Role of the medial prefrontal cortex in the effects of rapid acting antidepressants on decision-making biases in rodents.
Journal
Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology
ISSN: 1740-634X
Titre abrégé: Neuropsychopharmacology
Pays: England
ID NLM: 8904907
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
21
01
2020
accepted:
08
07
2020
revised:
01
07
2020
pubmed:
26
8
2020
medline:
24
6
2021
entrez:
26
8
2020
Statut:
ppublish
Résumé
Major depressive disorder is a significant and costly cause of global disability. Until the discovery of the rapid acting antidepressant (RAAD) effects of ketamine, treatments were limited to drugs that have delayed clinical benefits. The mechanism of action of ketamine is currently unclear but one hypothesis is that it may involve neuropsychological effects mediated through modulation of affective biases (where cognitive processes such as learning and memory and decision-making are modified by emotional state). Previous work has shown that affective biases in a rodent decision-making task are differentially altered by ketamine, compared to conventional, delayed onset antidepressants. This study sought to further investigate these effects by comparing ketamine with other NMDA antagonists using this decision-making task. We also investigated the subtype selective GluN2B antagonist, CP-101,606 and muscarinic antagonist scopolamine which have both been shown to have RAAD effects. Both CP-101,606 and scopolamine induced similar positive biases in decision-making to ketamine, but the same effects were not seen with other NMDA antagonists. Using targeted medial prefrontal cortex (mPFC) infusions, these effects were localised to the mPFC. In contrast, the GABA
Identifiants
pubmed: 32842137
doi: 10.1038/s41386-020-00797-3
pii: 10.1038/s41386-020-00797-3
pmc: PMC7784869
doi:
Substances chimiques
Antidepressive Agents
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2278-2288Subventions
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N015762/1
Pays : United Kingdom
Références
World Health Organization. Depression fact sheet. 2018. https://www.who.int/news-room/fact-sheets/detail/depression . Accessed 5 Nov 2019.
Anderson IM, Nutt DJ, Deakin JFW. Evidence-based guidelines for treating depressive disorders with antidepressants: a revision of the 1993 British Association for Psychopharmacology guidelines. J Psychopharmacol. 2000;14:3–20.
pubmed: 10757248
doi: 10.1177/026988110001400101
Zarate CA,Jr, Singh JB, Carlson PJ, Brutsche NE, Ameli R, Luckenbaugh DA. et al. A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch Gen Psychiatry. 2006;63:856–64.
pubmed: 16894061
doi: 10.1001/archpsyc.63.8.856
Berman RM, Cappiello A, Anand A, Oren DA, Heninger GR, Charney DS. et al. Antidepressant effects of ketamine in depressed patients. Biol Psychiatry. 2000;47:351–4.
pubmed: 10686270
doi: 10.1016/S0006-3223(99)00230-9
Zarate CA,Jr, Singh JB, Quiroz JA, De Jesus G, Denicoff KK, Luckenbaugh DA. et al. A double-blind, placebo-controlled study of memantine in the treatment of major depression. Am J Psychiatry. 2006;163:153–5.
pubmed: 16390905
doi: 10.1176/appi.ajp.163.1.153
DiazGranados N, Ibrahim LA, Brutsche NE, Ameli R, Henter ID, Luckenbaugh DA. et al. Rapid resolution of suicidal ideation after a single infusion of an N-methyl-D-aspartate antagonist in patients with treatment-resistant major depressive disorder. J Clin Psychiatry. 2010;71:1605–11.
pubmed: 20673547
pmcid: 3012738
doi: 10.4088/JCP.09m05327blu
Lapidus KA, Levitch CF, Perez AM, Brallier JW, Parides MK, Soleimani L. et al. A randomized controlled trial of intranasal ketamine in major depressive disorder. Biol Psychiatry. 2014;76:970–6.
pubmed: 24821196
pmcid: 4185009
doi: 10.1016/j.biopsych.2014.03.026
Price RB, Iosifescu DV, Murrough JW, Chang LC, Al Jurdi RK, Iqbal SZ. et al. Effects of ketamine on explicit and implicit suicidal cognition: a randomized controlled trial in treatment-resistant depression. Depression Anxiety. 2014;31:335–43.
