Joseph F. Cheer, PhD

Aroni S, Marino RAM, Girven KS, Irving JM, Cheer JF and Sparta DR. (2021) Repeated binge ethanol drinking enhances electrical activity of central amygdala corticotropin releasing factor neurons in vivo. Neuropharmacology, in press

Traccis F, Serra V, Sagheddu C, Congiu M, Saba P, Giua G, Devoto P, Frau R, Cheer JF and  Melis M. (2021) Prenatal THC Does Not Affect Female Mesolimbic Dopaminergic System in Preadolescent Rats. International Journal of Molecular Science, 22: 1666.

Gomez DM, Everett TJ, Hamilton LR, Ranganath A, Cheer JF and Oleson EB. (2021) Chronic cannabinoid exposure produces tolerance to the dopamine releasing effects of WIN 55,212-2 and heroin in adult male rats. Neuropharmacology, in press

Luján MÁ, Cheer JF and Melis M. (2021) Choosing the right drug: status and future of endocannabinoid research for the prevention of drug-seeking reinstatement. Current Opinion in Pharmacology, in press

Sagheddu C, Traccis F, Serra V, Congiu M, Frau R, Cheer JF and Melis M. (2021) Mesolimbic dopamine dysregulation as a signature of information processing deficits imposed by prenatal THC exposure. Progress in Neuropsychopharmacology and Biological Psychiatry, in press

Girven KS, Aroni S, Navarrete J, Marino RAM, McKeon PN, Cheer JF and Sparta DR. (2021) Glutamatergic input from the insula to the ventral bed nucleus of the stria terminalis controls reward-related behavior. Addiction Biology, 2026: e12961

Schneider KN, Sciarillo XA, Nudelman JL, Cheer JF and Roesch MR. (2020) Anterior Cingulate Cortex Signals Attention in a Social Paradigm that Manipulates Reward and Shock. Current Biology, 30: 3724-3735

Nam H, Chandra R, Francis TC, Dias C, Cheer JF and Lobo MK. (2019) Reduced nucleus accumbens enkephalins underlie vulnerability to social defeat stress. Neuropsychopharmacology, 44: 1876-1885

Cover KK, Gyawali U, Kerkhoff WG, Patton MH, Mu C, White MG, Marquardt AE, Roberts BM, Cheer JF and Mathur BN. (2019) Activation of the Rostral Intralaminar Thalamus Drives Reinforcement through Striatal Dopamine Release. Cell Reports, 26: 1389-1398

Wang HL, Zhang S, Qi J, Wang H, Cachope R, Mejias-Aponte CA, Gomez JA, Mateo-Semidey GE, Beaudoin GMJ, Paladini CA, Cheer JF and Morales M. (2019) Dorsal Raphe Dual Serotonin-Glutamate Neurons Drive Reward by Establishing Excitatory Synapses on VTA Mesoaccumbens Dopamine Neurons. Cell Reports, 26: 1128-1142

Radke AK, Kocharian A, Covey DP, Lovinger DM, Cheer JF, Mateo Y, Holmes A. (2019) Contributions of nucleus accumbens dopamine to cognitive flexibility. European Journal of  Neuroscience, 50: 2023-2035

Lichtenberg NT, Lee B, Kashtelyan V, Chappa BS, Girma HT, Green EA, Kantor S, Lagowala DA, Myers MA, Potemri D, Pecukonis MG, Tesfay RT, Walters MS, Zhao AC, Blair RJR, Cheer JF and Roesch MR. (2018) Rat behavior and dopamine release are modulated by conspecific distress. Elife, 28:7-e38090

Yohn SE, Foster DJ, Covey DP, Moehle MS, Galbraith J, Garcia-Barrantes PM, Cho HP, Bubser M, Blobaum AL, Joffe ME, Cheer JF, Jones CK, Lindsley CW and Conn PJ. (2018) Activation of the mGlu1 metabotropic glutamate receptor has antipsychotic-like effects and is required for efficacy of M4 muscarinic receptor allosteric modulators.  Molecular Psychiatry, 25: 2786-2799

Bacharach SZ, Nasser HM, Zlebnik NE, Dantrassy HM, Cheer JF and Calu DJ. (2018) Cannabinoid receptor-1 signaling contributions to sign-tracking and conditioned reinforcement in rats. Psychopharmacology, 235: 3031-3043

