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Faculty Research Labs

Atwood Lab Publications and Funding


  • 2023

    El Jordi O, Fischer KD, Meyer TB, Atwood BK, Oblak AL, Pan RW, McKinzie DL. Microglial knockdown does not affect acute withdrawal but delays analgesic tolerance from oxycodone in male and female C57BL/6J mice. Advances in Drug and Alcohol Research. In press.

    Morris CW, Watkins DS, Pennington T, Doud E, Qi G, Mosley A, Atwood BK, Baucum AJ. Spinophilin limits metabotropic glutamate receptor 5 scaffolding to the postsynaptic density and mediates excessive grooming cell type-specifically. Biological Psychiatry. In press. PMID: 36822932

    Haggerty DL, Grecco GG, Huang JY, Doud EH, Moseley AL, Lu H-C, Atwood BK. Prenatal methadone exposure selectively alters protein expression in primary motor cortex: implications for synaptic function. Frontiers in Pharmacology. 14:1124108 (2023). PMID: 36817148.

    Moutinho M, Coronel I, Tsai AP, Viana Di Prisco G, Pennington T, Atwood BK, Puntambekar SS, Smith DC, Martinez P, Han S, Lee Y, Lasagna-Reeves CA, Lamb BT, Bissel SJ, Nho K, Landreth GE. TREM2 splice isoforms increase in Alzheimer’s disease and generate soluble TREM2 which disrupts long-term potentiation. Genome Medicine. In press.

  • 2022

    Grecco GG, Haggerty DL, Reeves KC, Gao Y, Maulucci D, Atwood BK. Prenatal Opioid Exposure Reprograms the Behavioral Response to Future Alcohol Reward. Addiction Biology. 27(2):e13136 (2022). PMID: 35229956

    Grecco GG, Munoz B, Viana Di Prisco G, Doud EH, Fritz BM, Maulucci D, Gao Y, Moseley AL, Baucum AJ, Atwood BK. Prenatal opioid exposure impairs endocannabinoid and glutamate transmission in the dorsal striatum. eNeuro. 9(2):ENEURO.0119-22.2022 (2022). PMID: 35396255

    Grecco GG, Huang JY, Muñoz B, Doud EH, Hines CD, Gao Y, Rodriguez B, Moseley AL, Lu H-C, Atwood BK. Sex-Dependent Synaptic Remodeling of the Somatosensory Cortex in Mice With Prenatal Methadone Exposure. Advances in Drug and Alcohol Research. (2022).

    Reeves KC, Shah N, Muñoz B, Atwood BK. Opioid receptor-mediated regulation of neurotransmission in the brain. Frontiers in Molecular Neuroscience. 15:919773 (2022). PMID: 35782382

    Haggerty DL, Muñoz B, Pennington T, Grecco GG, Fritz BM, Atwood BK. Anterior insular cortex inputs to the dorsolateral striatum govern the maintenance of binge alcohol drinking. eLife. 11:e77411 (2022). PMID: 36098397. Selected for eLife “Insights” editorial.

    Martinez P, Patel H, You Y, Jury N, Perkins A, Lee-Gosselin A, Taylor X, You Y, Viana Di Prisco G, Huang X, Dutta S, Wijeratne A, Redding-Ochoa J, Shahid SS, Codocedo JF, Min S, Landreth GE, Mosley AL, Wu Y-C, McKinzie D, Rochet C, Zhang J, Atwood BK, Troncoso J, Lasagna-Reeves CA. Bassoon contributes to tau-seed neurotoxicity and propagation. Nature Neuroscience. 25(12):1597-1607 (2022). PMID: 36344699

    Muñoz B, Fritz BM, Yin F, Atwood BK.  HCN1 channels mediate mu opioid receptor long-term depression at insular cortex inputs to the dorsal striatum. Journal of Physiology. 600(22):4917-4938 (2022). PMID: 36181477

    Grecco GG, Shahid S, Atwood BK, Wu Y-C. Alterations of Brain Microstructures in a Mouse Model of Prenatal Opioid Exposure Detected by Diffusion MRI. Scientific Reports. 12(1):17085 (2022). PMID: 36224335

