Danny G. Winder, Ph.D.

Professor

danny.winder@vanderbilt.edu

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Faculty Appointments
Professor of Molecular Physiology and Biophysics Professor PharmacologyProfessor of Psychiatry and Behavioral Sciences
Education
Ph.D., Neuroscience, Emory University, Atlanta, GeorgiaB.S., Biology/Chemistry, North Georgia College & State University, Dahlonega, Georgia
Office Address
702 Light Hall
Nashville, TN 37232-0615
Research Description
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.
Research Keywords
Synaptic mechanisms in addiction and anxiety
Publications
Wills TA, Klug JR, Silberman Y, Baucum AJ, Weitlauf C, Colbran RJ, Delpire E, Winder DG. GluN2B subunit deletion reveals key role in acute and chronic ethanol sensitivity of glutamate synapses in bed nucleus of the stria terminalis. Proc. Natl. Acad. Sci. U.S.A [print-electronic]. 2012 Jan 1/31/2012; 109(5): E278-87. PMID: 22219357, PMCID: PMC3277158, PII: 1113820109, DOI: 10.1073/pnas.1113820109, ISSN: 1091-6490.

Conrad KL, Winder DG. Altered anxiety-like behavior and long-term potentiation in the bed nucleus of the stria terminalis in adult mice exposed to chronic social isolation, unpredictable stress, and ethanol beginning in adolescence. Alcohol [print-electronic]. 2011 Sep; 45(6): 585-93. PMID: 21194878, PMCID: PMC3085602, PII: S0741-8329(10)00197-7, DOI: 10.1016/j.alcohol.2010.11.002, ISSN: 1873-6823.

Lindsley CW, Bates BS, Menon UN, Jadhav SB, Kane AS, Jones CK, Rodriguez AL, Conn PJ, Olsen CM, Winder DG, Emmitte KA. (3-Cyano-5-fluorophenyl)biaryl negative allosteric modulators of mGlu(5): Discovery of a new tool compound with activity in the OSS mouse model of addiction. ACS Chem Neurosci. 2011 Aug 8/17/2011; 2(8): 471-82. PMID: 21927650, PMCID: PMC3172161, DOI: 10.1021/cn100099n, ISSN: 1948-7193.

Conrad KL, Louderback KM, Gessner CP, Winder DG. Stress-induced alterations in anxiety-like behavior and adaptations in plasticity in the bed nucleus of the stria terminalis. Physiol. Behav [print-electronic]. 2011 Aug 8/3/2011; 104(2): 248-56. PMID: 21396387, PMCID: PMC3118978, PII: S0031-9384(11)00107-7, DOI: 10.1016/j.physbeh.2011.03.001, ISSN: 1873-507X.

Gustin RM, Shonesy BC, Robinson SL, Rentz TJ, Baucum AJ, Jalan-Sakrikar N, Winder DG, Stanwood GD, Colbran RJ. Loss of Thr286 phosphorylation disrupts synaptic CaMKIIa targeting, NMDAR activity and behavior in pre-adolescent mice. Mol. Cell. Neurosci [print-electronic]. 2011 Aug; 47(4): 286-92. PMID: 21627991, PMCID: PMC3149813, PII: S1044-7431(11)00112-6, DOI: 10.1016/j.mcn.2011.05.006, ISSN: 1095-9327.

Gosnell HB, Silberman Y, Grueter BA, Duvoisin RM, Raber J, Winder DG. MGluR8 modulates excitatory transmission in the bed nucleus of the stria terminalis in a stress-dependent manner. Neuropsychopharmacology [print-electronic]. 2011 Jul; 36(8): 1599-607. PMID: 21451497, PMCID: PMC3138653, PII: npp201140, DOI: 10.1038/npp.2011.40, ISSN: 1740-634X.

Nobis WP, Kash TL, Silberman Y, Winder DG. ß-Adrenergic receptors enhance excitatory transmission in the bed nucleus of the stria terminalis through a corticotrophin-releasing factor receptor-dependent and cocaine-regulated mechanism. Biol. Psychiatry [print-electronic]. 2011 Jun 6/1/2011; 69(11): 1083-90. PMID: 21334600, PMCID: PMC3090515, PII: S0006-3223(10)01362-4, DOI: 10.1016/j.biopsych.2010.12.030, ISSN: 1873-2402.

