;40:37-47.
  • Aksoy A, Schulz D, Yilmaz A, Canbeyli R. Seasonal variability in behavioral despair in female rats. Intern J Neuroscience. 2004;114:1513-20.
  • Neumeister A, Konstantinidis A, Praschak-Rieder N, Willeit M, Hilger E, Stastny J, et al. Monoaminergic function in the pathogenesis of seasonal affective disorder. Int J Neuropsychopharmacology. 2001;4:409-20.
  • Levitan RD. The chronobiology and neurobiology of winter seasonal affective disorder. Dialogues Clin Neurosci. 2007;9:315-24.
  • Neumeister A, Pirker W, Willeit M, Praschak-Rieder N, Asenbaum S, Brücke T, et al. Seasonal variation of availability of serotonin transporter binding sites in healthy female subjects as measured by [123I]-2 beta-carbomethoxy-3 beta-(4-iodophenyl)tropane and single photon emission computed tomography. Biol Psychiatry. 2000;47:158-60.
  • Praschak-Rieder N, Willeit M, Wilson AA, Houle S, Meyer JH. Seasonal variation in human brain serotonin transporter binding. Arch Gen Psychiatry. 2008;65:1072-8.
  • Willeit M, Praschak-Rieder N, Neumeister A, Pirker W, Asenbaum S, Vitouch O, et al. [123I]-beta-CIT SPECT imaging shows reduced brain serotonin transporter availability in drug-free depressed patients with seasonal affective disorder. Biol Psychiatry. 2000;47:482-9.
  • Neumeister A, Willeit M, Praschak-Rieder N, Asenbaum S, Stastny J, Hilger E, et al. Dopamine transporter availability in symptomatic depressed patients with seasonal affective disorder and healthy controls. Psychol Med. 2001;31:1467-73.
  • Goda R, Otsuka T, Iwamoto A, Kawai M, Shibata S, Furuse M, et al. Serotonin levels in the dorsal raphe nuclei of both chipmunks and mice are enhanced by long photoperiod, but brain dopamine level response to photoperiod is species-specific. Neurosci Lett. 2015:593:95-100.
  • Gonzalez MM, Aston-Jones G. Light deprivation damages monoamine neurons and produces a depressive phenotype in rats. Proc Natl Acad Sci. 2008;105:4898-903.
  • Henn FA, Vollmayr B. Stress models of depression: forming genetically vulnerable strains. Neurosci Biobehav Rev. 2005;29:799-804.
  • Schulz D, Mirrione MM, Henn FA. Cognitive aspects of congenital learned helplessness and its reversal by the monoamine oxidase (MAO)-B inhibitor deprenyl. Neurobiol Learn Mem. 2010;93:291-301.
  • Schulz D, Smith D, Yu M, Henn FA. Selective breeding for helplessness in rats alters the metabolic profile of the hippocampus and frontal cortex: a 1H-MRS study at 9.4 T. Int J Neuropsychopharmacol. 2013;16:199-212.
  • Schulz D, Henn FA, Petri D, Huston JP. Rats bred for helplessness exhibit positive reinforcement learning deficits which are not alleviated by an antidepressant dose of the MAO-B inhibitor deprenyl. Neuroscience. 2016;329:83-92.
  • Knoll J, Miklya I. Enhanced catecholaminergic and serotoninergic activity in rat brain from weaning to sexual maturity: rationale for prophylactic (-)deprenyl (selegiline) medication. Life Sci. 1995;56:611-20.
  • Lamensdorf I, Youdim MB, Finberg JP. Effect of long-term treatment with selective monoamine oxidase A and B inhibitors on dopamine release from rat striatum in vivo. J Neurochem. 1996;67:1532-9.
  • Sunderland T, Mueller EA, Cohen RM, Jimerson DC, Pickar D, Murphy DL. Tyramine pressor sensitivity changes during deprenyl treatment. Psychopharmacol. 1985;86:432-7.
  • Fowler JS, Logan J, Volkow ND, Shumay E, McCall-Perez F, Jayne M, et al. Evidence that formulations of the selective MAO-B inhibitor, selegiline, which bypass first-pass metabolism, also inhibit MAO-A in the human brain. Neuropsychopharmacology. 2015;40:650-7.
  • Vollmayr B, Henn FA. Learned helplessness in the rat: improvements in validity and reliability. Brain Res Brain Res Protoc. 2001;8:1-7.
  • Carlsson A, Svennerholm L, Winblad B. Seasonal and circadian monoamine variations in human brains examined post mortem. Acta Psychiatr Scand Suppl. 1980; 280:75-85.
  • Whitaker PM, Warsh JJ, Stancer HC, Persad E, Vint CK. Seasonal variation in platelet 3H-imipramine binding: comparable values in control and depressed populations. Psychiatry Res. 1984;11:127-31.
  • Arora RC, Meltzer HY. Seasonal variation of imipramine binding in the blood platelets of normal controls and depressed patients. Biol Psychiatry. 1988;23:217-26.
  • DeMet EM, Chicz-DeMet A, Fleischmann J. Seasonal rhythm of platelet 3H-imipramine binding in normal controls. Biol Psychiatry. 1989;26:489-95.
  • Cappiello A, Malison RT, McDougle CJ, Vegso SJ, Charney DS, Heninger GR, et al. Seasonal variation in neuroendocrine and mood responses to IV L-tryptophan in depressed patients and healthy subjects. Neuropsychopharmacology. 1996;15:475-83.
  • Joseph-Vanderpool JR, Jacobsen FM, Murphy DL, Hill JL, Rosenthal NE. Seasonal variation in behavioural responses to m-CPP in patients with seasonal affective disorder and controls. Biol Psychiatry. 1993;33:496-504.
  • Oren DA, Moul DE, Schwartz PJ, Wehr TA, Rosenthal NE. A controlled trial of levodopa plus carbidopa in the treatment of winter seasonal affective disorder: a test of the dopamine hypothesis. J Clin Psychopharmacol. 1994;14:196-200.
  • Eisenberg DP, Kohn PD, Baller EB, Bronstein JA, Masdeu JC, Berman KF. Seasonal effects on human striatal presynaptic dopamine synthesis. J Neurosci. 2010;30:14691-4.
  • Naber D, Wirz-Justice A, Kafka MS, Tobler I, Borbely AA. Seasonal variations in the endogenous rhythm of dopamine receptor binding in the rat striatum. Biol Psychiatry. 1981;16:831-5.
  • Imbesi M, Yildiz S, Arslan AD, Sharma R, Manev H, Uz T. Dopamine receptor-mediated regulation of neuronal “clock” gene expression. Neuroscience. 2009;158:537-44.
  • Reichborn-Kjennerud T, Lingjaerde O, Oreland L. Platelet monoamine oxidase activity in patients with winter seasonal affective disorder. Psychiatry Res. 1996;62:273-80.
  • Chevillard C, Barden N, Saavedra JM. Twenty-four hour rhythm in monoamine oxidase activity in specific areas of the rat brain stem. Brain Res. 1981;223:205-9.
  • Hampp G, Ripperger JA, Houben T, Schmutz I, Blex C, Perreau-Lenz S, et al. Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr Biol. 2008;18:678-83.
  • Huston JP, Mueller CC, Mondadori C. Memory facilitation by posttrial hypothalamic stimulation and other reinforcers: a central theory of reinforcement. Biobehav Rev. 1977;1:143-50.
  • Huston JP, Oitzl M-S. The relationship between reinforcement and memory: parallels in the rewarding and mnemonic effects of the neuropeptide substance P. Neurosci Biobehav Rev. 1989;13:171-80.
  • White NM. Addictive drugs as reinforcers: Multiple partial actions on memory systems. Addiction. 1996;91:921-49.
Year 2016, , 312 - 6, 15.08.2016
https://doi.org/10.17546/msd.19700