Covey DP, Dantrassy HM, Yohn SE, Castro A, Conn JP, Mateo Y and Cheer JF. (2018) Inhibition of endocannabinoid degradation rectifies motivational and dopaminergic deficits in the Q175 mouse model of Huntington’s disease. Neuropsychopharmacology, 43: 2056-2063

Bailey MR, Goldman O, Bello EP, Jeong N, Winiger V, Chun E, Schipani E, Cheer JF, Balsam PD and Simpson E. (2018) A functional interaction between serotonin receptor signaling and striatal dopamine release enhances response vigor and goal-directed persistence in mice. Journal of Neuroscience, 38: 2385-2397

Wenzel JM and Cheer JF. (2018) Endocannabinoid regulation of reward and reinforcement through interaction with dopamine and endogenous opioid signaling. Neuropsychopharmacology 43: 103-115

Cheer JF and Hurd YL. (2017) A new dawn in cannabinoid neurobiology: The road from molecules to therapeutic discoveries. Neuropharmacology 124: 1-2

Covey DP, Mateo Y, Sulzer D, Cheer JF and Lovinger DM. (2017) Endocannabinoid modulation of dopamine neurotransmission. Neuropharmacology 124:52-61 

Patel S, Hill MN, Cheer JF, Wotjak CT and Holmes A. (2017) The endocannabinoid system as a target for novel anxiolytic drugs. Neuroscience & Biobehavioral Reviews, 76: 56-66, invited review 

Lopatina N, MCDanald MA, Styer CV, Peterson JF, Sadacca BF, Cheer JF and Schoenbaum G. (2017) Ensembles in medial and lateral orbitofrontal cortex construct cognitive maps emphasizing different features of the behavioral landscape. Behavioral Neuroscience 131: 201-212

Terrillion CE, Dao DT, Cachope R, Lobo MK, Puche A, Cheer JF and Gould TD. (2017) Reduced levels of Cacna1c modify the mesolimbic dopamine system. Genes, Brain and Behavior 16: 495-505

Fotowat H, Harvey-Girard E, Cheer JF, Krahe R and Maler L. (2016). Subsecond Sensory Modulation of Serotonin Levels in a Primary Sensory Area and Its Relation to Ongoing Communication Behavior in a Weakly Electric Fish. E-Neuro 3: 1-12

Can A, Zanos P, Moaddel R, Huang XP, Hye JK, Katinia SS, Irving WW, Cheer JF, Frost DO, Roth BL and Gould TD. (2016) The antidepressant effects of ketamine do not involve transduction of subsecond dopamine by dopamine receptors. Journal of Pharmacology and Experimental Therapeutics 359: 159-170

Zlebnik NE and Cheer JF. (2016) Drug-Induced Alterations of Endocannabinoid-Mediated Plasticity in Brain Reward Regions. Journal of Neuroscience 36: 10230-10238

Lopatina N, McDannald MA, Styer CV, Peterson JF, Sadacca BF, Cheer JF and Schoenbaum G. (2016) Medial Orbitofrontal Neurons Preferentially Signal Cues Predicting Changes in Reward during Unblocking. Journal of Neuroscience 36: 8416-8424

Cockerham R, Liu S, Cachope R, Kiyokage E, Cheer JF, Shipley MT and Puche AC. (2016) Subsecond Regulation of Synaptically Released Dopamine by COMT in the Olfactory Bulb. Journal of Neuroscience 36: 7779-7785

Covey DP, Zlebnik NE and Cheer JF. (2016) Endocannabinoid Regulation of Cocaine Reinforcement: an Upper or Downer? Neuropsychopharmacology. 41: 2189-2191

Covey DP, Dantrassy HM, Zlebnik NE, Gildish I and Cheer JF. (2016) Compromised Dopaminergic Encoding of Reward Accompanying Suppressed Willingness to Overcome High Effort Costs Is a Prominent Prodromal Characteristic of the Q175 Mouse Model of Huntington's Disease. Journal of Neuroscience 36: 4993-5002