Patel S, Winder DG. An odyssey of fear: Homer stresses new mechanisms. Biol. Psychiatry. 2010 Dec 12/1/2010; 68(11): 980-1. PMID: 21075227, PMCID: PMC3035943, PII: S0006-3223(10)01061-9, DOI: 10.1016/j.biopsych.2010.10.005, ISSN: 1873-2402.

McElligott ZA, Klug JR, Nobis WP, Patel S, Grueter BA, Kash TL, Winder DG. Distinct forms of Gq-receptor-dependent plasticity of excitatory transmission in the BNST are differentially affected by stress. Proc. Natl. Acad. Sci. U.S.A [print-electronic]. 2010 Feb 2/2/2010; 107(5): 2271-6. PMID: 20133871, PMCID: PMC2836642, PII: 0905568107, DOI: 10.1073/pnas.0905568107, ISSN: 1091-6490.

Olsen CM, Childs DS, Stanwood GD, Winder DG. Operant sensation seeking requires metabotropic glutamate receptor 5 (mGluR5). PLoS ONE. 2010; 5(11): e15085. PMID: 21152045, PMCID: PMC2994905, DOI: 10.1371/journal.pone.0015085, ISSN: 1932-6203.

Patel S, Kingsley PJ, Mackie K, Marnett LJ, Winder DG. Repeated homotypic stress elevates 2-arachidonoylglycerol levels and enhances short-term endocannabinoid signaling at inhibitory synapses in basolateral amygdala. Neuropsychopharmacology [print-electronic]. 2009 Dec; 34(13): 2699-709. PMID: 19675536, PMCID: PMC2881681, PII: npp2009101, DOI: 10.1038/npp.2009.101, ISSN: 1740-634X.

McElligott ZA, Winder DG. Modulation of glutamatergic synaptic transmission in the bed nucleus of the stria terminalis. Prog. Neuropsychopharmacol. Biol. Psychiatry [print-electronic]. 2009 Nov 11/13/2009; 33(8): 1329-35. PMID: 19524008, PMCID: PMC2783684, PII: S0278-5846(09)00190-0, DOI: 10.1016/j.pnpbp.2009.05.022, ISSN: 1878-4216.

Kash TL, Baucum AJ, Conrad KL, Colbran RJ, Winder DG. Alcohol exposure alters NMDAR function in the bed nucleus of the stria terminalis. Neuropsychopharmacology [print-electronic]. 2009 Oct; 34(11): 2420-9. PMID: 19553918, PMCID: PMC2864644, PII: npp200969, DOI: 10.1038/npp.2009.69, ISSN: 1740-634X.

Shields AD, Wang Q, Winder DG. Alpha2A-adrenergic receptors heterosynaptically regulate glutamatergic transmission in the bed nucleus of the stria terminalis. Neuroscience [print-electronic]. 2009 Sep 9/29/2009; 163(1): 339-51. PMID: 19527774, PMCID: PMC2744292, PII: S0306-4522(09)01024-0, DOI: 10.1016/j.neuroscience.2009.06.022, ISSN: 1873-7544.

Olsen CM, Winder DG. Operant sensation seeking engages similar neural substrates to operant drug seeking in C57 mice. Neuropsychopharmacology [print-electronic]. 2009 Jun; 34(7): 1685-94. PMID: 19145223, PMCID: PMC2720253, PII: npp2008226, DOI: 10.1038/npp.2008.226, ISSN: 1740-634X.

Matthies HJ, Han Q, Shields A, Wright J, Moore JL, Winder DG, Galli A, Blakely RD. Subcellular localization of the antidepressant-sensitive norepinephrine transporter. BMC Neurosci. 2009; 10: 65. PMID: 19545450, PMCID: PMC2716352, PII: 1471-2202-10-65, DOI: 10.1186/1471-2202-10-65, ISSN: 1471-2202.

