Andrew Holmes, Ph.D., Laboratory Chief, Principal Investigator
Laboratory of Behavioral and Genomic Neuroscience
National Institute on Alcohol Abuse and Alcoholism
5625 Fishers Lane, Room 2N09
Rockville MD 20852-9411
e-mail: holmesan@mail.nih.gov
telephone: +1 301 402 3519
fax: +1 301 480 1952 

 

Mission Statement

The mission of the Laboratory of Behavioral and Genomic Neuroscience is to contribute to a deeper understanding of the causes of alcoholism and comorbid neuropsychiatric conditions such as mood and anxiety disorders.  Our goal is to help identify new directions for the prevention and effective treatment of these devastating diseases. To this end, we are using models of chronic alcohol exposure and chronic stress to examine how these environmental insults reshape brain circuits to modify behavior, and why they do so in a manner that varies greatly from individual to individual as a function of genetics, sex and age.  A major current focus of our work is how alcohol and stress affect the structure and function of circuits interconnecting the prefrontal cortex with limbic and dorsal striatal regions that are critical for the regulation of emotion, cognition and executive control over drug-seeking.

 

Ten recent key publications

DePoy CL, Daut R, Brigman J, MacPherson KP, Crowley N, Gunduz-Cinar O, Pickens C, Cinar R, Saksida L, Kunos G, Lovinger D, Bussey TJ, Camp MC, Holmes A  (2013) Chronic alcohol produces neuroadaptations to prime learning. Proceedings of the National Academy of Sciences, USA 110:14738-14788 (Covered by various media, e.g., http://www.huffingtonpost.com/2013/08/22/brain-alcohol-behavior-control_n_3796813.html, Highlighted ‘In This Issue’ http://www.pnas.org/content/110/36/14505.full)

Griebel G, Holmes A (2013) 50 years of hurdles and hope in anxiolytic drug discovery.  Nature Reviews Drug Discovery 12:667-687 Pubmed

Holmes A, Singewald (2013) Individual differences in recovery from traumatic fear.  Trends in Neuroscience 36:23-31 Pubmed

Brigman JL, Daut RA, Wright T, Gunduz-Cinar O, Graybeal C, Davis MI, Jiang Z, Saksida LM, Jinde S, Pease M, Bussey TJ, Lovinger DM, Nakazawa K, Holmes A (2013) GluN2B in corticostriatal circuits governs choice learning and choice shifting.  Nature Neuroscience 16:1101-1110.  Pubmed  http://neurosciencenews.com/neurology-learning-addiction-behavior-alteration-294

Gunduz-Cinar O, MacPherson KP, Cinar R, Gamble-George J, Sugden K, Williams B, Ramikie TS, Gorka AX, Makriyannis A, Poulton R, Patel S, Hariri AR, Caspi A, Moffitt TE, Kunos G, Holmes A (2013) Convergent translational evidence of a role for anandamide in amygdala-mediated fear extinction, threat processing and stress-reactivity.  Molecular Psychiatry 18:813-823  (Covered by MSNBC, Yahoo News and other media, http://in.news.yahoo.com/altering-brain-chemistry-may-help-overcome-fear-more-073119888.html).  (Faculty 1000 2x ‘must read’ http://f1000.com/717948500)

Holmes A, Fitzgerald PJ, MacPherson K, DeBrouse L, Colacicco G, Flynn S, Masneuf S, Pleil KE, Li C, Marcinkiewcz CA, Kash TL, Gunduz-Cinar O, Camp M (2012) Chronic alcohol remodels prefrontal neurons and disrupts NMDA receptor-mediated fear extinction encoding. Nature Neuroscience 15:1359-1361 (Covered by media, e.g., http://now.msn.com/heavy-drinking-rewires-brains-and-increases-suspectibility-to-ptsd). (Faculty 1000 ‘must read’ http://f1000.com/717956468).

Graybeal C, Schulman E, Saksida LM, Bussey TJ, Feyder M, Holmes A (2011) Paradoxical reversal learning enhancement by stress or prefrontal cortical damage: rescue with BDNF.  Nature Neuroscience 14:1507-1509. Pubmed (Faculty 1000 ‘recommended’ paper http://f1000.com/13405009)

Caspi A, Moffit TE, Holmes A, Hariri AR (2010) Gene x environment studies in psychiatry. American Journal of Psychiatry 167:509-527. Pubmed

Mozhui K, Karlsson RM, Kash TL, Ihne J, Norcross M, Fitzgerald PF , Patel S, Camp M, Cameron HA, Ciobanu DC, Winder DG, Williams RW, Holmes A (2010) Neuronal and molecular correlates of trait and stress-induced variation in anxiety-like behavior between mouse strains. The Journal of Neuroscience 30:5357-5367. Pubmed

Brigman JL, Wright T, Talani G, Prasad-Mulcare S, Jinde S, Seabold GK, Mathur P, Davis MI, Bock R,. Alvarez VA, Nakazawa K, Delpire E, Lovinger DM, Holmes A. (2010) Deletion of NR2B-containing NMDA receptors in corticohippocampal principle neurons impairs long-term depression and learning. The Journal of Neuroscience 30:4590-4600. Pubmed (Press release: http://www.niaaa.nih.gov/news-events/news-releases/brain-circuits-learning-decision-making)

 

Current staff

Elizabeth Kirby; Lab Manager; kirbye@mail.nih.gov

 

Hadley Bergstrom, PhD, Post-doctoral fellow
Hadley.Bergstrom@nih.gov
Current projects: Neural circuits of higher-order cognition

 Photo of Hadley Bergstrom, PhD

 

Olena Bukalo, PhD, Post-doctoral fellow
bukalool@mail.nih.gov
Current projects: Optogenetic control of behavior

