NIDA Trainee Publications (Past 5 Years)

1: Todd WD, Venner A, Anaclet C, Broadhurst RY, De Luca R, Bandaru SS, Issokson
L, Hablitz LM, Cravetchi O, Arrigoni E, Campbell JN, Allen CN, Olson DP, Fuller
PM. Suprachiasmatic VIP neurons are required for normal circadian rhythmicity
and comprised of molecularly distinct subpopulations. Nat Commun. 2020 Sep
2;11(1):4410. doi: 10.1038/s41467-020-17197-2. PMID: 32879310; PMCID:
PMC7468160.

2: Reed C, Stafford AM, Mootz JRK, Baba H, Erk J, Phillips TJ. A breeding
strategy to identify modifiers of high genetic risk for methamphetamine intake.
Genes Brain Behav. 2020 May 18:e12667. doi: 10.1111/gbb.12667. Epub ahead of
print. PMID: 32424970; PMCID: PMC7671946.

3: Jacobs DS, Moghaddam B. Prefrontal Cortex Representation of Learning of
Punishment Probability During Reward-Motivated Actions. J Neurosci. 2020 Jun
24;40(26):5063-5077. doi: 10.1523/JNEUROSCI.0310-20.2020. Epub 2020 May 14.
PMID: 32409619; PMCID: PMC7314405.

4: Leff ER, Arttamangkul S, Williams JT. Chronic Treatment with Morphine
Disrupts Acute Kinase-Dependent Desensitization of GPCRs. Mol Pharmacol. 2020
Oct;98(4):497-507. doi: 10.1124/mol.119.119362. Epub 2020 May 3. PMID: 32362586;
PMCID: PMC7562982.

5: Bouchet CA, Ingram SL. Cannabinoids in the descending pain modulatory
circuit: Role in inflammation. Pharmacol Ther. 2020 May;209:107495. doi:
10.1016/j.pharmthera.2020.107495. Epub 2020 Jan 29. PMID: 32004514; PMCID:
PMC7183429.

6: Hablitz LM, Gunesch AN, Cravetchi O, Moldavan M, Allen CN. Cannabinoid
Signaling Recruits Astrocytes to Modulate Presynaptic Function in the
Suprachiasmatic Nucleus. eNeuro. 2020 Feb 13;7(1):ENEURO.0081-19.2020. doi:
10.1523/ENEURO.0081-19.2020. PMID: 31964686; PMCID: PMC7029187.

7: Mootz JRK, Miner NB, Phillips TJ. Differential genetic risk for
methamphetamine intake confers differential sensitivity to the temperature-
altering effects of other addictive drugs. Genes Brain Behav. 2020
Jun;19(5):e12640. doi: 10.1111/gbb.12640. Epub 2020 Jan 15. PMID: 31925906;
PMCID: PMC7286770.

8: Dennis LE, Kohno M, McCready HD, Schwartz DL, Schwartz B, Lahna D, Nagel BJ,
Mitchell SH, Hoffman WF. Neural correlates of reward magnitude and delay during
a probabilistic delay discounting task in alcohol use disorder.
Psychopharmacology (Berl). 2020 Jan;237(1):263-278. doi:
10.1007/s00213-019-05364-3. Epub 2019 Oct 31. Erratum in: Psychopharmacology
(Berl). 2019 Dec 21;: PMID: 31673722; PMCID: PMC6991625.

9: Kohno M, Morales AM, Dennis LE, McCready H, Hoffman WF, Korthuis PT. Effects
of Naltrexone on Large-Scale Network Interactions in Methamphetamine Use
Disorder. Front Psychiatry. 2019 Sep 3;10:603. doi: 10.3389/fpsyt.2019.00603.
PMID: 31551824; PMCID: PMC6735261.

10: Williams AR, Kim ES, Lattal KM. Behavioral and immunohistochemical
characterization of rapid reconditioning following extinction of contextual
fear. Learn Mem. 2019 Sep 16;26(10):1-16. doi: 10.1101/lm.048439.118. PMID:
31527183; PMCID: PMC6749931.

