A meta-analysis of D-cycloserine and the facilitation of fear extinction and exposure therapy

Norberg, Melissa M.; Krystal, John H.; Tolin, David F.

doi:10.1016/j.biopsych.2008.01.012

Cited by 510Memory and Neural MechanismsPosttraumatic Stress Disorder ResearchAnxiety, Depression, Psychometrics, Treatment, Cognitive Processes

A meta-analysis of D-cycloserine and the facilitation of fear extinction and exposure therapy

Norberg, Melissa M., Krystal, John H., Tolin, David F.·2008·Biological Psychiatry

DOI 10.1016/j.biopsych.2008.01.012

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Abstract

Background Translational research suggests that D-cycloserine (DCS), a partial N-methyl-D-aspartate (NMDA) receptor agonist, might facilitate fear extinction and exposure therapy by either enhancing NMDA receptor function during extinction or by reducing NMDA receptor function during fear memory consolidation. This article provides a quantitative review of DCS-augmented fear extinction and exposure therapy literature.Methods English-language journal articles that examined DCS augmented with fear extinction or exposure therapy were identified through public databases from June 1998 through September 2007, through references of originally identified articles and contact with DCS investigators. Data were extracted for study author, title, and year; trial design; type of subject (animal vs. human; clinical vs. nonclinical); sample size, DCS dose, and timing in relation to extinction/exposure procedures; dependent variable; group means and SDs at post-extinction/exposure; and follow-up outcome.Results D-cycloserine enhances fear extinction/exposure therapy in both animals and anxiety-disordered humans. Gains generally were maintained at follow-up, although some lessening of efficacy was noted. D-cycloserine was more effective when administered a limited number of times and when given immediately before or after extinction training/exposure therapy.Conclusions This meta-analysis suggests that DCS is a useful target for translational research on augmenting exposure-based treatment via compounds that impact neuroplasticity. D-cycloserine 's major contribution to exposure-based therapy might be to increase its speed or efficiency, because the effects of DCS seem to decrease over repeated sessions. This information might guide translational researchers in discovering more selective and/or effective agents that effectively enhance (or reduce) NMDA receptor function.

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The human amygdala plays a role in extinction learning.
“we know that the human amygdala plays a role in extinction learning.”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [104]
Intra-amygdala infusion of the NMDA receptor agonist d-cycloserine facilitates extinction learning, and this work has been successfully translated to humans.
“From rodent research showing that intra-amygdala infusion of the NMDA receptor agonist d-cycloserine, which enhances NMDA-dependent plasticity, facilitates extinction learning, and successful translation of this work to humans (see [104] for review), we know that the human amygdala plays a role in extinction learning.”
From Prefrontal cortex, amygdala, and threat processing: implications for PTSD (2022) · cites this paper as [104]
Pre-session dosing has been the strategy employed in all studies to date.
“Pre-session dosing has been the strategy employed in all studies to date (1).”
From D-cycloserine enhancement of fear extinction is specific to successful exposure sessions: evidence from the treatment of height phobia (2013) · cites this paper as [1]

