Soden ME, Yee JX, Cuevas B, Rastani A, Elum J, Zweifel LS. Distinct Encoding of Reward and Aversion by Peptidergic BNST Inputs to the VTA. Front Neural Circuits. 2022 Jul 4;16:918839. doi: 10.3389/fncir.2022.918839. PMID: 35860212; PMCID: PMC9289195.

Juarez B, Zweifel LS. Disinhibitory feedback loops for reward and aversion. Cell Res. 2022 Feb;32(2):115-116. doi: 10.1038/s41422-021-00601-x. PMID: 34949785; PMCID: PMC8807610.

Gamal El-Din TM, Lantin T, Tschumi CW, Juarez B, Quinlan M, Hayano JH, Li J, Zweifel LS, Catterall WA. Autism-associated mutations in KV7 channels induce gating pore current. Proc Natl Acad Sci U S A. 2021 Nov 9;118(45):e2112666118. doi: 10.1073/pnas.2112666118. PMID: 34728568; PMCID: PMC8609342.

Fellinger L, Jo YS, Hunker AC, Soden ME, Elum J, Juarez B, Zweifel LS. A midbrain dynorphin circuit promotes threat generalization. Curr Biol. 2021 Oct 11;31(19):4388-4396.e5. doi: 10.1016/j.cub.2021.07.047. Epub 2021 Aug 12. PMID: 34388372; PMCID: PMC8511093.

Kong MS, Kim EJ, Park S, Zweifel LS, Huh Y, Cho J, Kim JJ. 'Fearful-place' coding in the amygdala-hippocampal network. Elife. 2021 Sep 17;10:e72040. doi: 10.7554/eLife.72040. PMID: 34533133; PMCID: PMC8500711.

Stincic TL, Bosch MA, Hunker AC, Juarez B, Connors AM, Zweifel LS, Rønnekleiv OK, Kelly MJ. CRISPR knockdown of Kcnq3 attenuates the M-current and increases excitability of NPY/AgRP neurons to alter energy balance. Mol Metab. 2021 Jul;49:101218. doi: 10.1016/j.molmet.2021.101218. Epub 2021 Mar 22. PMID: 33766732; PMCID: PMC8093934.

Kong MS, Zweifel LS. Central amygdala circuits in valence and salience processing. Behav Brain Res. 2021 Jul 23;410:113355. doi: 10.1016/j.bbr.2021.113355. Epub 2021 May 11. PMID: 33989728; PMCID: PMC8178205.

Schindler AG, Baskin B, Juarez B, Janet Lee S, Hendrickson R, Pagulayan K, Zweifel LS, Raskind MA, Phillips PEM, Peskind ER, Cook DG. Repetitive blast mild traumatic brain injury increases ethanol sensitivity in male mice and risky drinking behavior in male combat veterans. Alcohol Clin Exp Res. 2021 May;45(5):1051-1064. doi: 10.1111/acer.14605. Epub 2021 Apr 9. PMID: 33760264; PMCID: PMC8936060.

Carlson ES, Hunker AC, Sandberg SG, Locke TM, Geller JM, Schindler AG, Thomas SA, Darvas M, Phillips PEM, Zweifel LS. Catecholaminergic Innervation of the Lateral Nucleus of the Cerebellum Modulates Cognitive Behaviors. J Neurosci. 2021 Apr 14;41(15):3512-3530. doi: 10.1523/JNEUROSCI.2406-20.2021. Epub 2021 Feb 3. PMID: 33536201; PMCID: PMC8051686.

Baird MA, Hsu TY, Wang R, Juarez B, Zweifel LS. κ Opioid Receptor-Dynorphin Signaling in the Central Amygdala Regulates Conditioned Threat Discrimination and Anxiety. eNeuro. 2021 Feb 4;8(1):ENEURO.0370-20.2020. doi: 10.1523/ENEURO.0370-20.2020. PMID: 33323398; PMCID: PMC7877472.

Locke TM, Fujita H, Hunker A, Johanson SS, Darvas M, du Lac S, Zweifel LS, Carlson ES. Purkinje Cell-Specific Knockout of Tyrosine Hydroxylase Impairs Cognitive Behaviors. Front Cell Neurosci. 2020 Jul 29;14:228. doi: 10.3389/fncel.2020.00228. PMID: 32848620; PMCID: PMC7403473.