Photo of Olena Bukalo

 

Ozge Gunduz-Cinar, PhD, Post-doctoral fellow
ozge.gunduzcinar@nih.gov
Current projects: Endocannabinoids in fear inhibition

Ozge Gunduz-Cinar, PhD, Post-doctoral fellow

 

Lindsay Halladay, PhD, Post-doctoral fellow
Lindsay.Halladay@nih.gov
Current projects: Reward processing in the amygdala following chronic ethanol exposure

Photo of Lindsay Halladay, PhD

 

Nick Jury, PhD, Post-doctoral fellow
Nick.Jury@nih.gov
Current projects: Alcohol exposure in females and adolescents

   Photos of Nick Jury

 

Katie Kaugars, BS, Post-baccalaureate
Katie.Kaugars@nih.gov 
Current projects: Optogenetic control of behavior
Photo of Katie Kaugers

 

Courtney Pinard, PhD, Post-doctoral fellow
courtney.pinard@nih.gov
Current projects: Neural circuits of fear and addiction

  Photo of Courtney Pinard, PhD, Post-doctoral fellow

 

Anna Radke, PhD, Post-doctoral fellow
anna.radke@nih.gov
Current projects: Neural mechanisms of addictive behaviors

Anna Radke, PhD, Post-doctoral fellow   

Maxine Reger, PhD, Post-doctoral fellow
maxine.reger@nih.gov
Current projects: Rodent models of anxiety disorders following traumatic brain injury.  Optogenetic control of fear learning and memory. 

Maxine Reger, PhD, Post-doctoral fellow

 

  

Section alumni

Erica Busch, BAcurrently at Kings College London

Erica Sagalyn, BA, currently at the University of Pennsylvania

Charles Pickens, PhD, currently Assistant Professor, Department of Psychology, Kansas State University

Shaun Flynn, BS, currently at Drexel University

Munisa Bachu, BA

Marguerite Camp, BS, currently Senior Associate at PriceWaterhouseCoopers

Sophie Masneuf, PhD

Giovanni Colacicco, MD, PhD, currently Senior Scientist and Senior Lecturer, Institute of Anatomy, University of Zurich

Rachel Daut, BS, currently at University of Colorado at Boulder

Carly Kiselycznyk, PhD, currently at Yale University

Paul Fitzgerald, PhD, currently at Texas A&M University

Carolyn Graybeal, PhD, currently a fellow at the National Academy of Sciences

Jonathan Brigman, PhD, currently Assistant Professor, Department of Neurosciences, University of New Mexico JBrigman@Salud.UNM.edu

Lauren DeBrouse, BS, currently at Emory University

Kathryn MacPherson, BS, currently at Emory University

Daniel Fisher, BS, currently at Northwestern University

Aaron Plitt, BS, currently at University of Texas Southwestern

Alicia Izquierdo, PhD, currently Assistant Professor, Department of Psychology, California State University, Los Angeles AIzquie@calstatela.edu

Janel Boyce-Rustay, PhD, currently Associate Research Pharmacologist, Abbott Laboratories

Rose-Marie Karlsson, PhD, currently at NIMH

Rachel Millstein, BA, currently at University California, San Diego

Lisa Wiedholz, BA, currently at Abbott Laboratories

Rebecca Yang, BA, currently at The Mayo Clinic Rochester

Kathryn Hefner, BA , currently at University Wisconsin-Madison

Poonam Mathur, BA, currently at Nova Southeastern University

Benjamin Palachick, BS, currently at Drexel University

Yi-Chyan Chen, MD, PhD, currently Director, Department of Psychiatry, Buddhist Tzu Chi General Hospital, Hualian, Taiwan

Maxine Norcross, BS, currently at NIMH

Tara Wright, BS, currently at University of North Carolina

Michael Feyder, BS, currently at the Karolinska Insitute

Jessica Ihne, BS, currently at Georgetown University

Susanna Weber, BS, currently at Gottingen University

Lauren Lederle, BS, currently at UCSF

Benita Hurd, BS, currently at Howard University

 

Collaborators

Dr. Timothy J. Bussey and Dr. Lisa M. Saksida, Department of Experimental Psychology, University of Cambridge; Weblink

Dr. Tom Kash, University of North Carolina; Weblink

Dr. David Lovinger, Dr. Rui Costa, Dr. Veronica Alvarez, Dr. Margaret Davis, Laboratory for Integrative Neuroscience, NIAAA; Weblink

Dr. Sachin Patel, Vanderbilt University Medical Center; Weblink

Dr. Cara Wellman, Department of Psychology, Indiana University; Weblink

Dr. Danny Winder, Department of Pharmacology, Vanderbilt University Medical Center; Weblink

 

Additional publications

Graybeal C, Bachu M, Mozhui K, Saksida LM, Bussey TJ, Sagalyn E, Williams RW, Holmes A (2014) Strains and stressors: an analysis of touchscreen learning in genetically diverse mouse strains.  PLoS One.  9:e87745. Pubmed.

Radke AK, Pickens CL, Holmes A (2014) “Stress and Alcohol-Drinking Behavior.”  Chapter in Neurobiology of Alcohol Dependence.  6:97-105.

Daut RA, Busch EF, Ihne J, Fisher D, Mishina M, Grant S, Camp M, Holmes A (in press) Tolerance to ethanol intoxication after chronic ethanol: role of GluN2A and PSD-95.  Addiction Biology. Pubmed.