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IV glycine and oral d-cycloserine effects on plasma and CSF amino acids in healthy humans
D’Souza, D. C., Gil, R. B., Cassello, K., Morrissey, K., Abi‐Saab, D., White, J., Sturwold, R., Bennett, A., Karper, L. P., Zuzarte, E., et al. (2000) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00133-x · Cited by 111 · see citing works
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Actions of ?-cycloserine at the ? glycine receptor site in vivo
Emmett, M. R. (1991) · Neuropharmacology · doi:10.1016/0028-3908(91)90161-4 · Cited by 108 · see citing works
A randomized controlled trial of the effect of D-cycloserine on extinction and fear conditioning in humans
Guastella, A. J., Lovibond, P. F., Dadds, M. R., Mitchell, P., & Richardson, R. (2007) · Behaviour Research and Therapy · doi:10.1016/j.brat.2006.07.005 · Cited by 106 · see citing works
Long‐term potentiation as a substrate for memory: Evidence from studies of amygdaloid plasticity and Pavlovian fear conditioning
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White matter lesions in Fabry disease occur in ‘prior’ selectively hypometabolic and hyperperfused brain regions
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Facilitation of conditioned fear extinction by d-cycloserine is mediated by mitogen-activated protein kinase and phosphatidylinositol 3-kinase cascades and requires de novo protein synthesis in basolateral nucleus of amygdala
Yang, Y.-L., & Lu, K. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.04.003 · Cited by 93 · see citing works
Effects of d-cycloserine on negative symptoms in schizophrenia
Duncan, E., Szilagyi, S., Schwartz, M. P., Bugarski‐Kirola, D., Kunzova, A., Negi, S., Stephanides, M., Efferen, T. R., Angrist, B., Peselow, E. D., et al. (2004) · Schizophrenia Research · doi:10.1016/j.schres.2004.03.013 · Cited by 90 · see citing works
Long-term memory of cocaine-associated context: disruption and reinstatement
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Excessive cerebrocortical release of acetylcholine induced by NMDA antagonists is reduced by GABAergic and α2-adrenergic agonists
Kim, S. H., Price, M. T., Olney, J. W., & Farber, N. B. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000529 · Cited by 86 · see citing works
Effects of D-cycloserine on extinction of learned fear to an olfactory cue
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Glutamate NMDA Receptors within the Amygdala Participate in the Modulatory Effect of Glucocorticoids on Extinction of Conditioned Fear in Rats
Yang, Y.-L., Chao, P.-K., Ro, L., Wo, Y., & Lu, K.-T. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301215 · Cited by 79 · see citing works
The NMDA receptor antagonist MK-801 blocks acquisition and extinction of conditioned hypoalgesic responses in the rat.
Cox, J., & Westbrook, R. F. (1994) · PubMed · Cited by 74 · see citing works
D-cycloserine for Alzheimer's disease
Jones, R. W., Laake, K., & Øksengård, A. R. (2002) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd003153 · Cited by 72 · see citing works
Influence of ethanol withdrawal on fear memory: Effect of d-cycloserine
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Desensitization of the NMDA receptor complex by glycinergic ligands in cerebellar granule cell cultures
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Glycine Site Agonists of the NMDA Receptor: A Review
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D-Cycloserine Treatment of Alzheimer Disease
RANDOLPH, C. C., Roberts, J. W., Tierney, M. C., Bravi, D., Mouradian, M. M., & Chase, T. N. (1994) · Alzheimer Disease & Associated Disorders · doi:10.1097/00002093-199408030-00006 · Cited by 53 · see citing works
Clinical perspectives on the combination of D-cycloserine and cognitive-behavioral therapy for the treatment of anxiety disorders.
Otto, M. W., Basden, S. L., Leyro, T. M., McHugh, R. K., & Hofmann, S. G. (2007) · CNS Spectrums · doi:10.1017/s1092852900020526 · Cited by 53 · see citing works
Evaluation of Cycloserine in the Treatment of Alzheimer's Disease
Fakouhi, T. D., Jhee, S. S., Sramek, J. J., Benes, C. O., Schwartz, P., Hantsburger, G., Herting, R. L., Swabb, E. A., & Cutler, N. R. (1995) · Journal of Geriatric Psychiatry and Neurology · doi:10.1177/089198879500800405 · Cited by 51 · see citing works