Hunker AC, Zweifel LS. Protocol to Design, Clone, and Validate sgRNAs for In Vivo Reverse Genetic Studies. STAR Protoc. 2020 Sep 18;1(2):100070. doi: 10.1016/j.xpro.2020.100070. Epub 2020 Jul 22. PMID: 33043306; PMCID: PMC7544006.

Soden ME, Chung AS, Cuevas B, Resnick JM, Awatramani R, Zweifel LS. Anatomic resolution of neurotransmitter-specific projections to the VTA reveals diversity of GABAergic inputs. Nat Neurosci. 2020 Aug;23(8):968-980. doi: 10.1038/s41593-020-0657-z. Epub 2020 Jun 15. PMID: 32541962; PMCID: PMC7927312.

Hunker AC, Soden ME, Krayushkina D, Heymann G, Awatramani R, Zweifel LS. Conditional Single Vector CRISPR/SaCas9 Viruses for Efficient Mutagenesis in the Adult Mouse Nervous System. Cell Rep. 2020 Mar 24;30(12):4303-4316.e6. doi: 10.1016/j.celrep.2020.02.092. PMID: 32209486; PMCID: PMC7212805.

Heymann G, Jo YS, Reichard KL, McFarland N, Chavkin C, Palmiter RD, Soden ME, Zweifel LS. Synergy of Distinct Dopamine Projection Populations in Behavioral Reinforcement. Neuron. 2020 Mar 4;105(5):909-920.e5. doi: 10.1016/j.neuron.2019.11.024. Epub 2019 Dec 23. PMID: 31879163; PMCID: PMC7060117.

Miller SM, Marcotulli D, Shen A, Zweifel LS. Divergent medial amygdala projections regulate approach-avoidance conflict behavior. Nat Neurosci. 2019 Apr;22(4):565-575. doi: 10.1038/s41593-019-0337-z. Epub 2019 Feb 25. PMID: 30804529; PMCID: PMC6446555.

Jo YS, Heymann G, Zweifel LS. Dopamine Neurons Reflect the Uncertainty in Fear Generalization. Neuron. 2018 Nov 21;100(4):916-925.e3. doi: 10.1016/j.neuron.2018.09.028. Epub 2018 Oct 11. PMID: 30318411; PMCID: PMC6226002.

Locke TM, Soden ME, Miller SM, Hunker A, Knakal C, Licholai JA, Dhillon KS, Keene CD, Zweifel LS, Carlson ES. Dopamine D1 Receptor-Positive Neurons in the Lateral Nucleus of the Cerebellum Contribute to Cognitive Behavior. Biol Psychiatry. 2018 Sep 15;84(6):401-412. doi: 10.1016/j.biopsych.2018.01.019. Epub 2018 Feb 2. PMID: 29478701; PMCID: PMC6072628.

Guo N, Soden ME, Herber C, Kim MT, Besnard A, Lin P, Ma X, Cepko CL, Zweifel LS, Sahay A. Dentate granule cell recruitment of feedforward inhibition governs engram maintenance and remote memory generalization. Nat Med. 2018 May;24(4):438-449. doi: 10.1038/nm.4491. Epub 2018 Mar 12. PMID: 29529016; PMCID: PMC5893385.

Chung AS, Miller SM, Sun Y, Xu X, Zweifel LS. Sexual congruency in the connectome and translatome of VTA dopamine neurons. Sci Rep. 2017 Sep 11;7(1):11120. doi: 10.1038/s41598-017-11478-5. PMID: 28894175; PMCID: PMC5593921.

Li J, Baird MA, Davis MA, Tai W, Zweifel LS, Adams Waldorf KM, Gale M Jr, Rajagopal L, Pierce RH, Gao X. Dramatic enhancement of the detection limits of bioassays via ultrafast deposition of polydopamine. Nat Biomed Eng. 2017;1:0082. doi: 10.1038/s41551-017-0082. Epub 2017 Jun 5. PMID: 29082104; PMCID: PMC5654575.

Gore BB, Miller SM, Jo YS, Baird MA, Hoon M, Sanford CA, Hunker A, Lu W, Wong RO, Zweifel LS. Roundabout receptor 2 maintains inhibitory control of the adult midbrain. Elife. 2017 Apr 10;6:e23858. doi: 10.7554/eLife.23858. PMID: 28394253; PMCID: PMC5419739.