Fitzgerald PJ, Whittle N, Flynn SM, Graybeal C, Pinard C, Gunduz-Cinar O, Kravitz A, Singewald N, Holmes A (in press) Pre-frontal single unit firing associated with deficient extinction in mice.  Neurobiology of Learning and Memory.  Pubmed

Wellman CL, Camp M, Jones VM, Macpherson KP, Ihne J, Fitzgerald P, Maroun M, Drabant E, Bogdan R, Hariri AR, Holmes A (2013) Convergent effects of mouse Pet-1 deletion and human PET-1 variation on amygdala fear and threat processing.  Experimental Neurology.  Pubmed

Horner AE, Heath CJ, Hvoslef-Eide M, Kent BA, Kim CH, Nilsson SR, Alsiö J, Oomen CA, Holmes A, Saksida LM, Bussey TJ (in press) The touchscreen operant platform for testing learning and memory in rats and mice.  Nature Protocols.  Pubmed

Mar AC, Horner AE, Nilsson S, Alsiö J, Kent BA, Kim CH, Holmes A, Saksida LM, Bussey TJ (in press) The touchscreen operant platform for assessing executive function in rats and mice.  Nature Protocols.

Gunduz-Cinar O, Hill MN, McEwen BS, Holmes A (in press) Amygdala FAAH and anandamide: mediating protection and recovery from stress.  Trends in Pharmacological Sciences. Covered by NPR News: "Could Pot Help Veterans With PTSD?  Brain Scientists Say Maybe” 

Holmes A, Spanagel R, Krystal JH (in press) Glutamatergic targets for new alcohol medications.  Psychopharmacology Pubmed

Maroun M, Ioannides PJ, Bergman KL, Kavushansky A, Holmes A, Wellman CL (2013)  Fear extinction deficits following acute stress associated with increased spine density and dendritic retraction in basolateral amygdala neurons.  European Journal of Neuroscience.  [Epub ahead of print]. Pubmed

Macpherson K, Whittle N, Camp M, Gunduz-Cinar O, Singewald N, Holmes A (2013) Temporal factors in the extinction of fear in inbred mouse strains differing in extinction efficacy.  Biology of Mood & Anxiety Disorders 3:13. Pubmed

Holmes A, Singewald N (2013) Individual differences in recovery from traumatic fear. Trends in Neurosciences 36:23-31. Pubmed

Kiselycznyk C, Zhang X, Huganir R, Holmes A, Svenningsson, P. (in press) Reduced phosphorylation of GluA1 subunits relates to anxiety-like behaviours in mice. International Journal of Neuropsychopharmacology Pubmed

Debrouse L, Hurd B, Kiselycznyk C, Plitt A, Todaro A, Mishina M, Grant SG, Camp M, Gunduz-Cinar O, Holmes A (2012-Epub ahead of print) Probing the modulation of acute ethanol intoxication by pharmacological manipulation of the NMDAR glycine co-agonist site. Alcoholism: Clinical and Experimental Research. Pubmed

Whittle N, Schmuckermair C, Gunduz Cinar O, Hauschild M, Ferraguti F, Holmes A, Singewald N (2013) Deep brain stimulation, histone deacetylase inhibitors and glutamatergic drugs rescue resistance to fear extinction in a genetic mouse model. Neuropharmacology. 64:414-423. Pubmed

Bussey TJ, Holmes A, Lyon L, Mar AC, McAllister K, Nithianantharajah J, Oomen CA, Saksida LM (2012) New translational assays for preclinical modelling of cognition in schizophrenia: the touchscreen testing method for mice and rats. Neuropharmacology 62:1191-1203. Pubmed

Graybeal C, Kiselycznyk C, Holmes A (2012) Stress-induced impairments in prefrontal-mediated behaviors and the role of the N-methyl-D-aspartate receptor.  Neuroscience 211:28-38. Pubmed

Karlsson RM, Adermark L, Molander A, Pereau-Lenz S, Singley E, Solomon M, Holmes A, Tanaka K, Lovinger DM, Spanagel R, Heilig M (2012) Reduced alcohol intake, lack of alcohol reward and impaired endocannabinoid signaling in mice with a deletion of the glutamate transporter GLAST. Neuropharmacology 63:181-189. Pubmed

Chesler EJ, Plitt A, Fisher D, Hurd B, Lederle L, Kiselycznyk C, Holmes A (2012) Quantitative trait loci for sensitivity to ethanol intoxication in a C57BL/6Jx129S1/SvImJ inbred mouse cross.  Mammalian Genome 23:305-321. Pubmed

Maroun M, Kavushansky A, Holmes A, Wellman C, Motanis H (2012) Enhanced extinction of aversive memories by high-frequency stimulation of the rat infralimbic cortex. PLoS One. 7:e35853. Pubmed

Hartley CA, McKenna MC, Salman R, Holmes A, Casey BJ, Phelps EA, Glatt CE (2012) Serotonin transporter polyadenylation polymorphism modulates the retention of fear extinction memory. Proceedings of the National Academy of Sciences, USA 109:5493-5498. Pubmed

Kiselycznyk C, Hoffman D, Holmes A (2012) Effects of genetic deletion of the Kv4.2 voltage-gated potassium channel on murine anxiety-, fear- and stress-related behaviors. Biology of Mood and Anxiety Disorders 2:5. Pubmed

Ihne J, Fitzgerald PF, Hefner K, Holmes A (2012) Pharmacological manipulation of stress-induced C57BL/6J anxiety-related behavior. Neuropharmacology 62:464-473 Pubmed

Camp MC, Macpherson KP, Lederle L, Graybeal C, Gaburro S, Debrouse LM, Ihne JL, Bravo JA, O'Connor RM, Ciocchi S, Wellman CL, Lüthi A, Cryan JF, Singewald N, Holmes A (2012) Genetic strain differences in learned fear inhibition associated with variation in neuroendocrine, autonomic, and amygdala dendritic phenotypes. Neuropsychopharmacology 37:1534-1547. Pubmed (Faculty 1000 ‘exceptional’ paper http://f1000.com/14267267).