Bergmann glial GlyT1 mediates glycine uptake and release in mouse cerebellar slices
Huang, H., Barakat, L., Wang, D. D., & Bordey, A. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.067801 · Cited by 50 · see citing works
Effects of ketamine and pentobarbitone on acetylcholine release from the rat frontal cortex in vivo
Kikuchi, T., Wang, Y., Shinbori, H., Sato, K., & Okumura, F. (1997) · British Journal of Anaesthesia · doi:10.1093/bja/79.1.128 · Cited by 49 · see citing works
Facilitation of Extinction of Conditioned Fear by D-Cycloserine: Implications for Psychotherapy
Davis, M., Myers, K. M., Ressler, K. J., & Rothbaum, B. O. (2005) · Current Directions in Psychological Science · doi:10.1111/j.0963-7214.2005.00367.x · Cited by 43 · see citing works
Effects of D-Cycloserine on Extinction: Consequences of Prior Exposure to Imipramine
Werner-Seidler, A., & Richardson, R. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.010 · Cited by 43 · see citing works
Delay aversion: Effects of 7-OH-DPAT, 5-HT1A/1B-receptor stimulation and d-cycloserine
van den Bergh, F. S., Bloemarts, E., Groenink, L., Olivier, B., & Oosting, R. S. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.11.007 · Cited by 42 · see citing works
NMDA Partial Agonist Reverses Blocking of Extinction of Aversive Memory by GABAA Agonist in the Amygdala
Akirav, I. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301050 · Cited by 42 · see citing works
d-Cycloserine and performance under different states of anxiety in healthy volunteers
Bailey, J., Papadopoulos, A., Lingford-Hughes, A. R., & Nutt, D. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0817-9 · Cited by 37 · see citing works
Neuroplasticity as a Target for the Pharmacotherapy of Psychiatric Disorders: New Opportunities for Synergy with Psychotherapy
Krystal, J. H. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.08.017 · Cited by 34 · see citing works
Self-citation
D-Cycloserine enhances memory consolidation of hippocampus-dependent latent extinctionPreprint
Gabriele, A., & Packard, M. G. (2007) · Learning & Memory · doi:10.1101/lm.528007 · Cited by 32 · see citing works
The Glial and the Neuronal Glycine Transporters Differ in Their Reactivity to Sulfhydryl Reagents
Roux, M. J., Maza, R. M., Goff, A. L., López‐Corcuera, B., Aragón, C., & Supplisson, S. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009196200 · Cited by 31 · see citing works
Pharmacotherapy for performance anxiety disorders: occasionally useful but typically contraindicated.
Birk, L. (2004) · Journal of Clinical Psychology · doi:10.1002/jclp.20044 · Cited by 31 · see citing works
Emotional Learning and Glutamate: Translational Perspectives
Gillespie, C. F., & Ressler, K. J. (2005) · CNS Spectrums · doi:10.1017/s1092852900010439 · Cited by 27 · see citing works
Manipulation of NMDA-receptor activity alters extinction of an instrumental response in rats
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Effects of light deprivation on recovery from neglect and extinction induced by unilateral lesions of the medial agranular cortex and dorsocentral striatum
Vleet, T. V., Heldt, S. A., Pyter, B., Corwin, J. V., & Reep, R. L. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00246-2 · Cited by 22 · see citing works
Unilateral destruction of the dorsocentral striatum in rats produces neglect but not extinction to bilateral simultaneous stimulation
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Glycine ketamine interactions in healthy humans
D’Souza, D. C., Gil, R. B., Zuzarte, E., Abi‐Saab, D., Damon, D., White, J., Zimmerman, L., & Krystal, J. H. (1997) · Schizophrenia Research · doi:10.1016/s0920-9964(97)82609-6 · Cited by 18 · see citing works
Self-citation
D-cycloserine Inhibits Amygdala Responses During Repeated Presentations of Faces
Britton, J. C., Gold, A. L., Feczko, E., Rauch, S. L., Williams, D., & Wright, C. I. (2007) · CNS Spectrums · doi:10.1017/s1092852900021398 · Cited by 16 · see citing works
Quantitative gene expression of two types of glycine transporter in the rat central nervous system
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Effects of activation and blockade of NMDA receptors on the extinction of a conditioned passive avoidance response in mice with different levels of anxiety
Tomilenko, R. A., & Dubrovina, N. I. (2007) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-007-0044-1 · Cited by 14 · see citing works

