Wolf Lab

A microscopic image revealing a multitude of multicolored dots.

A major challenge in treating substance use disorder is that persons with this disorder remain vulnerable to drug craving and relapse even after long periods of abstinence. The goal of the Wolf lab is to understand synaptic plasticity in the nucleus accumbens and related circuits that underlies this persistent vulnerability. We use the ‘incubation of drug craving’ model in which cue-induced drug craving in rats progressively intensifies (incubates) over the first weeks of abstinence from drug self-administration and then remains high for months. This model has translational relevance because incubation of craving also occurs in humans. Our experiments involve electrophysiology, chemogenetics, fiber photometry, translating ribosome affinity purification, and behavioral assessments. Specific projects are described under Lab Members. The lab is supported by two R01 grants from NIDA.

A professional photo of Dr. Marina Wolf.

Marina E. Wolf, Ph.D., Principal Investigator

Marina Wolf has been a pioneer in studying the role of synaptic plasticity in the actions of drugs of abuse. She received her Ph.D. in Pharmacology from Yale in 1986 and trained as a postdoctoral fellow at the Center for Cell Biology, Sinai Hospital of Detroit. She was Assistant Professor of Psychiatry at Wayne State University before moving to the Chicago Medical School in 1992 where she rose through the ranks, serving as Chair of Neuroscience from 2003-2018. She moved to OHSU in 2018.  Her lab has been continuously supported by NIDA since 1992, with past awards including an R37 (Merit Award). Dr. Wolf was elected Fellow of the American Association for the Advancement of Science in 2017. She served as President of the American College of Neuropsychopharmacology in 2019 and was the 2022 recipient of the Julius Axelrod Prize from the Society for Neuroscience. She has also served on many NIH advisory committees and study sections. Dr. Wolf founded a company in 2021 to develop therapeutics to facilitate abstinence in persons recovering from stimulant use disorder.

Lab members

A photo of Eun-Kyung Hwang smiling while standing next to a microscope in a lab.

Eun-Kyung Hwang, Ph.D., Senior Research Associate

Eun-Kyung received her Ph.D. in neuroscience from Ewha Woman’s University in South Korea, where she focused on slice electrophysiology and conducted research on monoaminergic modulation of glutamatergic transmission in the rat lateral habenula. She did her postdoctoral research in Carl Lupica's Lab at NIDA in Baltimore, where she worked on the effects of chronic cannabinoid exposure (Δ9-THC) on brain reward circuits using cellular, circuit, and behavioral approaches. Eun-Kyung joined the Wolf Lab in 2020, examining pathway and cell type specific synaptic plasticity in nucleus accumbens in a rat model of relapse in drug addiction by combining electrophysiology, optogenetics, and behavioral experiments. During her free time, she enjoys traveling, spending time with her family and watching her baby girl grow up.

A professional photo of Alex Kawa with the cityscape of Portland seen behind him.

Alex B. Kawa, Ph.D., Postdoctoral Fellow

Alex received his B.S. at the University of Maryland and his Ph.D. at the University of Michigan. He joined the Wolf lab in 2018. Alex’s projects have been aimed at understanding the role of protein translation in incubation of cocaine craving. His postdoctoral NRSA work identified a role for the Integrated Stress Response in mediating a unique form of LTD that reverses incubation-associated plasticity and thereby reduces cocaine seeking. In an ongoing project, he has combined translating ribosome affinity purification (TRAP) and RNA-seq to investigate gene expression changes that may underlie incubation of cocaine craving. Most recently, with support from a K99 award, Alex is investigating the role that cholinergic interneurons of the striatum play in incubation of cocaine craving. Outside of lab, Alex enjoys exploring Portland’s restaurants and hiking with his wife and dog.

A professional photo of Hayley Kuhn.

Hayley M. Kuhn, Ph.D. student

Hayley received her B.S. in Neuroscience from Michigan State University in spring of 2022. At Michigan State, she worked in the Robison lab investigating how cocaine regulates gene expression in ventral hippocampal neurons that synapse onto nucleus accumbens (NAc) neurons, as well studying how lateral entorhinal cortex neurons that project to the NAc mediate drug seeking and reward. With a strong interest to continue substance abuse research, Hayley matriculated in fall of 2022 to the Behavioral and Systems Neuroscience Ph.D. Program at OHSU. In the Wolf lab, she is using slice electrophysiology to characterize mechanisms underlying incubation of oxycodone craving by examining pathway specific and cell type specific plasticity in the NAc core and shell subregions. During her free time, Hayley likes to explore the outdoors, work out, and cozy up with a good tv series and her cat.

