Glutamatergic synaptic transmission is the primary means of fast excitatory neural communication in the brain. Modulation of this transmission serves an important role in brain function. For example, long-term potentiation (LTP), a persistent modification of synaptic transmission elicited by bursts of synaptic activity has been postulated to play roles in memory storage. LTP is an appealing candidate for a cellular substrate for memory storage in part because, like memory, it is a lasting change to a transient stimulus. Another brain function that involves a similar lasting change in response to a transient stimulus is the transition from recreational drug use to addiction. Thus, research in my lab is directed toward determining how synaptic transmission is modulated by stress and substances of abuse, and the signal transduction cascades utilized. To accomplish this, we employ a variety of electrophysiological and biochemical techniques in brain slices. Through the use of regulatable systems to overexpress transgenes that interfere with regulation of transmission in key brain regions, studies are also planned to address the roles of modulation of glutamatergic transmission in processes such as addiction and anxiety.


The following timeline graph is generated from all co-authored publications.

Featured publications are shown below:

  1. α-adrenergic heteroreceptors are required for stress-induced reinstatement of cocaine conditioned place preference. Perez RE, Basu A, Nabit BP, Harris NA, Folkes OM, Patel S, Gilsbach R, Hein L, Winder DG (2020) Neuropsychopharmacology 45(9): 1473-1481
    › Primary publication · 32074627 (PubMed) · PMC7360592 (PubMed Central)
  2. Chronic Intermittent Ethanol and Acute Stress Similarly Modulate BNST CRF Neuron Activity via Noradrenergic Signaling. Snyder AE, Salimando GJ, Winder DG, Silberman Y (2019) Alcohol Clin Exp Res 43(8): 1695-1701
    › Primary publication · 31141179 (PubMed) · PMC6677590 (PubMed Central)
  3. Disabling the Gβγ-SNARE interaction disrupts GPCR-mediated presynaptic inhibition, leading to physiological and behavioral phenotypes. Zurawski Z, Thompson Gray AD, Brady LJ, Page B, Church E, Harris NA, Dohn MR, Yim YY, Hyde K, Mortlock DP, Jones CK, Winder DG, Alford S, Hamm HE (2019) Sci Signal 12(569)
    › Primary publication · 30783011 (PubMed) · PMC7758873 (PubMed Central)
  4. α-Adrenergic Receptor Activation Decreases Parabrachial Nucleus Excitatory Drive onto BNST CRF Neurons and Reduces Their Activity . Fetterly TL, Basu A, Nabit BP, Awad E, Williford KM, Centanni SW, Matthews RT, Silberman Y, Winder DG (2019) J Neurosci 39(3): 472-484
    › Primary publication · 30478032 (PubMed) · PMC6335747 (PubMed Central)
  5. Endocannabinoid control of the insular-bed nucleus of the stria terminalis circuit regulates negative affective behavior associated with alcohol abstinence. Centanni SW, Morris BD, Luchsinger JR, Bedse G, Fetterly TL, Patel S, Winder DG (2019) Neuropsychopharmacology 44(3): 526-537
    › Primary publication · 30390064 (PubMed) · PMC6333805 (PubMed Central)
  6. Noradrenergic Transmission at Alpha1-Adrenergic Receptors in the Ventral Periaqueductal Gray Modulates Arousal. Porter-Stransky KA, Centanni SW, Karne SL, Odil LM, Fekir S, Wong JC, Jerome C, Mitchell HA, Escayg A, Pedersen NP, Winder DG, Mitrano DA, Weinshenker D (2019) Biol Psychiatry 85(3): 237-247
    › Primary publication · 30269865 (PubMed) · PMC6326840 (PubMed Central)
  7. Dorsal BNST α-Adrenergic Receptors Produce HCN-Dependent Excitatory Actions That Initiate Anxiogenic Behaviors. Harris NA, Isaac AT, Günther A, Merkel K, Melchior J, Xu M, Eguakun E, Perez R, Nabit BP, Flavin S, Gilsbach R, Shonesy B, Hein L, Abel T, Baumann A, Matthews R, Centanni SW, Winder DG (2018) J Neurosci 38(42): 8922-8942
    › Primary publication · 30150361 (PubMed) · PMC6191524 (PubMed Central)