Sanford CA, Soden ME, Baird MA, Miller SM, Schulkin J, Palmiter RD, Clark M, Zweifel LS. A Central Amygdala CRF Circuit Facilitates Learning about Weak Threats. Neuron. 2017 Jan 4;93(1):164-178. doi: 10.1016/j.neuron.2016.11.034. Epub 2016 Dec 22. PMID: 28017470; PMCID: PMC5217711.

Soden ME, Miller SM, Burgeno LM, Phillips PEM, Hnasko TS, Zweifel LS. Genetic Isolation of Hypothalamic Neurons that Regulate Context-Specific Male Social Behavior. Cell Rep. 2016 Jul 12;16(2):304-313. doi: 10.1016/j.celrep.2016.05.067. Epub 2016 Jun 23. PMID: 27346361; PMCID: PMC4945459.

Schindler AG, Soden ME, Zweifel LS, Clark JJ. Reversal of Alcohol-Induced Dysregulation in Dopamine Network Dynamics May Rescue Maladaptive Decision-making. J Neurosci. 2016 Mar 30;36(13):3698-708. doi: 10.1523/JNEUROSCI.4394-15.2016. PMID: 27030756; PMCID: PMC4812130.

Padilla SL, Qiu J, Soden ME, Sanz E, Nestor CC, Barker FD, Quintana A, Zweifel LS, Rønnekleiv OK, Kelly MJ, Palmiter RD. Agouti-related peptide neural circuits mediate adaptive behaviors in the starved state. Nat Neurosci. 2016 May;19(5):734-741. doi: 10.1038/nn.4274. Epub 2016 Mar 28. PMID: 27019015; PMCID: PMC4846501.

Jones GL, Soden ME, Knakal CR, Lee H, Chung AS, Merriam EB, Zweifel LS. A genetic link between discriminative fear coding by the lateral amygdala, dopamine, and fear generalization. Elife. 2015 Sep 24;4:e08969. doi: 10.7554/eLife.08969. PMID: 26402461; PMCID: PMC4621744.

Ehrich JM, Messinger DI, Knakal CR, Kuhar JR, Schattauer SS, Bruchas MR, Zweifel LS, Kieffer BL, Phillips PE, Chavkin C. Kappa Opioid Receptor-Induced Aversion Requires p38 MAPK Activation in VTA Dopamine Neurons. J Neurosci. 2015 Sep 16;35(37):12917-31. doi: 10.1523/JNEUROSCI.2444-15.2015. PMID: 26377476; PMCID: PMC4571610.

Han S, Soleiman MT, Soden ME, Zweifel LS, Palmiter RD. Elucidating an Affective Pain Circuit that Creates a Threat Memory. Cell. 2015 Jul 16;162(2):363-374. doi: 10.1016/j.cell.2015.05.057. PMID: 26186190; PMCID: PMC4512641.

Gore BB, Soden ME, Zweifel LS. Visualization of plasticity in fear-evoked calcium signals in midbrain dopamine neurons. Learn Mem. 2014 Oct 15;21(11):575-9. doi: 10.1101/lm.036079.114. PMID: 25320348; PMCID: PMC4201808.

Carter ME, Soden ME, Zweifel LS, Palmiter RD. Genetic identification of a neural circuit that suppresses appetite. Nature. 2013 Nov 7;503(7474):111-4. doi: 10.1038/nature12596. Epub 2013 Oct 13. PMID: 24121436; PMCID: PMC3878302.

Soden ME, Jones GL, Sanford CA, Chung AS, Güler AD, Chavkin C, Luján R, Zweifel LS. Disruption of dopamine neuron activity pattern regulation through selective expression of a human KCNN3 mutation. Neuron. 2013 Nov 20;80(4):997-1009. doi: 10.1016/j.neuron.2013.07.044. Epub 2013 Oct 24. PMID: 24206670; PMCID: PMC3840077.

Gore BB, Soden ME, Zweifel LS. Manipulating gene expression in projection-specific neuronal populations using combinatorial viral approaches. Curr Protoc Neurosci. 2013;65(435):4.35.1-20. doi: 10.1002/0471142301.ns0435s65. PMID: 25429312; PMCID: PMC4242517.