A professional photo of Gillian Driscoll.

Gillian S. Driscoll, Ph.D. student

Gillian graduated from Hamilton College in 2021 with a B.A. in Neuroscience. After graduating, she joined Dr. Elena Chartoff’s lab as a research assistant, where she explored the role of projections from the paraventricular nucleus of the thalamus (PVT) to the nucleus accumbens (NAc) shell in oxycodone withdrawal-associated negative affective states, as well as sex differences in oxycodone self-administration and reinstatement. Gillian joined the Wolf lab in 2024 and plans to use fiber photometry and chemogenetics to explore the role of cell type- and pathway-specific synaptic plasticity in the NAc core in the expression of incubated methamphetamine craving. Outside the lab, Gillian enjoys hiking, knitting, and spending time with her cats and a good book.

A professional photo of Madelyn Beutler.

Madelyn M. Beutler, Research Assistant

Madelyn graduated from Washington State University in 2022 with a B.S in Psychology. At Washington State University, she volunteered in Dr. Michael Morgan’s lab investigating the effect of testosterone exposure on pain-related behavior. Madelyn joined the Wolf lab as a Research Assistant in 2022. She is currently managing the transgenic breeding colony and assisting graduate students and postdocs with drug self-administration and other procedures.

A professional photo of Sophia Weber.

Sophia J. Weber, Ph.D. student

Sophia graduated from University of Washington in 2017 with a B.S. in Biology. During her undergraduate career she worked first as a volunteer and then as a technician in Dr. Jeremy Clark’s lab investigating the effect of adolescent alcohol exposure on adult decision making. After graduation she obtained a postbaccalaureate internship in the NIDA IRP program, working in the lab of Dr. Bruce Hope where she assisted postdoctoral fellow Dr. Rajtarun Madangopal on his various projects that sought to selectively study and manipulate active neurons during drug related behaviors. In the Wolf lab Sophia used fiber photometry with dopamine biosensors combined with behavioral pharmacology to investigate the role of dopamine in the expression of incubation of cocaine craving. Sophia received her Ph.D. in June 2024 and is presently a postdoctoral fellow in Dr. Marco Venniro’s lab at the University of Maryland.

A professional photo of Amanda Wunsch.

Amanda M. Wunsch, Ph.D., Senior Research Associate

Amanda received her B.S. in Psychology from University of Iowa and her Ph.D. in Neuroscience from the University of Washington. She joined the Wolf lab as a postdoctoral fellow in 2016. With initial support from an individual postdoctoral NRSA, Amanda investigated the role of retinoic acid dependent homeostatic plasticity in the incubation of cocaine craving. Recently she has been using a combination of chemogenetic and fiber photometry techniques to explore the role of nucleus accumbens neurons in incubation of cocaine and methamphetamine craving. She enjoys knitting sweaters, is a voracious reader, and loves going on hikes with her dog Cosmo. Amanda recently accepted a position as Principal Investigator at the National Center for Wellness and Recovery at Oklahoma State University.

Kimberley A. Engeln (now Kimberley A. Mount), Ph.D. 2023
Current position: Project Director, Stagewise Implementation to Target – Medications for Addiction Treatment (SITT-MAT), Division of Behavioral Health and Recovery, Washington State Health Care Authority

Conor H. Murray, Ph.D. 2019
Current position: Postdoctoral fellow, UCLA

Michael T. Stefanik, Ph.D., Postdoctoral fellow 2014-2018
Current position: Tenure track Assistant Professor of Psychology & Neuroscience, North Central College

Daniel T. Christian, Ph.D., Postdoctoral fellow 2012-2018
Current position: Tenure track Assistant Professor, Des Moines University

Jessica A. Loweth, Ph.D., Postdoctoral fellow 2010-2017
Current position: Tenure track Assistant Professor of Cell Biology and Neuroscience, Rowan University School of Osteopathic Medicine

Craig T. Werner, Ph.D. 2015
Current position: Tenure track Assistant Professor of Pharmacology & Physiology, Oklahoma State University

Anthony Purgianto, Ph.D. 2015 (M.D. 2017)
Current position: Attending Physician, Department of Psychiatry, University of Iowa

Andrew F. Scheyer, Ph.D. 2015
Current position: Scientific writer

Xuan (Anna) Li, Ph.D. 2012
Current position: Tenure track Assistant Professor of Psychology, University of Maryland

Xiaoting Wang, Ph.D. 2012
Current position: Director of Regulatory Affairs at ImmunoGen, Inc.