Barkus C, Feyder M, Graybeal C, Wright T, Wiedholz L, Izquierdo A, Kiselycznyk C, Schmitt W, Sanderson DJ, Rawlins JN, Saksida LM, Bussey TJ, Sprengel R, Bannerman D, Holmes A (2012) Do GluA1 knockout mice exhibit behavioral abnormalities relevant to the negative or cognitive symptoms of schizophrenia and schizoaffective disorder? Neuropharmacology 62:1263-1272. Pubmed

Kiselycznyk C, Svenningsson P, Delpire E, Holmes A (2011) Genetic, pharmacological and lesion analyses reveal a selective role for corticohippocampal GLUN2B in a novel repeated swim stress paradigm. Neuroscience 193:259-268. Pubmed

Camp M, Feyder M, Ihne J, Palachick B, Hurd B, Chen Y-C, Coba MP, Grant SGN, Holmes A (2011) A novel role for PSD-95 in mediating ethanol intoxication, drinking and place preference.  Addiction Biology 16:428-439. Pubmed

Lederle L, Weber S, Wright T, Feyder M, Brigman JL, Crombag H, Saksida LM, Bussey TJ, Holmes A (2011) Reward-related behavioral paradigms for addiction research in the mouse: performance of common inbred strains. PLoS One 6: e15536. Pubmed

Holmes A, Quirk GJ (2010) Pharmacological facilitation of fear extinction and the search for adjunct treatments for anxiety disorders - the case of yohimbine. Trends in Pharmacological Sciences 31:2-7. Pubmed

Holmes A, Wellman CL (2010) Stress-induced prefrontal reorganization and executive dysfunction. Neuroscience & Biobehavioral Reviews 33:773-783. Pubmed

Feyder M, Karlsson RM, Mathur P, Lyman M, Bock R, Momenan R, Munasinghe J, Scattoni ML, Ihne J, Camp M, Graybeal C, Strathdee D, Begg A, Alvarez VA, Kirsch P, Rietschel M, Cichon S, Walter H, Meyer-Lindenberg A, Grant SG, Holmes A (2010) Association of mouse Dlg4 (PSD-95) gene deletion and human DLG4 gene variation with phenotypes relevant to autism spectrum disorders and Williams' syndrome. American Journal of Psychiatry 167:1508-1517. Pubmed

Baganz N, Horton R, Martin K, Holmes A, Daws LC (2010) Repeated swim impairs serotonin clearance via a corticosterone-sensitive mechanism: organic cation transporter 3, the smoking gun. Journal of Neuroscience 30:15185-15195. Pubmed

Fitzgerald PJ, Barkus C, Feyder M, Wiedholz LM, Chen YC, Karlsson RM, Machado-Vieira R, Graybeal C, Sharp T, Zarate C, Harvey-White J, Du J, Sprengel R, Gass P, Bannerman D, Holmes A. (2010) Does gene deletion of AMPA GluA1 phenocopy features of schizoaffective disorder? Neurobiology of Disease 40:608-21. Pubmed

Whittle N, Hauschild M, Lubec G, Holmes A, Singewald N (2010) Rescue of impaired fear extinction and normalization of cortico-amygdala circuit dysfunction in a genetic mouse model by dietary zinc restriction. Journal of Neuroscience 30:13586-13596. Pubmed

Brigman J, Harvey-White J, Izquierdo A, Saksida LM, Bussey TJ, Murphy DL, Deneris E, Holmes A (2010) Pharmacological or genetic inactivation of the serotonin transporter improves reward-based cognitive flexibility on a mouse touchscreen-based assay. Cerebral Cortex 20:1955-1963. Pubmed

Fraser L, Brown RE, Hussin A, Fontana M, Whittaker A, O’Leary T, Lederle L, Holmes A, Ramos A (2010) Measuring locomotion and anxiety-related behaviours in mice: a new way of using old models. Psychopharmacology 211:99-112. Pubmed

Feyder M, Camp MC, Holmes A, Chen Y-C (2010) Ethanol and NMDA receptor interactions: Implications for pharmacotherapeutic treatments. Journal of Medical Sciences 30:3-10. Journal Website

Camp M, Norcross M, Whittle N, Feyder M, D’Hanis W, Yilmazer-Hanke D, Singewald N, Holmes A (2009) Impaired Pavlovian fear extinction is common across genetic lineages of the 129 inbred mouse strain. Genes, Brain & Behavior 8:744-752. Pubmed

Karlsson RM, Tanaka K, Saksida LM, Bussey TJ, Heilig M, Holmes A (2009) Assessment of glutamate transporter GLAST (EAAT1)-deficient mice for phenotypes relevant to the negative and executive/cognitive symptoms of schizophrenia. Neuropsychopharmacology 34:1578-1589. Pubmed

Zhou R, Holmes A, Du J, Malkesman O, Yuan P, Wang Y, Damschroder-Williams P, Chen G, Guitart X, Manji HK (2009) Genome-wide gene expression profiling in GluR1 knockout mice: Key role of the calcium signaling pathway in glutamatergically-mediated hippocampal transmission. European Journal of Neuroscience 30:2318-2326. Pubmed

Holmes A (2008) Genetic variation in cortico-amygdala serotonin function and risk for stress-related disease. Neuroscience & Biobehavioral Reviews 32:1293-1314. Pubmed

Karlsson RM, Tanaka K, Heilig M, Holmes A (2008) Loss of glial glutamate and aspartate transporter (excitatory amino acid transporter 1) causes locomotor hyperactivity and exaggerated responses to psychotomimetics: rescue by haloperidol and metabotropic glutamate 2/3 agonist. Biological  Psychiatry. 64:810-814. Pubmed (For example of media coverage of this article, see http://www.sciencedaily.com/releases/2008/10/081027115427.htm ).