11: Shi X, Swanson TL, Miner NB, Eshleman AJ, Janowsky A. Activation of Trace
Amine-Associated Receptor 1 Stimulates an Antiapoptotic Signal Cascade via
Extracellular Signal-Regulated Kinase 1/2. Mol Pharmacol. 2019
Oct;96(4):493-504. doi: 10.1124/mol.119.116798. Epub 2019 Aug 13. PMID:
31409621; PMCID: PMC6744391.

12: Arttamangkul S, Leff ER, Koita O, Birdsong WT, Williams JT. Separation of
Acute Desensitization and Long-Term Tolerance of <i>µ</i>-Opioid Receptors Is
Determined by the Degree of C-Terminal Phosphorylation. Mol Pharmacol. 2019
Oct;96(4):505-514. doi: 10.1124/mol.119.117358. Epub 2019 Aug 5. PMID: 31383769;
PMCID: PMC6750191.

13: Kim ES, Lattal KM. Context-Dependent and Context-Independent Effects of D1
Receptor Antagonism in the Basolateral and Central Amygdala during Cocaine Self-
Administration. eNeuro. 2019 Aug 13;6(4):ENEURO.0203-19.2019. doi:
10.1523/ENEURO.0203-19.2019. PMID: 31358512; PMCID: PMC6712201.

14: Miner NB, Phillips TJ, Janowsky A. The Role of Biogenic Amine Transporters
in Trace Amine-Associated Receptor 1 Regulation of Methamphetamine-Induced
Neurotoxicity. J Pharmacol Exp Ther. 2019 Oct;371(1):36-44. doi:
10.1124/jpet.119.258970. Epub 2019 Jul 18. PMID: 31320495; PMCID: PMC6750185.

15: Stafford AM, Reed C, Baba H, Walter NA, Mootz JR, Williams RW, Neve KA,
Fedorov LM, Janowsky AJ, Phillips TJ. <i>Taar1</i> gene variants have a causal
role in methamphetamine intake and response and interact with <i>Oprm1</i>.
Elife. 2019 Jul 9;8:e46472. doi: 10.7554/eLife.46472. PMID: 31274109; PMCID:
PMC6682400.

16: Kohno M, Link J, Dennis LE, McCready H, Huckans M, Hoffman WF, Loftis JM.
Neuroinflammation in addiction: A review of neuroimaging studies and potential
immunotherapies. Pharmacol Biochem Behav. 2019 Apr;179:34-42. doi:
10.1016/j.pbb.2019.01.007. Epub 2019 Jan 26. PMID: 30695700; PMCID: PMC6637953.

17: Hitchcock LN, Raybuck JD, Wood MA, Lattal KM. Effects of a histone
deacetylase 3 inhibitor on extinction and reinstatement of cocaine self-
administration in rats. Psychopharmacology (Berl). 2019 Jan;236(1):517-529. doi:
10.1007/s00213-018-5122-2. Epub 2018 Nov 28. PMID: 30488346; PMCID: PMC6459190.

18: McCready H, Kohno M, Kolessar M, Dennis L, Kriz D, Luber H, Anderson R,
Chang M, Sasaki A, Flora K, Vandenbark A, Mitchell SH, Loftis JM, Hoffman WF,
Huckans M. Functional MRI and delay discounting in patients infected with
hepatitis C. J Neurovirol. 2018 Dec;24(6):738-751. doi:
10.1007/s13365-018-0670-0. Epub 2018 Oct 8. PMID: 30298201; PMCID: PMC6279508.

19: Kohno M, Dennis LE, McCready H, Schwartz DL, Hoffman WF, Korthuis PT. A
preliminary randomized clinical trial of naltrexone reduces striatal resting
state functional connectivity in people with methamphetamine use disorder. Drug
Alcohol Depend. 2018 Nov 1;192:186-192. doi: 10.1016/j.drugalcdep.2018.07.045.
Epub 2018 Sep 21. PMID: 30266003; PMCID: PMC6200637.

20: Mills BD, Miranda-Dominguez O, Mills KL, Earl E, Cordova M, Painter J,
Karalunas SL, Nigg JT, Fair DA. ADHD and attentional control: Impaired
segregation of task positive and task negative brain networks. Netw Neurosci.
2018 Jun 1;2(2):200-217. doi: 10.1162/netn_a_00034. PMID: 30215033; PMCID:
PMC6130439.