  8. Ketamine administration during a critical period after forced ethanol abstinence inhibits the development of time-dependent affective disturbances. Vranjkovic O, Winkler G, Winder DG (2018) Neuropsychopharmacology 43(9): 1915-1923
    › Primary publication · 29907878 (PubMed) · PMC6046046 (PubMed Central)
  9. Metabotropic Glutamate Receptors in Alcohol Use Disorder: Physiology, Plasticity, and Promising Pharmacotherapies. Joffe ME, Centanni SW, Jaramillo AA, Winder DG, Conn PJ (2018) ACS Chem Neurosci 9(9): 2188-2204
    › Primary publication · 29792024 (PubMed) · PMC6192262 (PubMed Central)
  10. Dorsolateral Striatum Engagement Interferes with Early Discrimination Learning. Bergstrom HC, Lipkin AM, Lieberman AG, Pinard CR, Gunduz-Cinar O, Brockway ET, Taylor WW, Nonaka M, Bukalo O, Wills TA, Rubio FJ, Li X, Pickens CL, Winder DG, Holmes A (2018) Cell Rep 23(8): 2264-2272
    › Primary publication · 29791838 (PubMed) · PMC6015733 (PubMed Central)
  11. Role of Striatal Direct Pathway 2-Arachidonoylglycerol Signaling in Sociability and Repetitive Behavior. Shonesy BC, Parrish WP, Haddad HK, Stephenson JR, Báldi R, Bluett RJ, Marks CR, Centanni SW, Folkes OM, Spiess K, Augustin SM, Mackie K, Lovinger DM, Winder DG, Patel S, Colbran RJ (2018) Biol Psychiatry 84(4): 304-315
    › Primary publication · 29458998 (PubMed) · PMC6023784 (PubMed Central)
  12. The Corticotropin Releasing Factor Receptor 1 in Alcohol Use Disorder: Still a Valid Drug Target? Pomrenze MB, Fetterly TL, Winder DG, Messing RO (2017) Alcohol Clin Exp Res 41(12): 1986-1999
    › Primary publication · 28940382 (PubMed) · PMC5711524 (PubMed Central)
  13. The bed nucleus of the stria terminalis in drug-associated behavior and affect: A circuit-based perspective. Vranjkovic O, Pina M, Kash TL, Winder DG (2017) Neuropharmacology : 100-106
    › Primary publication · 28351600 (PubMed) · PMC5481847 (PubMed Central)
  14. Endocannabinoid signalling modulates susceptibility to traumatic stress exposure. Bluett RJ, Báldi R, Haymer A, Gaulden AD, Hartley ND, Parrish WP, Baechle J, Marcus DJ, Mardam-Bey R, Shonesy BC, Uddin MJ, Marnett LJ, Mackie K, Colbran RJ, Winder DG, Patel S (2017) Nat Commun : 14782
    › Primary publication · 28348378 (PubMed) · PMC5379055 (PubMed Central)
  15. Coupling optogenetic stimulation with NanoLuc-based luminescence (BRET) Ca sensing. Yang J, Cumberbatch D, Centanni S, Shi SQ, Winder D, Webb D, Johnson CH (2016) Nat Commun : 13268
    › Primary publication · 27786307 (PubMed) · PMC5476805 (PubMed Central)
  16. Preclinical voluntary drinking models for alcohol abstinence-induced affective disturbances in mice. Holleran KM, Winder DG (2017) Genes Brain Behav 16(1): 8-14
    › Primary publication · 27621103 (PubMed)
  17. Changes in the Adult GluN2B Associated Proteome following Adolescent Intermittent Ethanol Exposure. Swartzwelder HS, Risher ML, Miller KM, Colbran RJ, Winder DG, Wills TA (2016) PLoS One 11(5): e0155951
    › Primary publication · 27213757 (PubMed) · PMC4877005 (PubMed Central)
  18. Ketamine and MAG Lipase Inhibitor-Dependent Reversal of Evolving Depressive-Like Behavior During Forced Abstinence From Alcohol Drinking. Holleran KM, Wilson HH, Fetterly TL, Bluett RJ, Centanni SW, Gilfarb RA, Rocco LE, Patel S, Winder DG (2016) Neuropsychopharmacology 41(8): 2062-71
    › Primary publication · 26751284 (PubMed) · PMC4908652 (PubMed Central)
  19. Chronic intermittent alcohol disrupts the GluN2B-associated proteome and specifically regulates group I mGlu receptor-dependent long-term depression. Wills TA, Baucum AJ, Holleran KM, Chen Y, Pasek JG, Delpire E, Tabb DL, Colbran RJ, Winder DG (2017) Addict Biol 22(2): 275-290
    › Primary publication · 26549202 (PubMed) · PMC4860359 (PubMed Central)
  20. Ethanol produces corticotropin-releasing factor receptor-dependent enhancement of spontaneous glutamatergic transmission in the mouse central amygdala. Silberman Y, Fetterly TL, Awad EK, Milano EJ, Usdin TB, Winder DG (2015) Alcohol Clin Exp Res 39(11): 2154-62