Kash TL, Nobis WP, Matthews RT, Winder DG. Dopamine enhances fast excitatory synaptic transmission in the extended amygdala by a CRF-R1-dependent process. J. Neurosci. 2008 Dec 12/17/2008; 28(51): 13856-65. PMID: 19091975, PMCID: PMC2630395, PII: 28/51/13856, DOI: 10.1523/JNEUROSCI.4715-08.2008, ISSN: 1529-2401.

McElligott ZA, Winder DG. Alpha1-adrenergic receptor-induced heterosynaptic long-term depression in the bed nucleus of the stria terminalis is disrupted in mouse models of affective disorders. Neuropsychopharmacology [print-electronic]. 2008 Sep; 33(10): 2313-23. PMID: 18046308, PMCID: PMC3046390, PII: 1301635, DOI: 10.1038/sj.npp.1301635, ISSN: 1740-634X.

Kash TL, Matthews RT, Winder DG. Alcohol inhibits NR2B-containing NMDA receptors in the ventral bed nucleus of the stria terminalis. Neuropsychopharmacology [print-electronic]. 2008 May; 33(6): 1379-90. PMID: 17625498, PMCID: PMC2864636, PII: 1301504, DOI: 10.1038/sj.npp.1301504, ISSN: 0893-133X.

Healey JC, Winder DG, Kash TL. Chronic ethanol exposure leads to divergent control of dopaminergic synapses in distinct target regions. Alcohol [print-electronic]. 2008 May; 42(3): 179-90. PMID: 18358675, PMCID: PMC2855295, PII: S0741-8329(08)00025-6, DOI: 10.1016/j.alcohol.2008.01.003, ISSN: 0741-8329.

Olsen CM, Huang Y, Goodwin S, Ciobanu DC, Lu L, Sutter TR, Winder DG. Microarray analysis reveals distinctive signaling between the bed nucleus of the stria terminalis, nucleus accumbens, and dorsal striatum. Physiol. Genomics [print-electronic]. 2008 Feb 2/19/2008; 32(3): 283-98. PMID: 17911379, PII: 00224.2006, DOI: 10.1152/physiolgenomics.00224.2006, ISSN: 1531-2267.

Grueter BA, McElligott ZA, Winder DG. Group I mGluRs and long-term depression: potential roles in addiction?. Mol. Neurobiol [print-electronic]. 2007 Dec; 36(3): 232-44. PMID: 17955198, DOI: 10.1007/s12035-007-0037-7, ISSN: 0893-7648.

Robison AJ, Winder DG, Colbran RJ, Bartlett RK. Oxidation of calmodulin alters activation and regulation of CaMKII. Biochem. Biophys. Res. Commun [print-electronic]. 2007 Apr 4/27/2007; 356(1): 97-101. PMID: 17343827, PMCID: PMC1899527, PII: S0006-291X(07)00381-6, DOI: 10.1016/j.bbrc.2007.02.087, ISSN: 0006-291X.

Kash TL, Winder DG. Neuropeptide Y and corticotropin-releasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis. Neuropharmacology [print-electronic]. 2006 Oct; 51(5): 1013-22. PMID: 16904135, PII: S0028-3908(06)00196-1, DOI: 10.1016/j.neuropharm.2006.06.011, ISSN: 0028-3908.

Schramm-Sapyta NL, Olsen CM, Winder DG. Cocaine self-administration reduces excitatory responses in the mouse nucleus accumbens shell. Neuropsychopharmacology [print-electronic]. 2006 Jul; 31(7): 1444-51. PMID: 16205778, PII: 1300918, DOI: 10.1038/sj.npp.1300918, ISSN: 0893-133X.

Olsen CM, Winder DG. A method for single-session cocaine self-administration in the mouse. Psychopharmacology (Berl.) [print-electronic]. 2006 Jul; 187(1): 13-21. PMID: 16767412, DOI: 10.1007/s00213-006-0388-1, ISSN: 0033-3158.

Grueter BA, Gosnell HB, Olsen CM, Schramm-Sapyta NL, Nekrasova T, Landreth GE, Winder DG. 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. J. Neurosci. 2006 Mar 3/22/2006; 26(12): 3210-9. PMID: 16554472, PII: 26/12/3210, DOI: 10.1523/JNEUROSCI.0170-06.2006, ISSN: 1529-2401.