Abstract

References

  • Otsuka T, Kawai M, Togo Y, Goda R, Kawase T, Matsuo H, et al. Photoperiodic responses of depression-like behavior, the brain serotonergic system, and peripheral metabolism in laboratory mice. Psychoneuroendocrinology. 2014;40:37-47.
  • Aksoy A, Schulz D, Yilmaz A, Canbeyli R. Seasonal variability in behavioral despair in female rats. Intern J Neuroscience. 2004;114:1513-20.
  • Neumeister A, Konstantinidis A, Praschak-Rieder N, Willeit M, Hilger E, Stastny J, et al. Monoaminergic function in the pathogenesis of seasonal affective disorder. Int J Neuropsychopharmacology. 2001;4:409-20.
  • Levitan RD. The chronobiology and neurobiology of winter seasonal affective disorder. Dialogues Clin Neurosci. 2007;9:315-24.
  • Neumeister A, Pirker W, Willeit M, Praschak-Rieder N, Asenbaum S, Brücke T, et al. Seasonal variation of availability of serotonin transporter binding sites in healthy female subjects as measured by [123I]-2 beta-carbomethoxy-3 beta-(4-iodophenyl)tropane and single photon emission computed tomography. Biol Psychiatry. 2000;47:158-60.
  • Praschak-Rieder N, Willeit M, Wilson AA, Houle S, Meyer JH. Seasonal variation in human brain serotonin transporter binding. Arch Gen Psychiatry. 2008;65:1072-8.
  • Willeit M, Praschak-Rieder N, Neumeister A, Pirker W, Asenbaum S, Vitouch O, et al. [123I]-beta-CIT SPECT imaging shows reduced brain serotonin transporter availability in drug-free depressed patients with seasonal affective disorder. Biol Psychiatry. 2000;47:482-9.
  • Neumeister A, Willeit M, Praschak-Rieder N, Asenbaum S, Stastny J, Hilger E, et al. Dopamine transporter availability in symptomatic depressed patients with seasonal affective disorder and healthy controls. Psychol Med. 2001;31:1467-73.
  • Goda R, Otsuka T, Iwamoto A, Kawai M, Shibata S, Furuse M, et al. Serotonin levels in the dorsal raphe nuclei of both chipmunks and mice are enhanced by long photoperiod, but brain dopamine level response to photoperiod is species-specific. Neurosci Lett. 2015:593:95-100.
  • Gonzalez MM, Aston-Jones G. Light deprivation damages monoamine neurons and produces a depressive phenotype in rats. Proc Natl Acad Sci. 2008;105:4898-903.
  • Henn FA, Vollmayr B. Stress models of depression: forming genetically vulnerable strains. Neurosci Biobehav Rev. 2005;29:799-804.
  • Schulz D, Mirrione MM, Henn FA. Cognitive aspects of congenital learned helplessness and its reversal by the monoamine oxidase (MAO)-B inhibitor deprenyl. Neurobiol Learn Mem. 2010;93:291-301.
  • Schulz D, Smith D, Yu M, Henn FA. Selective breeding for helplessness in rats alters the metabolic profile of the hippocampus and frontal cortex: a 1H-MRS study at 9.4 T. Int J Neuropsychopharmacol. 2013;16:199-212.
  • Schulz D, Henn FA, Petri D, Huston JP. Rats bred for helplessness exhibit positive reinforcement learning deficits which are not alleviated by an antidepressant dose of the MAO-B inhibitor deprenyl. Neuroscience. 2016;329:83-92.
  • Knoll J, Miklya I. Enhanced catecholaminergic and serotoninergic activity in rat brain from weaning to sexual maturity: rationale for prophylactic (-)deprenyl (selegiline) medication. Life Sci. 1995;56:611-20.
  • Lamensdorf I, Youdim MB, Finberg JP. Effect of long-term treatment with selective monoamine oxidase A and B inhibitors on dopamine release from rat striatum in vivo. J Neurochem. 1996;67:1532-9.