Recent primary papers

  • Wang J, Ishikawa M, Yang Y, Otaka M, Kim JY, Gardner GR, Stefanik MT, Milovanovic M, Huang YH, Hell JW, Wolf ME, Schlüter OM, Dong Y (2018) Cascades of homeostatic dysregulation progressively intensify cocaine seeking. J Neurosci 38(18):4316-4328. PMC5932642
  • Werner CT*, Stefanik MT*, Milovanovic M, Caccamise A, Wolf ME (2018) Protein translation in the nucleus accumbens is dysregulated during cocaine withdrawal and required for expression of incubation of cocaine craving. J Neurosci 38(11):2683-2697. PMC5852654
  • Stefanik MT, Milovanovic M, Werner CT, Spainhour JCG, Wolf ME (2018) Withdrawal from cocaine self-administration alters the regulation of protein translation in the nucleus accumbens. Biol Psychiatry 84(3):223-232. PMC6054574
  • Stefanik MT, Sakas C, Lee D, Wolf ME (2018) Ionotropic and metabotropic glutamate receptors regulate protein translation in co-cultured nucleus accumbens and prefrontal cortex neurons. Neuropharmacology 140:62-75. PMC7575416
  • Scheyer AF, Christian DT, Wolf ME, Tseng KY (2018) Emergence of endocytosis-dependent mGlu1-LTD at nucleus accumbens synapses after withdrawal from cocaine self-administration. Front Synaptic Neurosci 10:36. Doi:10.3389/fnsyn.2018.00036. PMC6232902
  • Loweth JA, Reimers JM, Woo K-Y, Chauhan N, Werner CT, Wolf ME (2019) Metabotropic glutamate receptor 1 regulates GluA1 translation and cell surface expression of homomeric GluA1 receptors via retinoic acid signaling. Eur J Neurosci 50(3):2590-2601. PMC7556732
  • Murray CH, Loweth JA, Milovanovic M, Stefanik MT, Caccamise A, Dolubizno H, Funke JR, Olive MF, Wolf ME (2019) AMPA receptor and metabotropic glutamate receptor 1 adaptations in the nucleus accumbens core during incubation of methamphetamine craving. Neuropsychopharmacology 44(9):1534-1541. PMC6785134
  • Di S, Jiang Z, Wang S, Harrison L, Castro-Echeverry E, Stuart C, Wolf ME, Tasker J (2019) Labile calcium-permeable AMPA receptors constitute new glutamate synapses formed in hypothalamic neuroendocrine cells during salt loading. eNeuro 2019; 10.1523/ENEURO.0112-19.2019. PMC6675872
  • Munshi S, Rosenkranz JA, Caccamise A, Wolf ME, Corbett CM, Loweth JA (2019) Cocaine and chronic stress exposure produce an additive increase in neuronal activity in the basolateral amygdala. Addiction Biology 2019 Nov 21:e12848. PMC6675872
  • Murray CH, Christian DT, Milovanovic M, Loweth JA, Caccamise A, Funke JR, Wolf ME (2021) mGlu5 function in the nucleus accumbens core during the incubation of methamphetamine craving. Neuropharmacology, 2021 Mar 15;186:108452. doi: 10.1016/j.neuropharm.2021.108452. Epub 2021 Jan 12. PMC8440156
  • Christian DT, Stefanik MT, Bean LA, Loweth JA, Wunsch AM, Funke JR, Briggs CA, Lyons J, Neal D, Milovanovic M, D’Souza GX, Stutzmann GE, Nicholson DA, Tseng K-Y, Wolf ME (2021) GluN3-containing NMDA receptors in nucleus accumbens core are required for incubation of cocaine craving. J Neurosci. 41(39):8262-8277. PMC8482856
  • Murray CH, Gaulden AD, Kawa AB, Milovanovic M, Caccamise AJ, Funke JR, Patel S, Wolf ME (2021) CaMKII modulates diacylglycerol lipase-α activity in the rat nucleus accumbens after incubation of cocaine craving. eNeuro. 2021 Oct 8;8(5):ENEURO.0220-21.2021. doi: 10.1523/ENEURO.0220-21.2021. Print 2021 Sep-Oct. PMC8503962