Vanhoose AM, Clements JM, Winder DG. Novel blockade of protein kinase A-mediated phosphorylation of AMPA receptors. J. Neurosci. 2006 Jan 1/25/2006; 26(4): 1138-45. PMID: 16436600, PII: 26/4/1138, DOI: 10.1523/JNEUROSCI.3572-05.2006, ISSN: 1529-2401.

Weitlauf C, Honse Y, Auberson YP, Mishina M, Lovinger DM, Winder DG. Activation of NR2A-containing NMDA receptors is not obligatory for NMDA receptor-dependent long-term potentiation. J. Neurosci. 2005 Sep 9/14/2005; 25(37): 8386-90. PMID: 16162920, PII: 25/37/8386, DOI: 10.1523/JNEUROSCI.2388-05.2005, ISSN: 1529-2401.

Grueter BA, Winder DG. Group II and III metabotropic glutamate receptors suppress excitatory synaptic transmission in the dorsolateral bed nucleus of the stria terminalis. Neuropsychopharmacology. 2005 Jul; 30(7): 1302-11. PMID: 15812571, PII: 1300672, DOI: 10.1038/sj.npp.1300672, ISSN: 0893-133X.

Egli RE, Kash TL, Choo K, Savchenko V, Matthews RT, Blakely RD, Winder DG. Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis. Neuropsychopharmacology. 2005 Apr; 30(4): 657-68. PMID: 15602500, PII: 1300639, DOI: 10.1038/sj.npp.1300639, ISSN: 0893-133X.

Norman ED, Egli RE, Colbran RJ, Winder DG. A potassium channel blocker induces a long-lasting enhancement of corticostriatal responses. Neuropharmacology. 2005 Feb; 48(2): 311-21. PMID: 15695170, PII: S0028-3908(04)00348-X, DOI: 10.1016/j.neuropharm.2004.09.018, ISSN: 0028-3908.

Vanhoose AM, Ritchie MD, Winder DG. Regulation of cAMP levels in area CA1 of hippocampus by Gi/o-coupled receptors is stimulus dependent in mice. Neurosci. Lett. 2004 Nov 11/3/2004; 370(1): 80-3. PMID: 15489022, PII: S0304-3940(04)00981-4, DOI: 10.1016/j.neulet.2004.07.093, ISSN: 0304-3940.

Matthews RT, Coker O, Winder DG. A novel mouse brain slice preparation of the hippocampo-accumbens pathway. J. Neurosci. Methods. 2004 Aug 8/15/2004; 137(1): 49-60. PMID: 15196826, PII: S0165027004000469, DOI: 10.1016/j.jneumeth.2004.02.001, ISSN: 0165-0270.

Weitlauf C, Egli RE, Grueter BA, Winder DG. High-frequency stimulation induces ethanol-sensitive long-term potentiation at glutamatergic synapses in the dorsolateral bed nucleus of the stria terminalis. J. Neurosci. 2004 Jun 6/23/2004; 24(25): 5741-7. PMID: 15215296, PII: 24/25/5741, DOI: 10.1523/JNEUROSCI.1181-04.2004, ISSN: 1529-2401.

Schramm-Sapyta NL, Pratt AR, Winder DG. Effects of periadolescent versus adult cocaine exposure on cocaine conditioned place preference and motor sensitization in mice. Psychopharmacology (Berl.) [print-electronic]. 2004 Apr; 173(1-2): 41-8. PMID: 14712337, DOI: 10.1007/s00213-003-1696-3, ISSN: 0033-3158.

Morozov A, Muzzio IA, Bourtchouladze R, Van-Strien N, Lapidus K, Yin D, Winder DG, Adams JP, Sweatt JD, Kandel ER. Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron. 2003 Jul 7/17/2003; 39(2): 309-25. PMID: 12873387, PII: S0896627303004045, ISSN: 0896-6273.

Vanhoose AM, Winder DG. NMDA and beta1-adrenergic receptors differentially signal phosphorylation of glutamate receptor type 1 in area CA1 of hippocampus. J. Neurosci. 2003 Jul 7/2/2003; 23(13): 5827-34. PMID: 12843287, PII: 23/13/5827, ISSN: 1529-2401.