    › Primary publication · 26503065 (PubMed) · PMC4624256 (PubMed Central)
  21. The Anxiolytic Actions of 2-Arachidonoylglycerol: Converging Evidence From Two Recent Genetic Endocannabinoid Deficiency Models. Patel S, Shonesy BC, Bluett RJ, Winder DG, Colbran RJ (2016) Biol Psychiatry 79(10): e78-e79
    › Primary publication · 26212898 (PubMed)
  22. Ethanol and corticotropin releasing factor receptor modulation of central amygdala neurocircuitry: An update and future directions. Silberman Y, Winder DG (2015) Alcohol 49(3): 179-84
    › Primary publication · 25716197 (PubMed) · PMC4414799 (PubMed Central)
  23. Excitatory drive onto dopaminergic neurons in the rostral linear nucleus is enhanced by norepinephrine in an α1 adrenergic receptor-dependent manner. Williams MA, Li C, Kash TL, Matthews RT, Winder DG (2014) Neuropharmacology : 116-24
    › Primary publication · 25018040 (PubMed) · PMC4188726 (PubMed Central)
  24. α(2A)-adrenergic receptors filter parabrachial inputs to the bed nucleus of the stria terminalis. Flavin SA, Matthews RT, Wang Q, Muly EC, Winder DG (2014) J Neurosci 34(28): 9319-31
    › Primary publication · 25009265 (PubMed) · PMC4087209 (PubMed Central)
  25. Knockdown of BNST GluN2B-containing NMDA receptors mimics the actions of ketamine on novelty-induced hypophagia. Louderback KM, Wills TA, Muglia LJ, Winder DG (2013) Transl Psychiatry : e331
    › Primary publication · 24301649 (PubMed) · PMC4030322 (PubMed Central)
  26. Emerging role for corticotropin releasing factor signaling in the bed nucleus of the stria terminalis at the intersection of stress and reward. Silberman Y, Winder DG (2013) Front Psychiatry : 42
    › Primary publication · 23755023 (PubMed) · PMC3665954 (PubMed Central)
  27. Noradrenergic control of the bed nucleus of the stria terminalis in stress and reward. Flavin SA, Winder DG (2013) Neuropharmacology : 324-30
    › Primary publication · 23466330 (PubMed) · PMC3644325 (PubMed Central)
  28. A corticotropin releasing factor pathway for ethanol regulation of the ventral tegmental area in the bed nucleus of the stria terminalis. Silberman Y, Matthews RT, Winder DG (2013) J Neurosci 33(3): 950-60
    › Primary publication · 23325234 (PubMed) · PMC3566560 (PubMed Central)
  29. Yohimbine depresses excitatory transmission in BNST and impairs extinction of cocaine place preference through orexin-dependent, norepinephrine-independent processes. Conrad KL, Davis AR, Silberman Y, Sheffler DJ, Shields AD, Saleh SA, Sen N, Matthies HJ, Javitch JA, Lindsley CW, Winder DG (2012) Neuropsychopharmacology 37(10): 2253-66
    › Primary publication · 22617356 (PubMed) · PMC3422490 (PubMed Central)
  30. GluN2B subunit deletion reveals key role in acute and chronic ethanol sensitivity of glutamate synapses in bed nucleus of the stria terminalis. Wills TA, Klug JR, Silberman Y, Baucum AJ, Weitlauf C, Colbran RJ, Delpire E, Winder DG (2012) Proc Natl Acad Sci U S A 109(5): E278-87
    › Primary publication · 22219357 (PubMed) · PMC3277158 (PubMed Central)
  31. β-Adrenergic receptors enhance excitatory transmission in the bed nucleus of the stria terminalis through a corticotrophin-releasing factor receptor-dependent and cocaine-regulated mechanism. Nobis WP, Kash TL, Silberman Y, Winder DG (2011) Biol Psychiatry 69(11): 1083-90
    › Primary publication · 21334600 (PubMed) · PMC3090515 (PubMed Central)
  32. An odyssey of fear: Homer stresses new mechanisms. Patel S, Winder DG (2010) Biol Psychiatry 68(11): 980-1
    › Primary publication · 21075227 (PubMed) · PMC3035943 (PubMed Central)
  33. Distinct forms of Gq-receptor-dependent plasticity of excitatory transmission in the BNST are differentially affected by stress. McElligott ZA, Klug JR, Nobis WP, Patel S, Grueter BA, Kash TL, Winder DG (2010) Proc Natl Acad Sci U S A 107(5): 2271-6
    › Primary publication · 20133871 (PubMed) · PMC2836642 (PubMed Central)
  34. Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala. Patel S, Kingsley PJ, Mackie K, Marnett LJ, Winder DG (2009) Neuropsychopharmacology 34(13): 2699-709