pubmed: 24668760
doi: 10.1002/da.22253
Mathews A, MacLeod C. Cognitive vulnerability to emotional disorders. Annu Rev Clin Psychol. 2005;1:167–95.
pubmed: 17716086
doi: 10.1146/annurev.clinpsy.1.102803.143916
Clark L, Chamberlain SR, Sahakian BJ. Neurocognitive mechanisms in depression: implications for treatment. Annu Rev Neurosci. 2009;32:57–74.
pubmed: 19400725
doi: 10.1146/annurev.neuro.31.060407.125618
Gotlib IH, Joormann J. Cognition and depression: current status and future directions. Annu Rev Clin Psychol. 2010;6:285–312.
pubmed: 20192795
pmcid: 2845726
doi: 10.1146/annurev.clinpsy.121208.131305
Harmer CJ, Bhagwagar Z, Perrett DI, Vollm BA, Cowen PJ, Goodwin GM. Acute SSRI administration affects the processing of social cues in healthy volunteers. Neuropsychopharmacology. 2003;28:148–52.
pubmed: 12496951
doi: 10.1038/sj.npp.1300004
Harmer CJ, Shelley NC, Cowen PJ, Goodwin GM. Increased positive versus negative affective perception and memory in healthy volunteers following selective serotonin and norepinephrine reuptake inhibition. Am J Psychiatry. 2004;161:1256–63.
pubmed: 15229059
doi: 10.1176/appi.ajp.161.7.1256
Harmer CJ, de Bodinat C, Dawson GR, Dourish CT, Waldenmaier L, Adams S. et al. Agomelatine facilitates positive versus negative affective processing in healthy volunteer models. J Psychopharmacol (Oxf, Engl). 2011;25:1159–67.
doi: 10.1177/0269881110376689
Harmer CJ, O’Sullivan U, Favaron E, Massey-Chase R, Ayres R, Reinecke A. et al. Effect of acute antidepressant administration on negative affective bias in depressed patients. Am J Psychiatry. 2009;166:1178–84.
pubmed: 19755572
doi: 10.1176/appi.ajp.2009.09020149
Stuart SA, Butler P, Munafo MR, Nutt DJ, Robinson ES. A translational rodent assay of affective biases in depression and antidepressant therapy. Neuropsychopharmacology. 2013;38:1625–35.
pubmed: 23503126
pmcid: 3717539
doi: 10.1038/npp.2013.69
Harding EJ, Paul ES, Mendl M. Animal behaviour: Cognitive bias and affective state. Nature. 2004;427:312–312.
pubmed: 14737158
doi: 10.1038/427312a
Robinson E, Roiser J. Affective biases in humans and animals. In: Robbins TW, Sahakian BJ, editors. Translational neuropsychopharmacology. Current topics in behavioral neurosciences, Vol. 28. Cham: Springer; 2015.
Mendl M, Burman OHP, Paul ES. An integrative and functional framework for the study of animal emotion and mood. Proc R Soc B: Biol Sci. 2010;277:2895–904.
doi: 10.1098/rspb.2010.0303
Roelofs S, Boleij H, Nordquist RE, van der Staay FJ. Making decisions under ambiguity: judgment bias tasks for assessing emotional state in animals. Frontiers Behav Neurosci. 2016;10:119.
doi: 10.3389/fnbeh.2016.00119
Neville V, Nakagawa S, Zidar J, Paul ES, Lagisz M, Bateson M. et al. Pharmacological manipulations of judgement bias: a systematic review and meta-analysis. Neurosci Biobehav Rev. 2020;108:269–86.
pubmed: 31747552
pmcid: 6966323
doi: 10.1016/j.neubiorev.2019.11.008
Hales CA, Robinson ES, Houghton CJ. Diffusion modelling reveals the decision making processes underlying negative judgement bias in rats. PloS ONE. 2016;11:e0152592.
pubmed: 27023442
pmcid: 4811525
doi: 10.1371/journal.pone.0152592
Parker RM, Paul ES, Burman OH, Browne WJ, Mendl M. Housing conditions affect rat responses to two types of ambiguity in a reward-reward discrimination cognitive bias task. Behav Brain Res. 2014;274:73–83.