Egli RE, Winder DG. Dorsal and ventral distribution of excitable and synaptic properties of neurons of the bed nucleus of the stria terminalis. J. Neurophysiol [print-electronic]. 2003 Jul; 90(1): 405-14. PMID: 12649311, PII: 00228.2003, DOI: 10.1152/jn.00228.2003, ISSN: 0022-3077.

Winder DG, Egli RE, Schramm NL, Matthews RT. Synaptic plasticity in drug reward circuitry. Curr. Mol. Med. 2002 Nov; 2(7): 667-76. PMID: 12420805, ISSN: 1566-5240.

Schramm NL, Egli RE, Winder DG. LTP in the mouse nucleus accumbens is developmentally regulated. Synapse. 2002 Sep 9/15/2002; 45(4): 213-9. PMID: 12125042, DOI: 10.1002/syn.10104, ISSN: 0887-4476.

Vanhoose AM, Emery M, Jimenez L, Winder DG. ERK activation by G-protein-coupled receptors in mouse brain is receptor identity-specific. J. Biol. Chem [print-electronic]. 2002 Mar 3/15/2002; 277(11): 9049-53. PMID: 11782465, PII: M108309200, DOI: 10.1074/jbc.M108309200, ISSN: 0021-9258.

Winder, D.G. and Kandel, E.R. Genetic strategies for the study of hippocampal-based memory storage. In: J.J. Bolhuis (Ed.) Brain Mechanisms of Perception, Learning and Memory: Essays for Gabriel Horn. Oxford University Press. Oxford. 2002.

Winder DG, Schramm NL. Plasticity and behavior: new genetic techniques to address multiple forms and functions. Physiol. Behav. 2001 Aug; 73(5): 763-80. PMID: 11566210, PII: S0031-9384(01)00514-5, ISSN: 0031-9384.

Winder DG, Sweatt JD. Roles of serine/threonine phosphatases in hippocampal synaptic plasticity. Nat. Rev. Neurosci. 2001 Jul; 2(7): 461-74. PMID: 11433371, PII: 35081514, DOI: 10.1038/35081514, ISSN: 1471-003X.

Malleret, G., Haditsch, U., Genoux, D., Jones, M., Bliss, T.V.P., Vanhoose, A.M., Weitlauf, C., Kandel, E.R., Winder, D.G. and Mansuy, I.M. Inducible and reversible enhancement of learning, memory storage and long-term potentiation by genetic inhibition of calcineurin. Cell . 2001; 104: 675-86.

Winder DG, Martin KC, Muzzio IA, Rohrer D, Chruscinski A, Kobilka B, Kandel ER. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron. 1999 Nov; 24(3): 715-26. PMID: 10595521, PII: S0896-6273(00)81124-1, ISSN: 0896-6273.

Barad M, Bourtchouladze R, Winder DG, Golan H, Kandel E. Rolipram, a type IV-specific phosphodiesterase inhibitor, facilitates the establishment of long-lasting long-term potentiation and improves memory. Proc. Natl. Acad. Sci. U.S.A. 1998 Dec 12/8/1998; 95(25): 15020-5. PMID: 9844008, PMCID: PMC24568, ISSN: 0027-8424.

Mansuy IM, Winder DG, Moallem TM, Osman M, Mayford M, Hawkins RD, Kandel ER. Inducible and reversible gene expression with the rtTA system for the study of memory. Neuron. 1998 Aug; 21(2): 257-65. PMID: 9728905, PII: S0896-6273(00)80533-4, ISSN: 0896-6273.

Winder DG, Mansuy IM, Osman M, Moallem TM, Kandel ER. Genetic and pharmacological evidence for a novel, intermediate phase of long-term potentiation suppressed by calcineurin. Cell. 1998 Jan 1/9/1998; 92(1): 25-37. PMID: 9489697, PII: S0092-8674(00)80896-X, ISSN: 0092-8674.

Conn, P.J., Bradley, S.R., Macek, T.A., Winder, D.G. and Gereau, R.W. F. Moroni, F. Nicoletti, and D.E. Pellegrini-Giampietro (Eds.). Physiological roles of multiple metabotropic glutamate receptor subtypes in the hippocampus. Metabotropic Glutamate receptors and Brain Function. Portland Press Ltd. London. 1997; 87.