Witkiewitz K, Holmes A, Ray LA, Murphy LG, Richardson HN, Chen YC, McDevitt-Murphy ME, Cruz MT, Roberto M (2009) Young investigator award symposium. Alcohol 43:499-508 Pubmed

Hefner K, Whittle N, Juhasz J, Norcross M, Karlsson RM, Saksida LM, Bussey TJ, Singewald N, Holmes A (2008) Impaired fear extinction learning and cortico-amygdala circuit abnormalities in a common genetic mouse strain. Journal of Neuroscience. 28:8074-8085. Pubmed  (Journal Club Article : Sotres-Bayon F, Corcoran KA, Peters J, Sierra-Mercado D (2008) Neural correlates of individual variability in fear extinction. The Journal of Neuroscience 28:1-3. Pubmed).

Wiedholz LM, Owens WA, Horton RE, Feyder M, Hefner KR, Sprengel R, Celikel T, Daws LC, Holmes A (2008) Mice lacking the AMPA GluR1 receptor exhibit hyperdopaminergia and schizophrenia-related behaviors. Molecular Psychiatry 13:631-640. Pubmed . (Commentary: Fisher Y, Andre VM, Cepeda C, Levine MS (2008) Dopamine-glutamate interactions at the forefront of schizophrenia research. Cell Science Reviews 5:7-16 Journal website ).

Chen YC, Holmes A (2008) Effects of topiramate and other anti-glutamatergic drugs on the negative intoxicating actions of ethanol in mice: modulation by genetic strain and stress. Neuropsychopharmacology 34:1454-1466. Pubmed

Crusio WE, Goldowitz D, Holmes A, Wolfer D (2008) Standards for the publication of mouse mutant studies. Genes, Brain & Behavior 8:1-4. Pubmed

Murphy, DL, Fox MA, Timpano KR, Moya P, Ren-Patterson R, Andrews A, Holmes, A, Watts SW, Wendland J, Lesch KP (2008) How the serotonin story is being rewritten by new gene-based discoveries principally related to SLC6A4, the serotonin transporter gene, whose functions influence the entire serotonin system. Neuropharmacology 55:932-960 . Pubmed

Mathur P, Graybeal C, Feyder M, Holmes A (2008) Effects of systemic treatment with the NMDA NR2B subunit antagonist, Ro 25-6981, on mouse fear memory: attenuation with ageing. Pharmacology, Biochemistry & Behavior 91:453-460 . Pubmed

Brigman J, Feyder M, Saksida LM, Bussey TJ, Mishina M, Holmes A (2008) Impaired discrimination learning in mice lacking the NMDA receptor NR2A subunit. Learning and Memory 15:50-54. Pubmed

Davis AR, Shields AD, Brigman J, Norcross M, McElligott ZA, Holmes A, Winder DG (2008) Alpha2-adrenergic receptor regulation of extinction of cocaine conditioned place-preference. Learning and Memory 15:667-676. Pubmed

Fegley DB, Holmes A, Riordan T, Faber CA, Weiss JR, Ma S, Sleeman M, Usdin TB (2008) Regulation of anxiety and fear by tuberoinfundibular peptide of 39 residues. Genes, Brain & Behavior 7:933-942. Pubmed

Brigman J, Mathur P, Lu L, Williams RW, Holmes A (2008) Genetic relationship between fear- and anxiety-related behaviors in BXD recombinant inbred mice. Behavioural Pharmacology 20:204-209. Pubmed

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. Pubmed

Boyce-Rustay JM, Palachick B, Hefner KM, Chen YC, Karlsson RM, Millstein RA, Harvey-White J, Holmes A (2008) Desipramine potentiation of the acute depressant effects of ethanol: modulation by alpha2-adrenoreceptors and stress. Neuropharmacology 55:803-811. Pubmed

Karlsson RM, Hefner KM, Sibley DR, Holmes A (2008) Constitutive loss of dopamine D1, but not D5, receptor prevents locomotor sensitization to cocaine in mice. Psychopharmacology 200:117-127. Pubmed

Norcross M, Mathur P, Enoch AJ, Karlsson RM, Brigman JL, Cameron HA, Harvey-White J, Holmes A (2008) Effects of adolescent fluoxetine treatment on fear-, anxiety- or stress-related behaviors in C57BL/6J or BALB/cJ mice. Psychopharmacology 200:413-424. Pubmed

Parker CC, Ponicsan H, Spencer RL, Holmes A, Johnson TE (2008) Restraint stress and exogenous corticosterone differentially alter sensitivity to the sedative-hypnotic effects of ethanol in ILS and ISS mice. Alcohol 42:477-485. Pubmed

Adamec RA, Holmes A, Blundell J (2008) Vulnerability to lasting anxiogenic effects of brief exposure to predator stimuli: sex, serotonin and other factors - relevance to PTSD. Neuroscience & Biobehavioral Reviews 32:1287-1292. Pubmed

Palachick B, Chen Y-C, Enoch AJ, Karlsson RM, Sprengel R, Mishina M, Holmes A (2008) MK-801 potentiation of ethanol intoxication is not dependent upon major NMDAR or AMPA receptor subunits. Alcoholism: Clinical and Experimental Research 32:1479-1492. Pubmed

Feyder M, Wiedholz LM, Sprengel R, Holmes A (2008) Impaired associative fear learning following complete or partial loss of AMPA GluR1 receptors in mice. Frontiers in Behavioral Neuroscience 1:4. Journal website

Fox MA, Andrews AM, Wendland JR, Lesch KP, Holmes A, Murphy DL (2007) A pharmacological analysis of mice with a targeted disruption of the serotonin transporter. Psychopharmacology 195:147-166. Pubmed