Covey DP, Bunner KD, Schuweiler DR, Cheer JF and Garris PA. (2016) Amphetamine elevates nucleus accumbens dopamine via an action potential-dependent mechanism that is modulated by endocannabinoids. European Journal of Neuroscience 43: 1661-1673

Lopatina N, MCdannald MA, Styer CV, Sadacca BF, Cheer JF and Schoenbaum G. (2015) Lateral orbitofrontal neurons acquire responses to upshifted, downshifted or blocked cues during unblocking. E-Life, 4:e11299

Bagot RC, Parise EM, Maze I, Persaud B, Cachope R, Bolaños CA, Cheer JF, Deisseroth K and Nestler EJ. (2015) Ventral hippocampal afferents to the nucleus accumbens regulate susceptibility to depression-like& behavior. Nature Communications, 6: 7626-7631

Wang H, Treadway T, Covey DP, Cheer JF and Lupica CR. (2015) Cocaine-mediated endocannabinoid mobilization in the ventral tegmental area regulates subsecond dopamine release in nucleus accumbens. Cell Reports, 12: 1997-2008

Hernandez G and Cheer JF. (2015) To act or not to act: endocannabinoid/dopamine interactions in decision-making. Frontiers in Neuroscience, invited review, 9: 1-10

Wenzel JM, Rauscher NA, Cheer JF and Oleson EB. (2015) A role for phasic dopamine release within the nucleus accumbens in encoding aversion: a review of the neurochemical literature. ACS Chemical Neuroscience 6: 16-26

Covey DP, Wenzel JM and Cheer JF. (2014) Cannabinoid modulation of drug reward and the implications of marijuana legalization. Brain Research 1628(Pt A): 233-243

Kashtelyan V, Lichtenberg NT, Chen ML, Cheer JF and Roesch MR. (2014) Observation of reward delivery to a conspecific modulates dopamine release in ventral striatum. Current Biology 24: 2564-2568

Covey DP and Cheer JF. (2014) Pick your poison: not all opioids are created equal in the eyes of dopamine (commentary on Vander Weele et al.). European Journal of Neuroscience 40: 3040

Wenzel JM and Cheer JF. (2014) Endocannabinoid-dependent modulation of phasic dopamine signaling encodes external and internal reward-predictive cues. Frontiers in Psychiatry 5:118

Schluter EW, Mitz AR, Cheer JF and Averbeck BB. (2014) Real-time dopamine measurement in awake monkeys. PLoS One. 9:e98692

Cachope R and Cheer JF. (2014) Local control of striatal dopamine release. Frontiers in Behavioral Neuroscence 8: 188

Oleson EB, Cachope R, Fitoussi A, Tsutsui K, Wu S, Gallegos JA and Cheer JF. (2014) Cannabinoid receptor activation shifts temporally engendered patterns of dopamine release. Neuropsychopharmacology 39: 1441-1452

Lobo MK, Zaman S, Damez-Werno DM, Koo JW, Bagot RC, DiNieri JA, Nugent A, Finkel E, Chaudhury D, Chandra R, Riberio E, Rabkin J, Mouzon E, Cachope R, Cheer JF, Han MH, Dietz DM, Self DW, Hurd YL, Vialou V and Nestler EJ. (2013) ΔFosB induction in striatal medium spiny neuron subtypes in response to chronic pharmacological, emotional, and optogenetic stimuli. Journal of Neuroscience 33: 18381-18395

Vinish M, Elnabawi A, Milstein JA, Burke JS, Kallevang JK, Turek KC, Lansink CS, Merchenthaler I, Bailey AM, Kolb B, Cheer JF and Frost DO. (2013) Olanzapine treatment of adolescent rats alters adult reward behaviour and nucleus accumbens function. International Journal of Neuropsychopharmacology 16: 1599-5609

Wang B, You ZB, Oleson EB, Cheer JF, Myal S and Wise RA. (2013) Conditioned contribution of peripheral cocaine actions to cocaine reward and cocaine-seeking. Neuropsychopharmacology. 38: 1763-1769

Chandra R, Lenz JD, Gancarz AM, Chaudhury D, Schroeder GL, Han MH, Cheer JF, Dietz DM and Lobo MK. (2013) Optogenetic inhibition of D1R containing nucleus accumbens neurons alters cocaine-mediated regulation of Tiam1. Frontiers in Molecular Neuroscience 6:13