    › Primary publication · 19675536 (PubMed) · PMC2881681 (PubMed Central)
  35. Alcohol exposure alters NMDAR function in the bed nucleus of the stria terminalis. Kash TL, Baucum AJ, Conrad KL, Colbran RJ, Winder DG (2009) Neuropsychopharmacology 34(11): 2420-9
    › Primary publication · 19553918 (PubMed) · PMC2864644 (PubMed Central)
  36. Dopamine enhances fast excitatory synaptic transmission in the extended amygdala by a CRF-R1-dependent process. Kash TL, Nobis WP, Matthews RT, Winder DG (2008) J Neurosci 28(51): 13856-65
    › Primary publication · 19091975 (PubMed) · PMC2630395 (PubMed Central)
  37. In vivo metabotropic glutamate receptor 5 (mGluR5) antagonism prevents cocaine-induced disruption of postsynaptically maintained mGluR5-dependent long-term depression. Grueter BA, McElligott ZA, Robison AJ, Mathews GC, Winder DG (2008) J Neurosci 28(37): 9261-70
    › Primary publication · 18784306 (PubMed) · PMC2562219 (PubMed Central)
  38. Neuropeptide Y and corticotropin-releasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis. Kash TL, Winder DG (2006) Neuropharmacology 51(5): 1013-22
    › Primary publication · 16904135 (PubMed)
  39. A method for single-session cocaine self-administration in the mouse. Olsen CM, Winder DG (2006) Psychopharmacology (Berl) 187(1): 13-21
    › Primary publication · 16767412 (PubMed)
  40. Extracellular-signal regulated kinase 1-dependent metabotropic glutamate receptor 5-induced long-term depression in the bed nucleus of the stria terminalis is disrupted by cocaine administration. Grueter BA, Gosnell HB, Olsen CM, Schramm-Sapyta NL, Nekrasova T, Landreth GE, Winder DG (2006) J Neurosci 26(12): 3210-9
    › Primary publication · 16554472 (PubMed) · PMC6674094 (PubMed Central)
  41. Novel blockade of protein kinase A-mediated phosphorylation of AMPA receptors. Vanhoose AM, Clements JM, Winder DG (2006) J Neurosci 26(4): 1138-45
    › Primary publication · 16436600 (PubMed) · PMC6674559 (PubMed Central)
  42. Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptor-dependent long-term potentiation. Weitlauf C, Honse Y, Auberson YP, Mishina M, Lovinger DM, Winder DG (2005) J Neurosci 25(37): 8386-90
    › Primary publication · 16162920 (PubMed) · PMC6725680 (PubMed Central)
  43. Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis. Egli RE, Kash TL, Choo K, Savchenko V, Matthews RT, Blakely RD, Winder DG (2005) Neuropsychopharmacology 30(4): 657-68
    › Primary publication · 15602500 (PubMed)
  44. Roles of serine/threonine phosphatases in hippocampal synaptic plasticity. Winder DG, Sweatt JD (2001) Nat Rev Neurosci 2(7): 461-74
    › Primary publication · 11433371 (PubMed)
  45. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Malleret G, Haditsch U, Genoux D, Jones MW, Bliss TV, Vanhoose AM, Weitlauf C, Kandel ER, Winder DG, Mansuy IM (2001) Cell 104(5): 675-86
    › Primary publication · 11257222 (PubMed)
  46. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER (1999) Neuron 24(3): 715-26
    › Primary publication · 10595521 (PubMed)
  47. Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E (1998) Proc Natl Acad Sci U S A 95(25): 15020-5
    › Primary publication · 9844008 (PubMed) · PMC24568 (PubMed Central)
  48. Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER (1998) Cell 92(1): 25-37
    › Primary publication · 9489697 (PubMed)
  49. Novel glial-neuronal signalling by coactivation of metabotropic glutamate and beta-adrenergic receptors in rat hippocampus. Winder DG, Ritch PS, Gereau RW, Conn PJ (1996) J Physiol : 743-55
    › Primary publication · 8865071 (PubMed) · PMC1160674 (PubMed Central)
  50. Activation of metabotropic glutamate receptors increases cAMP accumulation in hippocampus by potentiating responses to endogenous adenosine. Winder DG, Conn PJ (1993) J Neurosci 13(1): 38-44
    › Primary publication · 8380851 (PubMed) · PMC6576299 (PubMed Central)