  • Sunderland T, Mueller EA, Cohen RM, Jimerson DC, Pickar D, Murphy DL. Tyramine pressor sensitivity changes during deprenyl treatment. Psychopharmacol. 1985;86:432-7.
  • Fowler JS, Logan J, Volkow ND, Shumay E, McCall-Perez F, Jayne M, et al. Evidence that formulations of the selective MAO-B inhibitor, selegiline, which bypass first-pass metabolism, also inhibit MAO-A in the human brain. Neuropsychopharmacology. 2015;40:650-7.
  • Vollmayr B, Henn FA. Learned helplessness in the rat: improvements in validity and reliability. Brain Res Brain Res Protoc. 2001;8:1-7.
  • Carlsson A, Svennerholm L, Winblad B. Seasonal and circadian monoamine variations in human brains examined post mortem. Acta Psychiatr Scand Suppl. 1980; 280:75-85.
  • Whitaker PM, Warsh JJ, Stancer HC, Persad E, Vint CK. Seasonal variation in platelet 3H-imipramine binding: comparable values in control and depressed populations. Psychiatry Res. 1984;11:127-31.
  • Arora RC, Meltzer HY. Seasonal variation of imipramine binding in the blood platelets of normal controls and depressed patients. Biol Psychiatry. 1988;23:217-26.
  • DeMet EM, Chicz-DeMet A, Fleischmann J. Seasonal rhythm of platelet 3H-imipramine binding in normal controls. Biol Psychiatry. 1989;26:489-95.
  • Cappiello A, Malison RT, McDougle CJ, Vegso SJ, Charney DS, Heninger GR, et al. Seasonal variation in neuroendocrine and mood responses to IV L-tryptophan in depressed patients and healthy subjects. Neuropsychopharmacology. 1996;15:475-83.
  • Joseph-Vanderpool JR, Jacobsen FM, Murphy DL, Hill JL, Rosenthal NE. Seasonal variation in behavioural responses to m-CPP in patients with seasonal affective disorder and controls. Biol Psychiatry. 1993;33:496-504.
  • Oren DA, Moul DE, Schwartz PJ, Wehr TA, Rosenthal NE. A controlled trial of levodopa plus carbidopa in the treatment of winter seasonal affective disorder: a test of the dopamine hypothesis. J Clin Psychopharmacol. 1994;14:196-200.
  • Eisenberg DP, Kohn PD, Baller EB, Bronstein JA, Masdeu JC, Berman KF. Seasonal effects on human striatal presynaptic dopamine synthesis. J Neurosci. 2010;30:14691-4.
  • Naber D, Wirz-Justice A, Kafka MS, Tobler I, Borbely AA. Seasonal variations in the endogenous rhythm of dopamine receptor binding in the rat striatum. Biol Psychiatry. 1981;16:831-5.
  • Imbesi M, Yildiz S, Arslan AD, Sharma R, Manev H, Uz T. Dopamine receptor-mediated regulation of neuronal “clock” gene expression. Neuroscience. 2009;158:537-44.
  • Reichborn-Kjennerud T, Lingjaerde O, Oreland L. Platelet monoamine oxidase activity in patients with winter seasonal affective disorder. Psychiatry Res. 1996;62:273-80.
  • Chevillard C, Barden N, Saavedra JM. Twenty-four hour rhythm in monoamine oxidase activity in specific areas of the rat brain stem. Brain Res. 1981;223:205-9.
  • Hampp G, Ripperger JA, Houben T, Schmutz I, Blex C, Perreau-Lenz S, et al. Regulation of monoamine oxidase A by circadian-clock components implies clock influence on mood. Curr Biol. 2008;18:678-83.
  • Huston JP, Mueller CC, Mondadori C. Memory facilitation by posttrial hypothalamic stimulation and other reinforcers: a central theory of reinforcement. Biobehav Rev. 1977;1:143-50.
  • Huston JP, Oitzl M-S. The relationship between reinforcement and memory: parallels in the rewarding and mnemonic effects of the neuropeptide substance P. Neurosci Biobehav Rev. 1989;13:171-80.
  • White NM. Addictive drugs as reinforcers: Multiple partial actions on memory systems. Addiction. 1996;91:921-49.
There are 35 citations in total.