Oleson EB and Cheer JF. (2013) On the role of subsecond dopamine release in conditioned avoidance. Frontiers in Neuroscience7: 96

Loewinger GC, Oleson EB and Cheer JF. (2013) Using dopamine research to generate rational cannabinoid drug policy. Drug Testing and Analysis 5: 22-26

Lee AM, Oleson EB, Diergaarde L, Cheer JF* and Pattij T*. (2012) Cannabinoids and value-based decision making: Implications for neurodegenerative disorders. Basal Ganglia 2: 131-138 Invited Review, * equal contribution

Oleson EB andCheer JF. (2012) Paradoxical effects of the endocannabinoid uptake inhibitor VDM11 on accumbal neural encoding of reward predictive cues. Synapse 66: 984-988

Hernandez G and Cheer JF. (2012) Effect of CB1 Receptor Blockade on Food-Reinforced Responding and Associated Nucleus AccumbensNeuronal Activity in Rats. Journal of Neuroscience 32: 11467-11477

Oleson EB and Cheer JF. (2012) A brain on cannabinoids: the role of dopamine release in reward seeking. Cold Spring Harbor Perspectives in Medicine 1;2(8)

Loewinger G, Beckert MV, Tejeda H and Cheer JF. (2012) Enduring methamphetamine-induced dopaminergic effects in the nucleus accumbens are exacerbated by reward associated cues and attenuated by CB1 receptor antagonism. Neuropharmacology 62: 2191-2200.

Morra JT, Glick SD and Cheer JF. (2012) Cannabinoid receptors mediate methamphetamine induction of gamma oscillations in the nucleus accumbens. Neuropharmacology 63: 565-574

Mazei-Robison MS, Koo JW, Lansink CS, Han MH, Robison AJ, Krishnan V, Kim S, Siuta MA, Galli A, Neve RL, Snyder SH, Cheer JF, Russo S and EJ Nestler. (2011) Morphine-induced changes in dopamine ventral tegmental area neuronal morphology are dependent on mTOR signaling and neuronal activity. Neuron 72: 977-990

Hernandez G, Bernstein D, Schoenbaum G and Cheer JF. (2011) Contrasting Effects of Lithium Chloride and CB1 Receptor Blockade on Enduring Changes in the Valuation of Reward. Frontiers in Behavioral Neuroscience 5: 53

Hernandez G and Cheer JF. (2011) Extinction learning of rewards in the rat: is there a role for CB1 receptors? Psychopharmacology (Berl). 217: 189-197

Trujillo-Pisanty I, Hernandez G, Moreau-Debord I, Cossette MP, Conover K, Cheer JF and Shizgal P. (2011) Cannabinoid receptor blockade reduces the opportunity cost at which rats maintain operant performance for rewarding brain stimulation. Journal of Neuroscience 31: 5426-5435

Morra JT, Glick SD and Cheer JF. (2010)Neural encoding of psychomotor activation in the nucleus accumbens core, but not the shell, requires cannabinoid receptor signaling. Journal of Neuroscience 30: 5102-5107

Mason R and Cheer JF. (2009) Cannabinoid receptor activation reverses kainate-induced synchronized population burst firing in rat hippocampus. Frontiers in Integrative Neuroscience 3: 13

Villanueva A, Yilmaz MS, Millington WR, Cutrera RA, Stouffer DG, Parsons LH, Cheer JF* and Feleder C*. (2009) Central Cannabinoid-1 Receptor Antagonist Administration Prevents Endotoxic Hypotension Affecting Norepinephrine Release in the Preoptic Anterior Hypothalamic Area. Shock 32: 514-620 (* Equal contribution)

Heien MLAV, Khan AS, Ariansen JL, Cheer JF, Phillips PEM, Wassum KM and Wightman RM. (2005) Principal component regression resolves dopamine fluctuations in the brain of behaving rats revealed from in vivo voltammetry. Proceedings of the National Academy of Sciences of the United States of America 102: 10023-10028

Research in my lab is aimed at understanding the physiological function of the endogenous cannabinoid system with a particular emphasis on normal motivated behaviors as well as its potential therapeutic role in pathological states such as addiction.