    Simmons SC, Grecco GG, Atwood BK, Nugent FS. Effects of Prenatal Opioid Exposure on Synaptic Plasticity and Behaviors Across Development. Neuropharmacology. 222:109312 (2022). PMID: 36334764

  • 2021

    Grecco GG, Haggerty DL, Doud E, Fritz BM, Hoffman H, Mosely A, Simpson E, Liu Y, Baucum AJ, Atwood BK. A Multi-Omic Analysis of the Dorsal Striatum in an Animal Model of Divergent Genetic Risk for Alcohol Use Disorder. J. Neurochem. 157(4):1013-1031. (2021). PMID: 33111353

    Kramer NB, Ross RA, Fenselau H, DQ, Haggerty DL, Atwood B, Lowell B, Flak JN. The Role of Ventromedial Hypothalamic PACAP in the Control of Body Weight and Metabolism. Endocrinology. 162(4):bqab012 (2021). PMID: 33460433

    Fritz BM, Yin F, Atwood BK. Input-Selective Adenosine A1 Receptor-Mediated Synaptic Depression of Excitatory Transmission in Dorsal Striatum. Scientific Reports. 11(1):6345 (2021). PMID: 33737568

    Grecco GG, Mork B, Huang JY, Metzger CE, Haggerty DL, Reeves KC, Gao Y, Hoffman H, Katner SN, Masters AR, Morris CW, Newell EA, Baucum, AJ Engleman EA, Kim J, Yamamoto BK, Allen MR, Wu YC, Lu HC, Sheets PL, Atwood BK. Prenatal Methadone Exposure Disrupts Behavioral Development and Alters Motor Neuron Intrinsic Properties and Local Circuitry. eLife. 10:e66230 (2021). PMID: 33724184.

    Grecco GG, Gao Y, Gao H, Liu Y, Atwood BK. Prenatal Opioid Administration Induces Shared Alterations to the Maternal and Offspring Gut Microbiome. Drug and Alcohol Dependence. 227:108914 (2021). PMID: 34364194

    Centanni S, Janes AC, Haggerty DL, Atwood BK, Hopf FW. Better living through understanding the insula: why subregions can make all the difference. Neuropharmacology. 198:108765 (2021). PMID: 34461066

    Karahan H, Smith D, Kim B, El-Amin MM, Dabin L, Pennington T, Viana di Prisco G, McCord B, Lin P, Atwood BK, Oblak A, Kim J. Deletion of Abi3 gene exacerbates neuropathological features of Alzheimer’s disease in a mouse model of Aβ amyloidosis. Science Advances. 7(45):eabe3954 (2021). PMID: 34731000
  • 2020
    Munoz B, Haggerty DL, Atwood BK. Synapse-specific expression of mu opioid receptor long-term depression in the dorsomedial striatum. Scientific Reports. 10(1):7234 (2020).PMID: 32350330

    Mulcahy G, Atwood B, Kuznetsov A. Basal Ganglia role in learning reward actions and executing previously learned choices: Healthy and diseased states.PLoS One. 2020 Feb 10;15(2):e0228081. PMID: 32040519

    Reeves KC, Kube MJ, Grecco GG, Fritz BM, Muñoz B, Yin F, Gao Y, Haggerty DL, Hoffman HJ, Atwood BK. Mu opioid receptors on vGluT2-expressing glutamatergic neurons modulate opioid reward. Addiction Biology. Jul 20:e12942 (2020). PMID: 32686251

    Cisternas P, Taylor X, Perkins A, Maldonado O, Allman E, Cordova R, Marambio Y, Munoz B, Pennington T, Xiang S, Zhang J, Vidal R, Atwood B, Lasagna-Reeves CA. Vascular amyloid accumulation alters the gabaergic synapse and induces hyperactivity in a model of cerebral amyloid angiopathy. Aging Cell. (2020). 19(10):e13233. PMID: 32914559

    Jadhav VS, Lin PB, Xu G, Pennington T, Viana Di Prisco G, Jacob A, Moutinho M, Puntambekar SS, Zhang J, Atwood BK, Bissel SJ, Oblak AL, Landreth GE, Lamb BT. Trem2 Y38C mutation and loss of Trem2 impairs neuronal synapses with age. Molecular Neurodegeneration. 15(1):62 (2020). PMID: 33115519