Tonelli LH, Holmes A, Postlache TT (2008) Intranasal immune challenge induces sex-dependent depressive-like behavior and cytokine expression in the brain. Neuropsychopharmacology 33:1038-1048. Pubmed

Karlsson RM, Holmes A, Crawley, JN, Heilig, MA (2008) The neuropeptide Y Y1 receptor subtype is necessary for the anxiolytic-like but not antidepressant-like effects of neuropeptide Y. Psychopharmacology 195:547-557. Pubmed

Boyce-Rustay JM, Janos A, Holmes A (2008) Effects of chronic swim stress on EtOH-related behaviors in C57BL/6J, DBA/2J and BALB/cByJ mice. Behavioural Brain Research 188:133-137. Pubmed

Hefner KM, Holmes A (2007) Short-term and long-term effects of exposure to an unfamiliar male in C57BL/6J mice. Behavioural Brain Research 182:344-348. Pubmed

Holmes A, Stein, MB, Steckler T (2008) Modeling anxiety in mice. In Animal and translational models of psychiatric disorders. RA McArthur and F Borsini (Eds). Elsevier, London.

Hefner KM, Holmes A (2007) an investigation of the behavioral effects of ethanol across adolescence in mice. Psychopharmacology 191:311-322. Pubmed

Hasnie FS, Wallace VC, Hefner K, Holmes A, Rice AS (2007). Mechanical and cold hypersensitivity in nerve-injured C57BL/6J mice is not associated with fear-avoidance- and depression-related behaviour. British Journal of Anaesthesia 98:816-822. Pubmed

Boyce-Rustay JM, Cameron HA, Holmes A (2007) Chronic swim stress alters sensitivity to acute behavioral effects of ethanol in mice. Physiology & Behavior, 91:77-86. Pubmed

Fisch GS, Holmes A (2007) Recent developments in the use of animal models of psychiatric disease. Behavior Genetics 37:259-263. Pubmed

Holmes A (2007) The pharmacology of anxiolysis. In Handbook of Anxiety and Fear. R Blanchard, DC Blanchard, DJ Nutt (Eds). Elsevier, London.

Hefner KM, Holmes A (2007) Short-term and long-term effects of exposure to an unfamiliar male in C57BL/6J mice. Behavioural Brain Research, 191:311-322. Pubmed

Holmes A (2007) Mouse models of anxiety. In Handbook of Behavioral Genetics of the Mouse. WE Crusio, F Sluyter, RT Gerlai (Eds). Cambridge University Press, Cambridge.

Mozhui K, Hamre K, Holmes A, Lu L, Williams RW (2007) Genetic and structural analysis of the mouse basolateral amygdala complex. Behavior Genetics, 37:223-243. Pubmed

Carroll J, Boyce-Rustay JM, Izquierdo A, Millstein RA, Yang RJ, Wiedholz LM, Murphy DL, Holmes A (2007) Effects of mild early life stress on abnormal emotional behaviors in 5-HTT knockout mice. Behavior Genetics, 37:214-222. Pubmed

Hefner KM, Holmes A (2007) Ontogeny of fear-, anxiety- and depression-related behavior across mouse adolescence. Behavioral Brain Research 176:210-215. Pubmed

Millstein RA, Holmes A (2007) Effects of repeated maternal separation on anxiety- and depression-related phenotypes in different mouse strains. Neuroscience & Biobehavioral Reviews 31:3-17. Pubmed

Caldwell HK, Stewart S, Wiedholz LM, Millstein RA, Holmes A, Young SW, Wersinger S (2007) The acute intoxicating effects of ethanol are not dependent on the vasopressin 1a or 1b receptors. Neuropeptides 40:325-337. Pubmed

Wellman CL, Izquierdo A, Garrett JE, Martin KP, Carroll J, Millstein RA, Lesch K-P, Murphy DL, Holmes A (2007) Impaired stress-coping and fear extinction and abnormal corticolimbic morphology in serotonin transporter knockout mice. The Journal of Neuroscience 27:684-691. Pubmed

Holmes A, Cryan JF (2006) Measuring anxiety- and depression-related behaviors in the mouse. In Transgenic and Knockout Models of Neuropsychiatric Disorders. GS Fisch and J Flint (Eds). Humana Press, New Jersey.

Boyce-Rustay JM, Holmes A (2006) Ethanol-related behaviors in mice lacking the NMDA receptor NR2A subunit. Psychopharmacology 187:455-466. Pubmed

Izquierdo A, Wellman CL, Holmes A (2006) Stress causes rapid dendritic retraction in infralimbic cortex and impairs fear extinction in mice. The Journal of Neuroscience 26:5733-5738. Pubmed

Hariri AR, Holmes A (2006) Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends in Cognitive Sciences 10:182-191. Pubmed

Boyce-Rustay JM, Wiedholz LM, Millstein RA, Carroll J, Murphy DL, Daws LC, Holmes A (2006) Behavioral responses to ethanol in serotonin transporter knockout mice. Alcohol: Clinical and Experimental Research 30:1957-1965. Pubmed

Wrenn CC, Holmes A (2006) Galanin; a novel target for stress-related disorders. Drug News and Perspectives, 26:753-778. Pubmed

Holmes A, Picciotto M (2006) Galanin; a novel target system for stress-related disorders and addiction? Current Drug Targets – CNS & Neurological Disorders 5:225-232. Pubmed

Boyce-Rustay JM, Holmes A (2006) Genetic inactivation of the NMDA NR2A subunit has anxiolytic- and antidepressant-like effects in mice. Neuropsychopharmacology, 31:2405-1414. Pubmed