Macek TA, Winder DG, Gereau RW, Ladd CO, Conn PJ. Differential involvement of group II and group III mGluRs as autoreceptors at lateral and medial perforant path synapses. J. Neurophysiol. 1996 Dec; 76(6): 3798-806. PMID: 8985877, ISSN: 0022-3077.

Winder DG, Conn PJ. Roles of metabotropic glutamate receptors in glial function and glial-neuronal communication. J. Neurosci. Res. 1996 Oct 10/15/1996; 46(2): 131-7. PMID: 8915890, PII: 10.1002/(SICI)1097-4547(19961015)46:2<131::AID-JNR1>3.0.CO;2-I, DOI: 10.1002/(SICI)1097-4547(19961015)46:2<131::AID-JNR1>3.0.CO;2-I, ISSN: 0360-4012.

Winder DG, Ritch PS, Gereau RW, Conn PJ. Novel glial-neuronal signalling by coactivation of metabotropic glutamate and beta-adrenergic receptors in rat hippocampus. J. Physiol. (Lond.). 1996 Aug 8/1/1996; 494 ( Pt 3): 743-55. PMID: 8865071, PMCID: PMC1160674, ISSN: 0022-3751.

Gereau RW, Winder DG, Conn PJ. Pharmacological differentiation of the effects of co-activation of beta-adrenergic and metabotropic glutamate receptors in rat hippocampus. Neurosci. Lett. 1995 Feb 2/17/1995; 186(2-3): 119-22. PMID: 7777178, ISSN: 0304-3940.

Winder DG, Conn PJ. Metabotropic glutamate receptor (mGluR)-mediated potentiation of cyclic AMP responses does not require phosphoinositide hydrolysis: mediation by a group II-like mGluR. J. Neurochem. 1995 Feb; 64(2): 592-9. PMID: 7830052, ISSN: 0022-3042.

Conn, P.J., Chung, D., Winder, D.G., Gereau IV, R. and Boss, V. T.W. Stone (ed.). Biochemical transduction systems operated by excitatory amino acids. CNS Neurotransmitters and Neuromodulators: Glutamate, CRC Press, Boca Raton, FL. 1995; 181-99.

Conn, P.J., Gereau, R.W. IV and Winder, D.G. P.J. Conn and J. Patel (eds.). Roles of metabotropic glutamate receptors in regulating neural circuits and animal behavior. The Metabotropic Glutamate Receptors, Humana Press, Totowa, NJ. 1995; 195-229.

Chung DS, Winder DG, Conn PJ. 4-Bromohomoibotenic acid selectively activates a 1-aminocyclopentane-1S,3R-dicarboxylic acid-insensitive metabotropic glutamate receptor coupled to phosphoinositide hydrolysis in rat cortical slices. J. Neurochem. 1994 Jul; 63(1): 133-9. PMID: 8207423, ISSN: 0022-3042.

Winder DG, Smith T, Conn PJ. Pharmacological differentiation of metabotropic glutamate receptors coupled to potentiation of cyclic adenosine monophosphate responses and phosphoinositide hydrolysis. J. Pharmacol. Exp. Ther. 1993 Aug; 266(2): 518-25. PMID: 8394908, ISSN: 0022-3565.

Winder DG, Conn PJ. Activation of metabotropic glutamate receptors increases cAMP accumulation in hippocampus by potentiating responses to endogenous adenosine. J. Neurosci. 1993 Jan; 13(1): 38-44. PMID: 8380851, ISSN: 0270-6474.

Chen SJ, Desai MA, Klann E, Winder DG, Sweatt JD, Conn PJ. Amygdala kindling alters protein kinase C activity in dentate gyrus. J. Neurochem. 1992 Nov; 59(5): 1761-9. PMID: 1402921, ISSN: 0022-3042.

Winder DG, Conn PJ. Activation of metabotropic glutamate receptors in the hippocampus increases cyclic AMP accumulation. J. Neurochem. 1992 Jul; 59(1): 375-8. PMID: 1351930, ISSN: 0022-3042.