    Radhakrishnan R, Grecco G, Stolze K, Atwood BK, Jennings SG, Lien IZ, Saykin AJ, Sadhasivam S. Early Neuroimaging in Infants with Prenatal Opioid Exposure: Insights and Recent Developments. Journal of Neuroradiology. 13:S0150-9861(20)30278-9 (2020). PMID: 33065196

    Grecco GG, Atwood BK. Prenatal Opioid Exposure Enhances Responsiveness to Future Drug Reward and Alters Sensitivity to Pain: A Review of Preclinical Models and Contributing Mechanisms. eNeuro. ENEURO.0393-20.2020 (2020) PMID: 33060181

  • 2019

    Haggerty DL, Grecco GG, Reeves K, Atwood BK. Adeno-associated viral vectors in neuroscience research. Molecular Therapy - Methods and Clinical Development. 17:69-82 (2019). PMID: 31890742

    Fritz BM, Munoz B, Atwood BK. Genetic Selection for Alcohol Preference in Mice Alters Dorsal Striatum Neurotransmission. Alcoholism: Clinical and Experimental Research. 43 (11):2312-2321 (2019). PMID: 31491046.

    Jay T, von Saucken VE, Muñoz B, Codocedo JF, Atwood BK, Lamb BT, Landreth GE. The neurodegeneration-associated receptor TREM2 is required for microglial instruction of astrocytic synaptic engulfment in neurodevelopment. Glia. 67(10):1873-1892 (2019). PMID: 31265185.

    You Y, Perkins A, Cisternas P, Muñoz B, Taylor X, You Y, Garringer HJ, Oblak AL, Ghetti B, Atwood BK, Vidal R, Lasagna-Reeves C. Tau as a mediator of neurotoxicity associated to Cerebral Amyloid Angiopathy. Acta Neuropathologica Communications. 7(1):26 (2019). PMID: 30808415.

  • 2018

    Munoz, B., Fritz, B.M., Yin, F., Atwood, B.K.  Alcohol exposure disrupts mu opioid receptor-mediated long-term depression at insular cortex inputs to dorsolateral striatum. Nature Communications. In press.

    Fritz, B.M., Munoz, B., Yin, F., Bauchle, C., Atwood, B.K. A high-fat, high-sugar ‘western’ diet alters dorsal striatal glutamate, opioid, and dopamine transmission in mice. Neuroscience, Epub December 28, 2017PMID: 29289718.

  • 2017
    Mateo, Y., Johnson, K., Covery, D.P., Atwood, B.K., Wang, H.-L., Zhang, S., Gildish, I., Cachope, R., Bellocchio, L., Guzman, M., Morales, M., Cheer, J., Lovinger, D. M. Endocannabinoid Actions on Cortical Terminals Orchestrate Local Modulation of Dopamine Release in the Nucleus Accumbens. Neuron, 96(5):1112-1126 (2017). PMID: 29216450

    Atwood, B.K., Lovinger, D.M. Endocannabinoid-Dependent Synaptic Plasticity in the Striatum. Endocannabinoids and Lipid Mediators in Brain Functions. 109-153 (2017)

  • 2016
    Gremel, C., Chancey, J., Atwood, B.K., Luo, G., Neve, R., Ramakrishnan, C., Deisseroth, K., Lovinger, D.M., Costa, R. Endocannabinoid modulation of orbitostriatal circuits gates habit formation. Neuron. 90(6):1312-1324 (2016). PMID: 27238866
  • 2014
    Atwood, B.K., Lovinger, D.M., Mathur, B.M. Presynaptic long-term depression mediated by Gi/o-coupled receptors. Trends in Neurosciences. 37(11): 663-673 (2014). PMID: 25160683

    Atwood, B.K., Kupferschmidt, D.A., Lovinger, D.M. Opioids induce dissociable forms of long-term depression of excitatory inputs to the dorsal striatum. Nature Neuroscience. 17(4): 540-548 (2014). PMID: 24561996