Ren-Patterson R, Cochran LW, Holmes A, Lesch K-P, Lu B, Murphy DL (2006) Gender-dependent modulation of brain monoamines and anxiety-like behaviors in mice with genetic serotonin transporter and BDNF deficiencies. Molecular and Cellular Biology 26:753-778. Pubmed

Karlsson R, Holmes A (2006) Galanin; a modulator of stress and emotion. Amino Acids, 31:231-239. Pubmed

Millstein RA, Ralph RJ, Yang RJ, Holmes A (2006) Effects of repeated maternal separation on prepulse inhibition of startle across inbred mouse strains. Genes, Brain & Behavior 5:346-354. Pubmed

Izquierdo A, Wiedholz LM, Millstein, RA, Yang, RJ, Bussey TJ, Saksida LM, Holmes A (2006) Genetic and dopaminergic modulation of reversal learning in a touchscreen-based operant procedure for mice. Behavioral Brain Research, 171:181-188. Pubmed

Daws LC, Montañez S, Munn JL, Owens WA, Baganz NL, Boyce-Rustay JM, Millstein RA, Wiedholz LM, Murphy DL, Holmes A (2006) Ethanol inhibits clearance of brain serotonin by a serotonin transporter-independent mechanism. The Journal of Neuroscience 26:6431-6438. Pubmed . (News Highlight: McGown D (2006) Neurophysiology: Under the influence. Nature Reviews Neuroscience 7:593 Journal website ).

Adamec, RA, Burton, P, Blundell, J, Murphy, DL, Holmes A (2006) Vulnerability to mild predator stress in serotonin transporter knockout mice. Behavioral Brain Research 170:126-140. Pubmed

Cryan, JF, Holmes A (2005) The ascent of mouse: advances in modeling human depression and anxiety. Nature Reviews Drug Discovery 4:775-790. Pubmed

Zhao S, Edwards J, Carroll J, Wiedholz L, Millstein RA, Murphy DL, Lanthorn TH, Holmes A (2005) Mutant mice reveal an essential functional role for the C-terminus of the 5-HT transporter. Neuroscience 140:321-334. Pubmed

Kim D-K, Tolliver TJ, Huang SJ, Martin BJ, Andrews AM, Wichems C, Holmes A, Lesch K-P, Murphy DL (2005) Altered serotonin synthesis, turnover and dynamic regulation regions of mice lacking the serotonin transporter. Neuropharmacology 49:798-810. Pubmed

Esaki T, Cook M, Shimoji K, Murphy DL, Sokoloff L, Holmes A (2005) Developmental disruption of serotonin transporter function impairs cerebral responses to whisker stimulation in mice. Proceedings of the National Academy of Sciences USA 102:5582-5587. Pubmed

Holmes A, le Guisquet AM, Vogel E, Millstein RA, Leman S, Belzung C (2005) Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neuroscience & Biobehavioral Reviews 29:1335-1346. Pubmed

Rustay NR, Wrenn CC, Kinney JW, Holmes A, Bailey KR, Sullivan T, Harris AP, Long KC, Saavedra MC, Starosta G, Innerfield CE, Yang RJ, Dreiling JL, Crawley JN (2005) Galanin impairs performance on learning and memory tasks: findings from galanin transgenic and GAL-R1 knockout mice. Neuropeptides 39:237-241. Pubmed

Boyce-Rustay JM, Holmes A (2005) Functional roles of NMDA receptor NR2A and NR2B subunits in the acute intoxicating effects of ethanol in mice. Synapse 56:222-225. Pubmed

Ren-Patterson RF, Cochran LW, Holmes A, Sherrill S, Huang S-J, Tolliver T, Lesch, K-P, Lu B, Murphy DL (2005) Loss of BDNF gene allele exacerbates brain monoamine deficiencies and increases stress abnormalities of serotonin transporter knockout mice. Journal of Neuroscience Research 79:756-771. Pubmed

Karlsson RM, Holmes A, Heilig M, Crawley JN (2005) Comparative profiles of centrally-administered neuropeptide Y and galanin in mouse tasks for fear and anxiety-related behaviors. Pharmacology, Biochemistry and Behavior 80:427-436. Pubmed

Holmes A, Li Q, Koenig EA, Gold E, Stephenson D, Yang RY, Crawley JN (2005) Phenotypic assessment of galanin modulation of the acute behavioral effects of antidepressants in mice. Psychopharmacology 178:276-285. Pubmed

Li Q, Holmes A, Ma L, Murphy DL (2004) Medial hypothalamic 5-HT1A receptors may be involved in the regulation of defensive behaviors, but not exploratory anxiety-like behaviors in mice. The Journal of Neuroscience 24:10868-10877. Pubmed

Holmes A, Lachowicz JE, Sibley DR (2004) Functional specificity of dopamine receptor subtypes; recent evidence from knockout mice. Neuropharmacology 47:1117-1134. Pubmed

Wrenn CC, Kinney JW, Marriott LK, Holmes A, Harris AP, Saavedra MC, Innerfield CE, Jacoby AS, Shine J, Wenk G, Iismaa TP, Crawley JN (2004) Learning and memory performance in GAL-R1 null mutant mice. European Journal of Neuroscience 19:1384-1396. Pubmed

Murphy DL, Ren-Patterson R, Holmes A, Hall FS, Uhl G (2003) Experimental gene interaction studies with mutant mice as models for human polygenic traits and disorders. Genes, Brain and Behavior 2:350-364. Pubmed

Holmes A, Yang RJ, Lesch KP, Crawley JN, Murphy DL (2003) Mice lacking the serotonin transporter exhibit 5-HT1A receptor-mediated abnormalities in anxiety-like and exploratory behavior. Neuropsychopharmacology 28:2077-2088. Pubmed