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Glutamate Receptor Ion Channels: Structure, Regulation, and Function
Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., Hansen, K. B., Yuan, H., Myers, S. J., & Dingledine, R. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002451 · Cited by 3,568 · see citing works
World Federation of Societies of Biological Psychiatry (WFSBP) Guidelines for the Pharmacological Treatment of Anxiety, Obsessive-Compulsive and Post-Traumatic Stress Disorders – First Revision
Bandelow, B., Zohar, J., Hollander, E., Kasper, S., Möller, H., & WFSBP Task Force on Treatment Guide (2008) · The World Journal of Biological Psychiatry · doi:10.1080/15622970802465807 · Cited by 862 · see citing works
Obsessive-compulsive disorder: An integrative genetic and neurobiological perspective
Pauls, D. L., Abramovitch, A., Rauch, S. L., & Geller, D. A. (2014) · Nature Reviews Neuroscience · doi:10.1038/nrn3746 · Cited by 793 · see citing works
The biomedical model of mental disorder: A critical analysis of its validity, utility, and effects on psychotherapy research
Deacon, B. J. (2013) · Clinical Psychology Review · doi:10.1016/j.cpr.2012.09.007 · Cited by 656 · see citing works
Fear conditioning, synaptic plasticity and the amygdala: implications for posttraumatic stress disorder
Mahan, A. L., & Ressler, K. J. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.06.007 · Cited by 616 · see citing works
Practice Parameter for the Assessment and Treatment of Children and Adolescents With Obsessive-Compulsive Disorder
GELLER, D. A., & March, J. S. (2011) · Journal of the American Academy of Child & Adolescent Psychiatry · doi:10.1016/j.jaac.2011.09.019 · Cited by 516 · see citing works
Implications of memory modulation for post-traumatic stress and fear disorders
Parsons, R. G., & Ressler, K. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3296 · Cited by 476 · see citing works
Efficacy of Cognitive Behavioral Therapy for Anxiety Disorders: A Review of Meta-Analytic Findings
Olatunji, B. O., Cisler, J. M., & Deacon, B. J. (2010) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2010.04.002 · Cited by 483 · see citing works
From Pavlov to PTSD: The extinction of conditioned fear in rodents, humans, and anxiety disorders
VanElzakker, M. B., Kathryn Dahlgren, M., Caroline Davis, F., Dubois, S., & Shin, L. M. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.11.014 · Cited by 482 · see citing works
How the Neurocircuitry and Genetics of Fear Inhibition May Inform Our Understanding of PTSD
Jovanović, T., & Ressler, K. J. (2010) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.09071074 · Cited by 441 · see citing works
Glutamate abnormalities in obsessive compulsive disorder: neurobiology, pathophysiology, and treatment
Pittenger, C., Bloch, M. H., & Williams, K. (2011) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2011.09.006 · Cited by 426 · see citing works
50 years of hurdles and hope in anxiolytic drug discovery
Griebel, G., & Holmes, A. (2013) · Nature Reviews Drug Discovery · doi:10.1038/nrd4075 · Cited by 414 · see citing works
Pharmacology of cognitive enhancers for exposure-based therapy of fear, anxiety and trauma-related disorders
Singewald, N., Schmuckermair, C., Whittle, N., Holmes, A., & Ressler, K. J. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2014.12.004 · Cited by 390 · see citing works
“Indeed, by successfully translating findings from animal models, progress has been made in enhancing the outcomes of exposure-based CBT using compounds such as DCS, yohimbine and glucocorticoids as cognitive enhancers in the treatment of patientswith anxiety disorders, PTSD andOCD (Hofmann& Smits, 2008; McGuire et al.…”
Method
The Study of Fear Extinction: Implications for Anxiety Disorders
Graham, B. M., & Milad, M. R. (2011) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2011.11040557 · Cited by 387 · see citing works