21: Walsh SM, Mathiasen S, Christensen SM, Fay JF, King C, Provasi D, Borrero E,
Rasmussen SGF, Fung JJ, Filizola M, Hristova K, Kobilka B, Farrens DL, Stamou D.
Single Proteoliposome High-Content Analysis Reveals Differences in the Homo-
Oligomerization of GPCRs. Biophys J. 2018 Jul 17;115(2):300-312. doi:
10.1016/j.bpj.2018.05.036. PMID: 30021106; PMCID: PMC6050755.

22: Mills BD, Grayson DS, Shunmugavel A, Miranda-Dominguez O, Feczko E, Earl E,
Neve KA, Fair DA. Correlated Gene Expression and Anatomical Communication
Support Synchronized Brain Activity in the Mouse Functional Connectome. J
Neurosci. 2018 Jun 20;38(25):5774-5787. doi: 10.1523/JNEUROSCI.2910-17.2018.
Epub 2018 May 22. PMID: 29789379; PMCID: PMC6010566.

23: Kohno M, Loftis JM, Huckans M, Dennis LE, McCready H, Hoffman WF. The
relationship between interleukin-6 and functional connectivity in
methamphetamine users. Neurosci Lett. 2018 Jun 11;677:49-54. doi:
10.1016/j.neulet.2018.04.037. Epub 2018 Apr 22. PMID: 29689344; PMCID:
PMC5971003.

24: Reed C, Baba H, Zhu Z, Erk J, Mootz JR, Varra NM, Williams RW, Phillips TJ.
A Spontaneous Mutation in <i>Taar1</i> Impacts Methamphetamine-Related Traits
Exclusively in DBA/2 Mice from a Single Vendor. Front Pharmacol. 2018 Jan
22;8:993. doi: 10.3389/fphar.2017.00993. PMID: 29403379; PMCID: PMC5786530.

25: Hitchcock LN, Lattal KM. Involvement of the dorsal hippocampus in expression
and extinction of cocaine-induced conditioned place preference. Hippocampus.
2018 Mar;28(3):226-238. doi: 10.1002/hipo.22826. Epub 2018 Feb 2. PMID:
29341327; PMCID: PMC5916867.

26: Robinson BG, Condon AF, Radl D, Borrelli E, Williams JT, Neve KA. Cocaine-
induced adaptation of dopamine D2S, but not D2L autoreceptors. Elife. 2017 Nov
20;6:e31924. doi: 10.7554/eLife.31924. PMID: 29154756; PMCID: PMC5695907.

27: Eastwood EC, Eshleman AJ, Janowsky A, Phillips TJ. Verification of a genetic
locus for methamphetamine intake and the impact of morphine. Mamm Genome. 2018
Apr;29(3-4):260-272. doi: 10.1007/s00335-017-9724-5. Epub 2017 Nov 10. PMID:
29127441; PMCID: PMC5889309.

28: Kohno M, Dennis LE, McCready H, Hoffman WF. Executive Control and Striatal
Resting-State Network Interact with Risk Factors to Influence Treatment Outcomes
in Alcohol-Use Disorder. Front Psychiatry. 2017 Sep 25;8:182. doi:
10.3389/fpsyt.2017.00182. PMID: 28993741; PMCID: PMC5622290.

29: Miner NB, Elmore JS, Baumann MH, Phillips TJ, Janowsky A. Trace amine-
associated receptor 1 regulation of methamphetamine-induced neurotoxicity.
Neurotoxicology. 2017 Dec;63:57-69. doi: 10.1016/j.neuro.2017.09.006. Epub 2017
Sep 15. PMID: 28919515; PMCID: PMC5683899.

30: Impey S, Jopson T, Pelz C, Tafessu A, Fareh F, Zuloaga D, Marzulla T,
Riparip LK, Stewart B, Rosi S, Turker MS, Raber J. Bi-directional and shared
epigenomic signatures following proton and <sup>56</sup>Fe irradiation. Sci Rep.
2017 Aug 31;7(1):10227. doi: 10.1038/s41598-017-09191-4. PMID: 28860502; PMCID:
PMC5579159.