pubmed: 25106739
pmcid: 4199117
doi: 10.1016/j.bbr.2014.07.048
Hales CA, Houghton CJ, Robinson ESJ. Behavioural and computational methods reveal differential effects for how delayed and rapid onset antidepressants effect decision making in rats. Eur Neuropsychopharmacol. 2017;27:1268–80.
pubmed: 29100819
pmcid: 5720479
doi: 10.1016/j.euroneuro.2017.09.008
Sanacora G, Johnson MR, Khan A, Atkinson SD, Riesenberg RR, Schronen JP. et al. Adjunctive lanicemine (AZD6765) in patients with major depressive disorder and history of inadequate response to antidepressants: a randomized, placebo-controlled study. Neuropsychopharmacology. 2017;42:844–53.
pubmed: 27681442
doi: 10.1038/npp.2016.224
Smith EG, Deligiannidis KM, Ulbricht CM, Landolin CS, Patel JK, Rothschild AJ. Antidepressant augmentation using the N-methyl-D-aspartate antagonist memantine: a randomized, double-blind, placebo-controlled trial. J Clin Psychiatry. 2013;74:966–73.
pubmed: 24229746
pmcid: 4000742
doi: 10.4088/JCP.12m08252
Ates-Alagoz Z, Adejare A. NMDA receptor antagonists for treatment of depression. Pharmaceuticals (Basel). 2013;6:480–99.
doi: 10.3390/ph6040480
Preskorn SH, Baker B, Kolluri S, Menniti FS, Krams M, Landen JW. An innovative design to establish proof of concept of the antidepressant effects of the NR2B subunit selective N-methyl-D-aspartate antagonist, CP-101,606, in patients with treatment-refractory major depressive disorder. J Clin Psychopharmacol. 2008;28:631–7.
pubmed: 19011431
doi: 10.1097/JCP.0b013e31818a6cea
Furey ML, Drevets WC. Antidepressant efficacy of the antimuscarinic drug scopolamine: a randomized, placebo-controlled clinical trial. Arch Gen Psychiatry. 2006;63:1121–9.
pubmed: 17015814
pmcid: 3250308
doi: 10.1001/archpsyc.63.10.1121
Browne CA, Lucki I. Antidepressant effects of ketamine: mechanisms underlying fast-acting novel antidepressants. Front Pharmacol. 2013;4:161.
pubmed: 24409146
pmcid: 3873522
doi: 10.3389/fphar.2013.00161
Li CT, Chen MH, Lin WC, Hong CJ, Yang BH, Liu RS. et al. The effects of low-dose ketamine on the prefrontal cortex and amygdala in treatment-resistant depression: a randomized controlled study. Hum Brain Mapp. 2016;37:1080–90.
pubmed: 26821769
pmcid: 6867460
doi: 10.1002/hbm.23085
Abdallah CG, De Feyter HM, Averill LA, Jiang L, Averill CL, Chowdhury GMI. et al. The effects of ketamine on prefrontal glutamate neurotransmission in healthy and depressed subjects. Neuropsychopharmacology. 2018;43:2154–60.
pubmed: 29977074
pmcid: 6098048
doi: 10.1038/s41386-018-0136-3
Stuart SA, Butler P, Munafo MR, Nutt DJ, Robinson ES. Distinct neuropsychological mechanisms may explain delayed- versus rapid-onset antidepressant efficacy. Neuropsychopharmacology. 2015;40:2165–74.
pubmed: 25740288
pmcid: 4487826
doi: 10.1038/npp.2015.59
Stuart SA, Robinson ESJ. Reducing the stress of drug administration: implications for the 3Rs. Sci Rep. 2015;5:14288.
pubmed: 26395864
pmcid: 4585806
doi: 10.1038/srep14288
Duman RS. Ketamine and rapid-acting antidepressants: a new era in the battle against depression and suicide. F1000Research 2018;7:F1000 Faculty Rev-659.
Benn A, Robinson ES. Investigating glutamatergic mechanism in attention and impulse control using rats in a modified 5-choice serial reaction time task. PloS ONE. 2014;9:e115374.
pubmed: 25526617
pmcid: 4272291
doi: 10.1371/journal.pone.0115374
Paxinos G, Watson C. The rat brain—in stereotaxic coordinates. San Diego, CA: Academic Press; 1998.