The efficacy of exposure therapy for anxiety-related disorders and its underlying mechanisms: The case of OCD and PTSD
Foa, E. B., & McLean, C. P. (2016) · Annual Review of Clinical Psychology · doi:10.1146/annurev-clinpsy-021815-093533 · Cited by 360 · see citing works
Prefrontal cortex, amygdala, and threat processing: implications for PTSD
Alexandra Kredlow, M., Fenster, R. J., Laurent, E. S., Ressler, K. J., & Phelps, E. A. (2022) · Neuropsychopharmacology · doi:10.1038/s41386-021-01155-7 · Cited by 346 · see citing works
“From rodent research showing that intra-amygdala infusion of the NMDA receptor agonist d-cycloserine, which enhances NMDAdependent plasticity, facilitates extinction learning, and successful translation of this work to humans (see [104] for review), we know that the human amygdala plays a role in extinction learning.”
Background
D-Cycloserine Augmentation of Exposure-Based Cognitive Behavior Therapy for Anxiety, Obsessive-Compulsive, and Posttraumatic Stress Disorders: A Systematic Review and Meta-analysis of Individual Participant Data
Mataix-Cols, D., Fernández de la Cruz, L., Monzani, B., Rosenfield, D., Andersson, E., Pérez-Vigil, A., Frumento, P., de Kleine, R. A., Difede, J., Dunlop, B. W., et al. (2017) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2016.3955 · Cited by 288 · see citing works
Self-citation
Glucocorticoids enhance extinction-based psychotherapy
de Quervain, D. J. ‐., Bentz, D., Michael, T., Bolt, O. C., Wiederhold, B. K., Margraf, J., & Wilhelm, F. H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018214108 · Cited by 263 · see citing works
Sleep and REM sleep disturbance in the pathophysiology of PTSD: the role of extinction memory
Pace-Schott, E. F., Germain, A., & Milad, M. R. (2015) · Biology of Mood & Anxiety Disorders · doi:10.1186/s13587-015-0018-9 · Cited by 255 · see citing works
Cocaine‐induced neuroadaptations in glutamate transmission
Schmidt, H. D., & Pierce, R. C. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05144.x · Cited by 254 · see citing works
Efficacy of D-Cycloserine for Enhancing Response to Cognitive-Behavior Therapy for Panic Disorder
Otto, M. W., Tolin, D. F., Simon, N. M., Pearlson, G. D., Basden, S., Meunier, S. A., Hofmann, S. G., Eisenmenger, K., Krystal, J. H., & Pollack, M. H. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.07.036 · Cited by 251 · see citing works
Self-citation
The modification of attentional bias to emotional information: A review of the techniques, mechanisms, and relevance to emotional disorders
Browning, M., Holmes, E. A., & Harmer, C. J. (2010) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.10.1.8 · Cited by 247 · see citing works
Examining potential contraindications for prolonged exposure therapy for PTSD
van Minnen, A., Harned, M. S., Zoellner, L., & Mills, K. (2012) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v3i0.18805 · Cited by 248 · see citing works
Genetic Gating of Human Fear Learning and Extinction
Lonsdorf, T. B., Weike, A. I., Nikamo, P., Schalling, M., Hamm, A. O., & Öhman, A. (2009) · Psychological Science · doi:10.1111/j.1467-9280.2009.02280.x · Cited by 242 · see citing works
Role of inhibition in exposure therapy
Craske, M. G., Liao, B., Brown, L., & Vervliet, B. (2012) · Journal of Experimental Psychopathology · doi:10.5127/jep.026511 · Cited by 237 · see citing works
Effects of sleep on memory for conditioned fear and fear extinction.
Pace-Schott, E. F., Germain, A., & Milad, M. R. (2015) · Psychological Bulletin · doi:10.1037/bul0000014 · Cited by 218 · see citing works
Psychopharmacological Treatment of Obsessive-Compulsive Disorder (OCD)
CASALE, A. D., Sorice, S., Padovano, A., Simmaco, M., Ferracuti, S., Lamis, D. A., Rapinesi, C., Sani, G., Girardi, P., Kotzalidis, G. D., et al. (2018) · Current Neuropharmacology · doi:10.2174/1570159x16666180813155017 · Cited by 231 · see citing works