31: Pizzimenti CL, Navis TM, Lattal KM. Persistent effects of acute stress on
fear and drug-seeking in a novel model of the comorbidity between post-traumatic
stress disorder and addiction. Learn Mem. 2017 Aug 16;24(9):422-431. doi:
10.1101/lm.044164.116. PMID: 28814468; PMCID: PMC5580533.

32: Fay JF, Farrens DL. Purification of Functional CB<sub>1</sub> and Analysis
by Site-Directed Fluorescence Labeling Methods. Methods Enzymol.
2017;593:343-370. doi: 10.1016/bs.mie.2017.06.026. Epub 2017 Jul 17. PMID:
28750810.

33: Shorey-Kendrick LE, McEvoy CT, Ferguson B, Burchard J, Park BS, Gao L,
Vuylsteke BH, Milner KF, Morris CD, Spindel ER. Vitamin C Prevents Offspring DNA
Methylation Changes Associated with Maternal Smoking in Pregnancy. Am J Respir
Crit Care Med. 2017 Sep 15;196(6):745-755. doi: 10.1164/rccm.201610-2141OC.
PMID: 28422514; PMCID: PMC5620677.

34: Jimenez VA, Allen DC, McClintick MN, Grant KA. Social setting, social rank
and HPA axis response in cynomolgus monkeys. Psychopharmacology (Berl). 2017
Jun;234(12):1881-1889. doi: 10.1007/s00213-017-4596-7. Epub 2017 Mar 22. PMID:
28332004; PMCID: PMC5451300.

35: Johnson LA, Torres ER, Impey S, Stevens JF, Raber J. Apolipoprotein E4 and
Insulin Resistance Interact to Impair Cognition and Alter the Epigenome and
Metabolome. Sci Rep. 2017 Mar 8;7:43701. doi: 10.1038/srep43701. PMID: 28272510;
PMCID: PMC5341123.

36: Miner NB, O'Callaghan JP, Phillips TJ, Janowsky A. The combined effects of
3,4-methylenedioxymethamphetamine (MDMA) and selected substituted methcathinones
on measures of neurotoxicity. Neurotoxicol Teratol. 2017 May;61:74-81. doi:
10.1016/j.ntt.2017.02.003. Epub 2017 Feb 16. PMID: 28212938; PMCID: PMC5453829.

37: Su W, Foster SC, Xing R, Feistel K, Olsen RH, Acevedo SF, Raber J, Sherman
LS. CD44 Transmembrane Receptor and Hyaluronan Regulate Adult Hippocampal Neural
Stem Cell Quiescence and Differentiation. J Biol Chem. 2017 Mar
17;292(11):4434-4445. doi: 10.1074/jbc.M116.774109. Epub 2017 Jan 31. PMID:
28154169; PMCID: PMC5377763.

38: Yorgason JT, Zeppenfeld DM, Williams JT. Cholinergic Interneurons Underlie
Spontaneous Dopamine Release in Nucleus Accumbens. J Neurosci. 2017 Feb
22;37(8):2086-2096. doi: 10.1523/JNEUROSCI.3064-16.2017. Epub 2017 Jan 23. PMID:
28115487; PMCID: PMC5338756.

39: Buck JM, Morris AS, Weber SJ, Raber J, Siegel JA. Effects of adolescent
methamphetamine and nicotine exposure on behavioral performance and MAP-2
immunoreactivity in the nucleus accumbens of adolescent mice. Behav Brain Res.
2017 Apr 14;323:78-85. doi: 10.1016/j.bbr.2017.01.010. Epub 2017 Jan 12. PMID:
28089854; PMCID: PMC5919189.

40: Vaaga CE, Yorgason JT, Williams JT, Westbrook GL. Presynaptic gain control
by endogenous cotransmission of dopamine and GABA in the olfactory bulb. J
Neurophysiol. 2017 Mar 1;117(3):1163-1170. doi: 10.1152/jn.00694.2016. Epub 2016
Dec 28. PMID: 28031402; PMCID: PMC5340883.