Bethell EJ. A “how-to” guide for designing judgment bias studies to assess captive animal welfare. J Appl Anim Welf Sci. 2015;18:S18–S42.
pubmed: 26440495
doi: 10.1080/10888705.2015.1075833
Baciadonna L, McElligott AG. The use of judgement bias to assess welfare in farm livestock. Anim Welf. 2015;24:81–91.
doi: 10.7120/09627286.24.1.081
Polis AJ, Fitzgerald PJ, Hale PJ, Watson BO. Rodent ketamine depression-related research: Finding patterns in a literature of variability. Behav Brain Res. 2019;376:112153.
pubmed: 31419519
doi: 10.1016/j.bbr.2019.112153
pmcid: 6783386
Gerhard DM, Pothula S, Liu RJ, Wu M, Li XY, Girgenti MJ et al. GABA interneurons are the cellular trigger for ketamine’s rapid antidepressant actions. J Clin Invest. 2020;130:1336–1349.
Drewniany E, Han J, Hancock C, Jones RL, Lim J, Nemat Gorgani N. et al. Rapid-onset antidepressant action of ketamine: potential revolution in understanding and future pharmacologic treatment of depression. J Clin Pharm Ther. 2015;40:125–30.
pubmed: 25545040
doi: 10.1111/jcpt.12238
Li N, Lee B, Liu RJ, Banasr M, Dwyer JM, Iwata M. et al. mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science. 2010;329:959–64.
pubmed: 20724638
pmcid: 3116441
doi: 10.1126/science.1190287
Voleti B, Navarria A, Liu RJ, Banasr M, Li N, Terwilliger R. et al. Scopolamine rapidly increases mammalian target of rapamycin complex 1 signaling, synaptogenesis, and antidepressant behavioral responses. Biol Psychiatry. 2013;74:742–9.
pubmed: 23751205
doi: 10.1016/j.biopsych.2013.04.025
Wohleb ES, Wu M, Gerhard DM, Taylor SR, Picciotto MR, Alreja M. et al. GABA interneurons mediate the rapid antidepressant-like effects of scopolamine. J Clin Invest. 2016;126:2482–94.
pubmed: 27270172
pmcid: 4922686
doi: 10.1172/JCI85033
Murphy ER, Fernando ABP, Urcelay GP, Robinson ESJ, Mar AC, Theobald DEH. et al. Impulsive behaviour induced by both NMDA receptor antagonism and GABAA receptor activation in rat ventromedial prefrontal cortex. Psychopharmacology. 2012;219:401–10.
pubmed: 22101355
doi: 10.1007/s00213-011-2572-1
Ceglia I, Carli M, Baviera M, Renoldi G, Calcagno E, Invernizzi RW. The 5-HT receptor antagonist M100,907 prevents extracellular glutamate rising in response to NMDA receptor blockade in the mPFC. J Neurochem. 2004;91:189–99.
pubmed: 15379899
doi: 10.1111/j.1471-4159.2004.02704.x
Moghaddam B, Adams B, Verma A, Daly D. Activation of glutamatergic neurotransmission by ketamine: a novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci. 1997;17:2921–7.
pubmed: 9092613
pmcid: 6573099
doi: 10.1523/JNEUROSCI.17-08-02921.1997
Eshel N, Roiser JP. Reward and punishment processing in depression. Biol Psychiatry. 2010;68:118–24.
pubmed: 20303067
doi: 10.1016/j.biopsych.2010.01.027
Murrough JW, Iacoviello B, Neumeister A, Charney DS, Iosifescu DV. Cognitive dysfunction in depression: neurocircuitry and new therapeutic strategies. Neurobiol Learn Mem. 2011;96:553–63.
pubmed: 21704176
doi: 10.1016/j.nlm.2011.06.006
Biselli T, Lange S, Sablottny L, Steffen J, Walther A. Optogenetic and chemogenetic insights into the neurocircuitry of depression-like behaviour: a systematic review. Eur J Neurosci. https://doi.org/10.1111/ejn.14603 . [Epub ahead of print].
Hare BD, Shinohara R, Liu RJ, Pothula S, DiLeone RJ, Duman RS. Optogenetic stimulation of medial prefrontal cortex Drd1 neurons produces rapid and long-lasting antidepressant effects. Nat Commun. 2019;10:223.
pubmed: 30644390
pmcid: 6333924
doi: 10.1038/s41467-018-08168-9