A Randomized Placebo-Controlled Trial of d-Cycloserine to Enhance Exposure Therapy for Posttraumatic Stress Disorder
de Kleine, R. A., Hendriks, G.-J., Kusters, W. J. C., Broekman, T. G., & van Minnen, A. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.02.033 · Cited by 220 · see citing works
Pharmacological Treatment of Obsessive-Compulsive Disorder
Pittenger, C., & Bloch, M. H. (2014) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2014.05.006 · Cited by 222 · see citing works
Treatment of Posttraumatic Stress Disorder: A State-of-the-art Review
Burback, L., Brémault‐Phillips, S., Nijdam, M. J., McFARLANE, A. C., & Vermetten, E. H. G. J. M. (2023) · Current Neuropharmacology · doi:10.2174/1570159x21666230428091433 · Cited by 232 · see citing works
Depression: An Evolutionarily Conserved Mechanism to Terminate Separation Distress? A Review of Aminergic, Peptidergic, and Neural Network Perspectives
Watt, D. F., & Panksepp, J. (2009) · Neuropsychoanalysis · doi:10.1080/15294145.2009.10773593 · Cited by 207 · see citing works
New perspectives in glutamate and anxiety
Riaza Bermudo-Soriano, C., Perez-Rodriguez, M. M., Vaquero-Lorenzo, C., & Baca-Garcia, E. (2012) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.04.010 · Cited by 207 · see citing works
Impaired Extinction Retention in Adolescent Rats: Effects of D-Cycloserine
McCallum, J., Kim, J. H., & Richardson, R. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.92 · Cited by 198 · see citing works
A randomized placebo-controlled trial of d-cycloserine and exposure therapy for posttraumatic stress disorder
Litz, B. T., Salters-Pedneault, K., Steenkamp, M. M., Hermos, J. A., Bryant, R. A., Otto, M. W., & Hofmann, S. G. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.05.006 · Cited by 196 · see citing works
A Preliminary Study of D-Cycloserine Augmentation of Cognitive-Behavioral Therapy in Pediatric Obsessive-Compulsive Disorder
Storch, E. A., Murphy, T. K., Goodman, W. K., Geffken, G. R., Lewin, A. B., Henin, A., Micco, J. A., Sprich, S. E., Wilhelm, S., Bengtson, M. A., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.07.015 · Cited by 193 · see citing works
Psychiatric Disorders: Diagnosis to Therapy
Krystal, J. H., & State, M. W. (2014) · Cell · doi:10.1016/j.cell.2014.02.042 · Cited by 191 · see citing works
Self-citation
Glutamate dysregulation and glutamatergic therapeutics for PTSD: Evidence from human studies
Averill, L. A., Purohit, P., Averill, C. L., Boesl, M. A., Krystal, J. H., & Abdallah, C. G. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.11.064 · Cited by 184 · see citing works
Self-citation
Pharmacological treatment of anxiety disorders: Current treatments and future directions
Farach, F. J., Pruitt, L. D., Jun, J. J., Jerud, A. B., Zoellner, L. A., & Roy‐Byrne, P. (2012) · Journal of Anxiety Disorders · doi:10.1016/j.janxdis.2012.07.009 · Cited by 183 · see citing works
Prolonged exposure therapy for post-traumatic stress disorder: a review of evidence and dissemination
McLean, C. P., & Foa, E. B. (2011) · Expert Review of Neurotherapeutics · doi:10.1586/ern.11.94 · Cited by 148 · see citing works
Potential Psychiatric Applications of Metabotropic Glutamate Receptor Agonists and Antagonists
Krystal, J. H., Mathew, S. J., DʼSouza, D. C., Garakani, A., Gunduz-Bruce, H., & Charney, D. S. (2010) · CNS Drugs · doi:10.2165/11533230-000000000-00000 · Cited by 180 · see citing works
Self-citation
A randomized add-on trial of high-dose d-cycloserine for treatment-resistant depression
Heresco-Levy, U., Gelfin, G., Bloch, B., Levin, R., Edelman, S., Javitt, D. C., & Kremer, I. (2013) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000910 · Cited by 177 · see citing works
Pilot controlled trial of d-serine for the treatment of post-traumatic stress disorder
Heresco‐Levy, U., Vass, Á., Bloch, B., Wolosker, H., Dumin, E., Balan, L., Deutsch, L., & Kremer, I. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709000339 · Cited by 171 · see citing works