Endogenous cannabinoids such as arachidonoylethanolamide (anandamide from the sanskrit word "ananda" meaning bliss) and 2-arachidonoylglycerol (2-AG) and their binding to central cannabinoid receptors (CB1) in the brain and spinal cord make up this widespread signaling system. These molecules are involved in a wide spectrum of physiological states ranging from reinforcement processing to pain perception and executive function.

Our research employs state-of-the-art electrophysiological (ensemble recordings) and electrochemical (fast-scan cyclic voltammetry) techniques to extract neurobiological correlates of key aspects of behavior in real-time. We have also implemented the use of a microsensor that can simultaneously record extracellular single-unit activity and neurotransmitter release. These techniques are used in conjunction with tools such as systemic drug administration, cerebral microinjection, iontophoresis, optogenetics, chemogenetics and calcium imaging to examine how endogenous cannabinoids modulate the encoding of motivated behavior.

We are specifically interested in the dopaminergic projection from the ventral tegmental area to the nucleus accumbens. Dopaminergic neurons burst fire in response to rewards and play a key role in the prediction of the availability of reward. We have shown that exogenous cannabinoids potently modulate the activity of dopaminergic neurons, in particular their ability to burst fire and to produce transient increases in dopamine concentration in the nucleus accumbens, suggesting that endogenous cannabinoids are indeed important mediators of reward encoding in behaving animals. Thus, understanding the interactions between endogenous cannabinoid and dopaminergic signaling in the nucleus accumbens during reward-related behavior is likely to yield unprecedented insight on the pathogenesis of disorders of motivation such as addiction.

Awards

1996         Pre-doctoral Scholarship from the Colombian Science Foundation

1997         Glaxo-Wellcome Ph.D. Studentship

1997         British Pharmacological Society travel award

1997         British Association of Psychopharmacology travel award

1998         British Association of Psychopharmacology award

1999         Brain ®/IBRO award

1999         British Pharmacological Society travel award

2001         Coy Waller Merit Award on Cannabinoid Research

2001         International Cannabinoid Research Society/NIDA travel award

2003         10th International Conference on In Vivo Methods travel award

2004         Cover, The Journal of Neuroscience, Volume 24, Number 18

2004         Smallwood Award for Teaching Undergraduate Research

2005         International Cannabinoid Research Society/NIDA travel award

2006         Winter Conference on Brain Research Fellowship

2007         Albany Medical College Junior Faculty Award

2008         NARSAD Young Investigator Award

2010         Top reviewer for “Neuropharmacology”

2012         Cachope et al, Cell Reports, Faculty of 1000, Neuron commentary

2013         Plenary speaker for the Carolina Cannabinoid Collaborative Annual meeting

2014         Accepted into the American College of Neuropsychopharmacology

2014         Hernandez et al, Biological Psychiatry, featured article and commentary

2015         Invited Visiting Professorship (UNICA VP), University of Cagliari, Italy

2016         Covey et al, The Journal of Neuroscience, featured article

2017         Sterling Visiting Fellow, Boston University

2017         Plenary Speaker, International Cannabinoid Research Society (declined)

2017         GPILS/OPS Postdoctoral Mentor Award at UMSOM

2018         STAR-PREP Excellence in Mentoring Award

2019         Plenary Speaker, Gordon Research Conference on Cannabinoid Function in the CNS

2019         Wenzel et al., Current Biology, Faculty of 1000

2019         Keynote Speaker, 20^th Annual Meeting of the Spanish Society for Cannabinoid Research

2019         Biomedical Distinguished Lecturer, The Frank Reidy Center for Bioelectrics, Old Dominion University

Society Memberships

1997 – 2000       British Association of Psychopharmacology

1997 – 2000       British Pharmacological Society

1999 – present  Society for Neuroscience

2000 – present  International Cannabinoid Research Society

2003 – present  International Society for Monitoring Molecules in Neuroscience

CHDI project 12 (PI)                             04/01/14-03/31/2023

CHDI, Huntington’s foundation


Harnessing the predictive power of endocannabinoid signaling in Huntington’s


This study probes the endocannabinoid system as a potential biomarker system for the progression of the disease in a mouse model with face and construct validity.