41: McGinnis GJ, Friedman D, Young KH, Torres ER, Thomas CR Jr, Gough MJ, Raber
J. Neuroinflammatory and cognitive consequences of combined radiation and
immunotherapy in a novel preclinical model. Oncotarget. 2017 Feb
7;8(6):9155-9173. doi: 10.18632/oncotarget.13551. PMID: 27893434; PMCID:
PMC5354722.

42: Impey S, Jopson T, Pelz C, Tafessu A, Fareh F, Zuloaga D, Marzulla T,
Riparip LK, Stewart B, Rosi S, Turker MS, Raber J. Short- and long-term effects
of <sup>56</sup>Fe irradiation on cognition and hippocampal DNA methylation and
gene expression. BMC Genomics. 2016 Oct 24;17(1):825. doi:
10.1186/s12864-016-3110-7. PMID: 27776477; PMCID: PMC5078898.

43: Abraham AD, Neve KA, Lattal KM. Effects of D1 receptor knockout on fear and
reward learning. Neurobiol Learn Mem. 2016 Sep;133:265-273. doi:
10.1016/j.nlm.2016.07.010. Epub 2016 Jul 14. PMID: 27423521; PMCID: PMC5001556.

44: Shi X, Walter NA, Harkness JH, Neve KA, Williams RW, Lu L, Belknap JK,
Eshleman AJ, Phillips TJ, Janowsky A. Genetic Polymorphisms Affect Mouse and
Human Trace Amine-Associated Receptor 1 Function. PLoS One. 2016 Mar
31;11(3):e0152581. doi: 10.1371/journal.pone.0152581. PMID: 27031617; PMCID:
PMC4816557.

45: Zuloaga DG, Wang J, Weber S, Mark GP, Murphy SJ, Raber J. Chronic
methamphetamine exposure prior to middle cerebral artery occlusion increases
infarct volume and worsens cognitive injury in Male mice. Metab Brain Dis. 2016
Aug;31(4):975-81. doi: 10.1007/s11011-016-9808-z. Epub 2016 Mar 28. PMID:
27021292; PMCID: PMC5940345.

46: Tipps ME, Raybuck JD, Kozell LB, Lattal KM, Buck KJ. G Protein-Gated
Inwardly Rectifying Potassium Channel Subunit 3 Knock-Out Mice Show Enhanced
Ethanol Reward. Alcohol Clin Exp Res. 2016 Apr;40(4):857-64. doi:
10.1111/acer.13012. Epub 2016 Mar 25. Erratum in: Alcohol Clin Exp Res. 2016
Oct;40(10 ):2253. PMID: 27012303; PMCID: PMC4820358.

47: Zuloaga DG, Lahvis GP, Mills B, Pearce HL, Turner J, Raber J. Fetal domoic
acid exposure affects lateral amygdala neurons, diminishes social investigation
and alters sensory-motor gating. Neurotoxicology. 2016 Mar;53:132-140. doi:
10.1016/j.neuro.2016.01.007. Epub 2016 Jan 18. PMID: 26797589; PMCID:
PMC5929993.

48: Abraham AD, Neve KA, Lattal KM. Activation of D1/5 Dopamine Receptors: A
Common Mechanism for Enhancing Extinction of Fear and Reward-Seeking Behaviors.
Neuropsychopharmacology. 2016 Jul;41(8):2072-81. doi: 10.1038/npp.2016.5. Epub
2016 Jan 14. PMID: 26763483; PMCID: PMC4908654.

49: Zuloaga DG, Johnson LA, Weber S, Raber J. Immediate and lasting effects of
chronic daily methamphetamine exposure on activation of cells in hypothalamic-
pituitary-adrenal axis-associated brain regions. Psychopharmacology (Berl). 2016
Feb;233(3):381-92. doi: 10.1007/s00213-015-4114-8. Epub 2015 Nov 2. PMID:
26525566; PMCID: PMC4815259.

50: Kugelman T, Zuloaga DG, Weber S, Raber J. Post-training gamma irradiation-
enhanced contextual fear memory associated with reduced neuronal activation of
the infralimbic cortex. Behav Brain Res. 2016 Feb 1;298(Pt B):1-11. doi:
10.1016/j.bbr.2015.10.050. Epub 2015 Oct 29. PMID: 26522840; PMCID: PMC4688165.