Advancing psychotherapy and evidence‐based psychological interventions
Emmelkamp, P. M. G., David, D., Beckers, T., Muris, P., Cuijpers, P. J., Lutz, W., Andersson, G., Araya, R., Rivera, R. M. B., Barkham, M., et al. (2013) · International Journal of Methods in Psychiatric Research · doi:10.1002/mpr.1411 · Cited by 167 · see citing works
Improving Outcome of Psychosocial Treatments by Enhancing Memory and Learning
Harvey, A. G., Lee, J., Williams, J. J., Hollon, S. D., Walker, M. P., Thompson, M. A., & Smith, R. (2014) · Perspectives on Psychological Science · doi:10.1177/1745691614521781 · Cited by 162 · see citing works
Evidence-based treatment research: advances, limitations, and next steps
Kazdin, A. E. (2011) · American Psychologist · doi:10.1037/a0024975 · Cited by 155 · see citing works
Neuropeptide regulation of fear and anxiety: Implications of cholecystokinin, endogenous opioids, and neuropeptide Y
Bowers, M. E., Choi, D. C., & Ressler, K. J. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.03.004 · Cited by 155 · see citing works
Glutamatergic transmission in schizophrenia
Kantrowitz, J. T., & Javitt, D. C. (2012) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e32835035b2 · Cited by 155 · see citing works
Pharmacotherapy of anxiety disorders: A critical review
Koen, N., & Stein, D. J. (2011) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2011.13.4/nkoen · Cited by 151 · see citing works
Evidence base update for psychosocial treatments for pediatric obsessive-compulsive disorder
Freeman, J., Garcia, A., Frank, H., Benito, K., Conelea, C., Walther, M., & Edmunds, J. (2014) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374416.2013.804386 · Cited by 139 · see citing works
An Overview of Translationally Informed Treatments for Posttraumatic Stress Disorder: Animal Models of Pavlovian Fear Conditioning to Human Clinical Trials
Bowers, M. E., & Ressler, K. J. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.008 · Cited by 147 · see citing works
Cannabinoid modulation of prefrontal–limbic activation during fear extinction learning and recall in humans
Rabinak, C. A., Angstadt, M., Lyons, M., Mori, S., Milad, M. R., Liberzon, I., & Phan, K. L. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.09.009 · Cited by 148 · see citing works
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REVIEW A Meta-Analysis of D-Cycloserine and the Facilitation of Fear Extinction and Exposure Therapy
Norberg, M. M., Krystal, J. H., & Tolin, D. F. (2013)
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Authors: Norberg, M. M., Krystal, J. H., & Tolin, D. F.
Affiliations: Yale University (US)
Corresponding author: Tolin, David F.
ORCID: Norberg, Melissa M.
Krystal, John H.
Tolin, David F.
Venue: Biological Psychiatry
Publisher: Elsevier BV
Published: 2008-06
Volume: 63
Issue: 12
Pages: 1118-1126
ISSN: 0006-3223 (ISSN-L)
DOI: 10.1016/j.biopsych.2008.01.012
OpenAlex: W2159630298
Cited by: 510
References: 121
Citations by year: 2026: 10 · 2025: 9 · 2024: 8 · 2023: 8 · 2022: 15 · 2021: 13 · 2020: 12 · 2019: 16 · 2018: 28 · 2017: 28 · 2016: 23 · 2015: 50 · 2014: 37 · 2013: 53 · 2012: 51
FWCI: 3.80
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Biological Psychiatry (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
Keywords: D-cycloserine, fear extinction, exposure therapy, NMDA receptor agonist, anxiety disorders, fear memory consolidation, neuroplasticity, augmentation therapy, translational research
MeSH terms: Animals, Anxiety Disorders, Combined Modality Therapy, Cycloserine, Desensitization, Psychologic, Extinction, Psychological, Fear, Humans, Implosive Therapy, Neuronal Plasticity, Receptors, N-Methyl-D-Aspartate, Treatment Outcome

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A meta-analysis of D-cycloserine and the facilitation of fear extinction and exposure therapy

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