  • 2012
    Atwood, B.K., Wager-Miller, J., Haskins, C., Straiker, A, Mackie, K. Functional selectivity in CB(2) cannabinoid receptor signaling and regulation: implications for the therapeutic potential of CB(2) ligands. Molecular Pharmacology. 81(2): 250-263 (2012). PMID: 22064678

    Atwood, B.K., Straiker A., Mackie, K. CB(2) cannabinoid receptors inhibit synaptic transmission when expressed in cultured autaptic neurons. Neuropharmacology. 63(4): 514-523 (2012). PMID: 22579668

    Atwood, B.K., Straiker, A., Mackie, K. CB(2): Therapeutic target-in-waiting. Progress in Neuro-Psychopharmacology and Biological Psychiatry. 38(1): 16-20 (2012). PMID: 22197668

  • 2011
    Atwood, B.K., Lopez, J., Wager-Miller, J., Mackie, K., Straiker, A. Expression of G protein-coupled receptors and related proteins in HEK293, AtT20, BV2, and N18 cell lines as revealed by microarray analysis. BMC Genomics. 12:14. (2011). PMID: 21214938

    Atwood, B.K., Lee, D., Straiker, A., Widlanski, T.S., Mackie, K. CP47,497-C8 and JWH073, commonly found in ‘Spice’ herbal blends, are potent and efficacious CB(1) cannabinoid receptor agonists. European Journal of Pharmacology. 659(2-3): 139-145 (2011). PMID: 21333643

  • 2010
    Atwood, B.K., Mackie, K. CB2: a cannabinoid receptor with an identity crisis. British Journal of Pharmacology. 160(3): 467-479 (2010). PMID: 20590558

    Atwood, B.K., Huffman, J., Straiker, A., Mackie, K. JWH018, a common constituent of ‘Spice’ herbal blends, is a potent and efficacious cannabinoid CB receptor agonist. British Journal of Pharmacology. 160(3): 585-593 (2010). PMID: 20100276


  • R21 AA030319 (MPI w/ AJ Baucum)

    A novel proteomics approach to identify alcohol-induced changes in synapse-specific presynaptic protein interactions.


    Role: MPI w/ AJ Baucum

  • R01 AA027214 (PD/PI)


    Synapse-specific interactions between ethanol and opioid receptor-mediated synaptic depression in dorsal striatum


    Role: PD/PI

  • R01 NS119280 (PI: Lasagna-Reeves)


    Tau-seed protein interactome and its role in neurodegenerative tauopathies.


    Role: Co-investigator

  • 1RF1AG074543-01 (PI: Kim)


    The role of ABI3 in Alzheimers disease.


    Role: Co-investigator

  • 1F31AA029297-01A1

    Anterior insular cortex to dorsolateral striatum neural circuit regulation of binge drinking and habitual behaviors


    Role: Primary Sponsor/Mentor for Graduate Student David Haggerty 

  • U54 (PIs: Lamb, Oblak, Territo, Sasner, Howell, Rizzo, Carter)

    The IU/JAX Alzheimer's Disease Precision Models Center


    Role: Co-investigator

Research Collaborators at IU

Matthew R. Allen, PhD

Professor of Anatomy, Cell Biology & Physiology

AJ Baucum, PhD

Associate Professor of Pharmacology & Toxicology

Jungsu Kim, PhD

P. Michael Conneally Professor of Medical and Molecular Genetics

Bruce T. Lamb, PhD

Executive Director, Paul and Carole Stark Neurosciences Research Institute

Gary E. Landreth, PhD

Martin Professor of Alzheimer's Research

Cristian A. Lasagna Reeves, PhD, MS

Associate Professor of Anatomy, Cell Biology & Physiology

Patrick L. Sheets, PhD

Associate Professor of Pharmacology & Toxicology

Bryan K. Yamamoto, PhD

Robert B. Forney Professor Emeritus of Toxicology

Alexy Kuznetsov

Alexy Kuznetsov, PhD

Associate Professor of Mathematical Sciences

Hui-Chen Lu

Hui-Chen Lu, PhD

Linda and Jack Gill Chair of Neuroscience and Professor