Details

Journal Section Research Article
Authors

Daniela Schulz This is me

Publication Date August 15, 2016
Published in Issue Year 2016

Cite

APA Schulz, D. (2016). Seasonal effects of the monoamine oxidase inhibitor deprenyl but not the tricyclic antidepressant imipramine in rats bred for helplessness. Medical Science and Discovery, 3(8), 312-6. https://doi.org/10.17546/msd.19700
AMA Schulz D. Seasonal effects of the monoamine oxidase inhibitor deprenyl but not the tricyclic antidepressant imipramine in rats bred for helplessness. Med Sci Discov. August 2016;3(8):312-6. doi:10.17546/msd.19700
Chicago Schulz, Daniela. “Seasonal Effects of the Monoamine Oxidase Inhibitor Deprenyl But Not the Tricyclic Antidepressant Imipramine in Rats Bred for Helplessness”. Medical Science and Discovery 3, no. 8 (August 2016): 312-6. https://doi.org/10.17546/msd.19700.
EndNote Schulz D (August 1, 2016) Seasonal effects of the monoamine oxidase inhibitor deprenyl but not the tricyclic antidepressant imipramine in rats bred for helplessness. Medical Science and Discovery 3 8 312–6.
IEEE D. Schulz, “Seasonal effects of the monoamine oxidase inhibitor deprenyl but not the tricyclic antidepressant imipramine in rats bred for helplessness”, Med Sci Discov, vol. 3, no. 8, pp. 312–6, 2016, doi: 10.17546/msd.19700.
ISNAD Schulz, Daniela. “Seasonal Effects of the Monoamine Oxidase Inhibitor Deprenyl But Not the Tricyclic Antidepressant Imipramine in Rats Bred for Helplessness”. Medical Science and Discovery 3/8 (August 2016), 312-6. https://doi.org/10.17546/msd.19700.
JAMA Schulz D. Seasonal effects of the monoamine oxidase inhibitor deprenyl but not the tricyclic antidepressant imipramine in rats bred for helplessness. Med Sci Discov. 2016;3:312–6.
MLA Schulz, Daniela. “Seasonal Effects of the Monoamine Oxidase Inhibitor Deprenyl But Not the Tricyclic Antidepressant Imipramine in Rats Bred for Helplessness”. Medical Science and Discovery, vol. 3, no. 8, 2016, pp. 312-6, doi:10.17546/msd.19700.
Vancouver Schulz D. Seasonal effects of the monoamine oxidase inhibitor deprenyl but not the tricyclic antidepressant imipramine in rats bred for helplessness. Med Sci Discov. 2016;3(8):312-6.