R01DA042595 (PI)                              07/01/16-04/30/2021


NIH/NIDA

Enduring consequences of adolescent cannabinoid and methylphenidate exposure

 This study is an assessment of how adolescent co-exposure to THC (the main psychoactive of marijuana) and methylphenidate (Ritalin ®); enduringly changes decision-making and its dopaminergic neural substrates.

R01MH112504 (MPI)                            04/01/17-03/31/2022


NIH/NIMH

Neural mechanisms of decisions made in the context of social distress

 This study aims to examine the neural mechanisms related to modification of reward-guided behavior during conspecific distress in multiple social contexts and time scales as contingencies are learned and social relationships change with experience. 

R01DA044925 (PI)                                09/30/18-05/31/2023


NIH/NIDA

Neurodevelopmental effects of THC on the VTA dopamine system and behavior

This study will probe the extent of adaptations that arise from in utero exposure to THC in the context of dopamine system developments and related reward behaviors. 

R01DA045639 (PI)                                01/31/19-12/31/2024

NIH/NIDA

Cannabinoid receptor control of DRN to VTA pathway and its role in affective states

This study focuses on the dorsal raphe serotonergic innervation to the dopaminergic midbrain as a critical circuit mediating the amotivational effects of adolescent exposure to marijuana.

Administrative Service

Institutional Service

Department of Anatomy and Neurobiology UMSOM

• 2008 – 2011: Curriculum Committee
• 2008 – present: Alternate for SOM council
• 2010 – 2011: Seminar Committee, Co-chair
• 2010 – present: Faculty Search Committee, Chair (successfully recruited Drs. Mary Kay Lobo in 2011, Dennis Sparta in 2014 and Donna Calu in 2015 at the tenure-track Assistant Professor level)
• 2011 – 2014: Seminar Committee, Chair

• 2017 – present Faculty Search committee, Chair

University of Maryland School of Medicine Program Memberships and Service

• 2008 – present: Program in Neuroscience
• 2008 – present: Cellular and Integrative Neuroscience Training Program
• 2008 – present: Interviewer, Program in Neuroscience candidates
• 2008 – present: Interviewer, M.D./Ph.D. candidates
• 2010: Invited speaker: “Publish, Don’t Perish” workshop
• 2013: Invited speaker: “Building an Effective Research Team” workshop
• 2014: Invited speaker: “Building an Effective Research Team” workshop
• 2015 – present: Brain Sciences Research Consortium (BSRCU) advisory board
• 2016: Invited speaker: “Strategies to Build Your Research Program” workshop
• 2020 - present: SOM APT Committee Member

National Service

NIH study sections

• 2009: ARRA Challenge Grant Reviewer
• 2010: NIH/NIDA BRLE Study Section (ad hoc)
• 2011: NIH/NIDA NMB Study Section (ad hoc)
• 2011: NIH/NIDA RPHB Study Section (ad hoc)
• 2012: National Center for Advancing Translational Sciences (NCATS), NIH review
• 2011-2015: NIH/NIDA BRLE Study Section (permanent/declined)
• 2012-2016: NIH/NIDA NMB Study Section (permanent)
• 2014-2015: ZMH1 ERB-L (01) S, Silvio O. Conte Centers for Basic or Translational Mental Health Research (P50) (ad hoc)
• 2016: Cutting-Edge Basic Research Awards (CEBRA) (R21) (ad hoc)
• 2017:  NIH/NIDA P50 and P30 Centers of Excellence
• 2018: BRAIN initiative research awards
• 2019: NIH/NIDA BRLE Study Section (ad hoc)
• 2020: NIH F03B Study Section (ad hoc)

Reviewing Editor

• 2011-present:Frontiers in Neuropharmacology
• 2015-present: Cannabis and Cannabinoid Research
• 2015-present: Journal of Neuroscience
• 2018-present: Journal of Cannabis Research
• 2019-present: ELife

• Behavioral analysis with AI video capture
• Fast-scan cyclic voltammetry
• Ensemble single-unit recordings
• Iontophoresis
• Cerebral micro-injection
• Optogenetics
• Chemogenetics
• Cre-lox recombination for directed mutagenesis
• Calcium mini-endoscope technology
• Fluorescence microscopy
• Fiber photometry

www.cheerlab.org