Holmes A, Rodgers RJ (2003) Prior exposure to the elevated plus-maze sensitizes mice to the acute behavioral effects of phenelzine and fluoxetine. European Journal of Pharmacology 459:221-230. Pubmed

Holmes A, Hariri AR (2003) Genetic variation in serotonin transporter function and negative emotionality; placing single gene effects in the context of genetic background and environment. Genes, Brain and Behavior 2:332-335. Pubmed

Holmes A, Kinney JW, Wrenn CC, Li Q, Yang RJ, Ma L, Vishwanath J, Saveedra MC, Innerfield CE, Jacoby AS, Shine J, Iismaa TP, Crawley JN (2003) Galanin GAL-R1 receptor null mutant mice display increased anxiety-like behavior specific to the elevated plus-maze test. Neuropsychopharmacology 28:1031-1044. Pubmed

Holmes A, Murphy DL, Crawley JN (2003) Abnormal behavioral phenotypes of serotonin transporter knockout mice; parallels with human anxiety and depression. Biological Psychiatry 54:953-959. Pubmed

Holmes A, Li Q, Murphy DL, Gold E, Crawley JN (2003) Abnormal anxiety-related behavior in serotonin transporter null mutant mice; the influence of genetic background. Genes, Brain and Behavior 2:365-380. Pubmed

Holmes A, Heilig M, Rupniak, NMJ, Steckler T, Griebel G (2003) Neuropeptides as novel therapeutic targets for stress-related disorders; recent developments. Trends in Pharmacological Sciences 24:580-558. Pubmed

Holmes A, Yang RJ, Crawley JN (2002) Evaluation of an anxiety-related phenotype in galanin overexpressing transgenic mice. Journal of Molecular Neuroscience 18:151-165. Pubmed

Wrenn CC, Marriott L, Kinney JW, Holmes A, Wenk G, Crawley JN (2002) Galanin peptide levels in hippocampus and cortex of galanin overexpressing transgenic mice evaluated for cognitive performance. Neuropeptides 36:413-426. Pubmed

Kinney JW, Starosta G, Holmes A, Wrenn CC, Yang RJ, Harris AP, Long KC, Crawley JN (2002) Deficits in trace cued fear conditioning in galanin-treated rats and galanin-overexpressing transgenic mice. Learning and Memory 9:178-190. Pubmed

Holmes A, Yang RJ, Crawley JN, Murphy DL (2002) Evaluation of antidepressant-related behavioral responses in mice lacking the serotonin transporter. Neuropsychopharmacology 27:914-923. Pubmed

Holmes A, Wrenn CC, Harris AP, Thayer K, Crawley JN (2002) Behavioral profiles of inbred strains on novel, olfactory, spatial and emotional tests for reference memory in mice. Genes, Brain and Behavior 1:55-69. Pubmed

Holmes A, Murphy DL, Crawley JN (2002) Reduced aggression in mice lacking the 5-HT transporter. Psychopharmacology 161:160-167. Pubmed

Williams RW, Dubnau J, Enoch MA, Flaherty L, Sluyter F, Gannon KS, Maxson SC, Riedl CAL, Williams KD, Holmes A, Bolivar VJ, Crusio WE (2002) Hot topics in behavioral and neural genetics. Genes, Brain and Behavior 2:117-130. Pubmed

Steiner RA, Hohmann JG, Holmes A, Wrenn CC, Cadd G, Jureus A, Clifton DK, Luo M, Gutshall M, Ma SY, Mufson EJ, Crawley JN (2001) Galanin overexpression provokes selective cognitive deficits and reduces cholinergic survival in a transgenic mouse model of Alzheimer's disease. Proceedings of the National Academy of Sciences USA 98:4184-4189. Pubmed

Holmes A, Iles JP, Mayell SJ, Rodgers RJ (2001) Prior test experience compromises the anxiolytic efficacy of chlordiazepoxide in the mouse light/dark exploration test. Behavioral Brain Research 122:159-167. Pubmed

Holmes A, Hollon TR, Liu Z, Sibley DR, Dreiling J, Gleason TC, Crawley JN (2001) Behavioral characterization of dopamine D5 receptor null mutant mice. Behavioral Neuroscience 115:1129-1144. Pubmed

Holmes A (2001) Transgenic and gene knockout approaches to the study of anxiety-like behavior in mice. Neuroscience & Biobehavioral Reviews 25:261-273. Pubmed

Holmes A, Crawley JN (2000) Promises and limitations of transgenic and knockout mice in modeling psychiatric symptoms. In Contemporary Issues in Modeling Psychopathology. M Myslobodsky and I Weiner (Eds). Kluwer, Boston.

Holmes A, Parmigiani S, Ferrari PF, Palanza PJ, Rodgers RJ (2000) Behavioral profile of wild mice in the elevated plus-maze test for anxiety. Physiology & Behavior 71:509-516. Pubmed

Rodgers RJ, Haller J, Holmes A, Halasz J, Walton T, Brain PF (1999) Corticosterone response to the plus-maze: high correlation with risk assessment in rats and mice. Physiology & Behavior 68:47-53. Pubmed

Holmes A, Rodgers RJ (1999) Influence of spatial and temporal manipulations on the anxiolytic efficacy of chlordiazepoxide in mice previously exposed to the elevated plus-maze. Neuroscience & Biobehavioral Reviews 23:971-980. Pubmed

Holmes A, Rodgers RJ (1998) Responses of Swiss-Webster mice to repeated plus-maze experience: further evidence for a qualitative shift in emotional state? Pharmacology, Biochemistry & Behavior 60:473-488. Pubmed

Rodgers RJ, Cao BJ, Dalvi A, Holmes A (1997) Animal models of anxiety: an ethological perspective. Brazilian Journal of Medical and Biological Research 30:289-304. Pubmed 

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