  • Kawa AB, Hwang EK, Funke JR, Zhou H, Costa-Mattioli M, Wolf ME (2022) Positive allosteric modulation of mGlu1 reverses cocaine-induced behavioral and synaptic plasticity through the integrated stress response and oligophrenin-1. Biological Psychiatry 92(11):871-879. PMC10656746.
  • Wong B, Zimbelman AR, Milovanovic M, Wolf ME, Stefanik MT (2022) GluA2-lacking AMPA receptors in the nucleus accumbens core and shell contribute to the expression of incubation of oxycodone craving in male rats. Addiction Biology. Nov 2022;e13237. doi:10.1111/adb.13237. PMID: 36301206.
  • Funke JR, Hwang EK, Wunsch AM, Baker R, Engeln KA, Murray CH, Milovanovic M, Caccamise AJ, Wolf ME (2023) Persistent neuroadaptations in the nucleus accumbens core accompany incubation of methamphetamine craving in male and female rats. eNeuro. doi: 10.1523/ENEURO.0480-22.2023. Online ahead of print (Feb 13 2023). PMID: 36792361
  • Zimbelman AR, Wong B, Murray CH, Wolf ME, Stefanik MT. Dopamine D1 and NMDA receptor co-regulation of protein translation in cultured nucleus accumbens neurons. In revision. Posted to bioRxiv, April 2023.
  • Zhuo Y, Luo B, Yi X, Dong H, Miao X, Wan J, Williams JT, Campbell MG, Cai R, Qian T, Li F, Weber SJ, Wang L, Li B, Wei Y, Li G, Wang H, Zheng Y, Zhao Y, Wolf ME, Zhu Y, Watabe-Uchida M, Li Y (2023) Improved green and red GRAB sensors for monitoring dopaminergic activity in vivo. Nature Meth. 2023 Nov 30. doi: 10.1038/s41592-023-02100-w. Epub ahead of print. PMID 38036855.
  • Wunsch AM, Hwang E-K, Funke JR, Baker R, Moutier A, Milovanovic M, Green TA, Wolf ME (2024) Retinoic acid-mediated homeostatic plasticity in the nucleus accumbens core contributes to incubation of cocaine craving. Psychopharmacology, in press.
  • Weber SJ, Kawa AB, Moutier AL, Beutler MM, Koyshman LM, Moreno CD, Westlake JG, Wunsch AM, Wolf ME. Dopamine transmission at D1 and D2 receptors in the nucleus accumbens contributes to the expression of incubation of cocaine craving. In revision for Neuropsychopharmacology.
  • Kawa AB, Hashimoto JG, Nectow AR, Guizzetti M, Wolf ME. Changes in nucleus accumbens core translatome accompanying incubation of cocaine craving. Submitted.
  • Hwang E-K, Wunsch AM, Wolf ME. Retinoic acid-mediated homeostatic plasticity drives cell type-specific CP-AMPAR accumulation in nucleus accumbens core and incubation of cocaine craving. Submitted.

Recent review articles

  • Wolf ME, Zlebnik N (2024) Addiction. In: Basic Neurochemistry, 9th edition, ST Brady & G Siegel, eds. Elsevier Academic Press.
  • Wolf ME (2024) Targeting Neuroplasticity in Substance Use Disorders: Implications for Therapeutics. Annu Rev Pharmacol & Toxicology, Vol. 65 (in press).

  • Sophia Weber defended her Ph.D. on June 10 2024 and has moved to the University of Maryland for postdoctoral training in the lab of Dr. Marco Venniro.
  • Amanda Wunsch moved in July 2024 to a faculty position at Oklahoma State University. Amanda has made many contributions to the lab over the years and we wish her great success in her new position.
  • We welcome new Ph.D. student Gillian Driscoll!
  • Marina Wolf will be the Keynote Speaker at the Neurobiology of Drug Addiction Gordon Research Conference in August 2024.

Contact us

For questions or if you are interested in joining the lab as a Research Assistant or Postdoctoral Fellow, please contact Marina Wolf.

To learn more about our Ph.D. program, visit our Behavioral Neuroscience website.