Parker JG, Wanat MJ, Soden ME, Ahmad K, Zweifel LS, Bamford NS, Palmiter RD. Attenuating GABA(A) receptor signaling in dopamine neurons selectively enhances reward learning and alters risk preference in mice. J Neurosci. 2011 Nov 23;31(47):17103-12. doi: 10.1523/JNEUROSCI.1715-11.2011. PMID: 22114279; PMCID: PMC3235504.

a) Ongoing Research Support

1. R01MH104450, NIMH, 3/2015-3/2025, Zweifel (PI). Phasic dopamine and symptom domains of mental illness. The goal of this project is to establish how mutations in human genes encoding ion channels that are associated with mental illness impact dopamine neuron activity pattern regulation and behavioral function when selectively expressed in mouse dopamine neurons.

2. R01DA044315, NIDA, 3/2018-2/2023, Zweifel (PI). Isolation of brain reward circuits using peptidergic systems. The goal of this project is to utilize genetic strategies in mice to isolate dopamine neurons with distinct projection patterns based on neuropeptide and neuropeptide receptor expression. Using this approach, we aim to establish the contribution of dopamine subpopulations to reinforcement learning and aversive memory formation.

3. P30 DA048736, 7/2019-6/2024, Zweifel (Core Director/Co-I)/Chavkin (Admin PI). University of Washington Center of Excellence in Opioid Addiction Research/ Molecular Genetics Resource Core. The purpose of this Center is to provide molecular genetics resources for investigators at the University of Washington to facilitate studies into the genetic and molecular basis of opioid addiction.

b) Completed Research Support

1. R21MH098177, NIMH, 8/2012-7/2014, Zweifel (PI). Cell type-specific calcium imaging during hippocampus-dependent memory. The goal of this project is to establish a method for live imaging of calcium dynamics in select cell types of the hippocampus during fear conditioning.

2. UW Innovator, University of Washington, 1/2015-1/2017, Zweifel (PI). Connection specific site directed genome engineering in the adult nervous system. The goal of this project was to establish viral-mediated CRISPR/saCas9 genome editing strategies in dopamine neurons making specific connections in the brain of the mouse.

3. R01MH094536, NIMH Biobehavioral Research Award for Innovative New Scientists (BRAINS Award), 9/2011-8/2017, Zweifel (PI). Functional mapping of dopamine-dependent fear circuitry using genetic and neural imaging techniques. The goal of this project was to establish in vivo calcium imaging techniques to monitor activity in midbrain dopamine neurons in the freely behaving mouse.

4. NARSAD Independent Investigator Grant, 9/2016-8-2018, Zweifel (PI). Differential genetic control of dopamine neuron activity patterns and behavioral regulation. The goal of this project was to establish a viral-mediated CRISPR/saCas9 strategy for inactivation of ion channels and related genes in midbrain dopamine neurons associated with mental illness.

5. P50MH106428, NIMH, 4/2015-3/2020, Zweifel (Project Leader). Center title: Stress mechanisms increasing risk of mood disorders. Project title: Circuit dissection of dopamine and serotonin interactions in depression. The goal of this project is to determine how serotonin inputs from the dorsal raphe nucleus to the ventral tegmental area regulate dopamine neuron activity and contribute to behaviors relevant to depression-like phenotypes in mice.

6. R01MH105427, NIMH, 7/2015-3/2020, Zweifel (Co-Investigator). Inhibitory neurons circuit organization and function in prefrontal cortex. The goal of this project is two establish how parvalbumin and somatostatin interneurons in the prefrontal cortex of mice regulate network activity to regulate learning and memory and to establish the role of specific long-range connections to these cells in behavioral regulation.

7. 1R56MH116938, NIDA, 9/2018-8/2019, Zweifel (Admin PI, MPI). Common neural circuits of anorexia and fear. This project aims to establish how a common population of neurons in the parabrachial nucleus of the hindbrain regulate conditioned taste aversion and conditioned fear through distinct and overlapping circuit connections in the mouse.

8. R21DA047626, 7/2019-6/2021, Zweifel (MPI)/Stella (Admin PI). ABHD6 and amphetamine stimulated locomotion. The goals of this project are to elucidate interactions between the endocannabinoid hydrolyzing enzyme, ABHD6, dopamine release, and amphetamine stimulated locomotor activity.

9. 573779, SFARI Research Award, Simons Foundation, 10/2018-9/2021 Zweifel (Admin PI, MPI). Pathogenic gating pore current in autism. The goals of this project are to establish how de novo mutations in human ion channel genes associated with neurodevelopmental disorders impact neural physiology in function. We identified recurrent mutations in gating charges in numerous voltage-gated ion channels and seek to determine whether these mutations lead to a common manifestation of gating pore currents.