Priyattam J. Shiromani

Title
InstitutionMedical University of South Carolina
DepartmentPsychiatry and Behavioral Sciences
AddressP.O. Box MSC 861
404
114 Doughty St.
Phone843-789-6778
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    Sleep Molecular Laboratory

    The lab’s research strategy is to identify the neural circuitry responsible for the alternation between wake, sleep and REM sleep. Sleep and circadian rhythms of body temperature and activity are measured in rodents (rats and mice). Molecular (Dr. Meng Liu), pharmacological (Dr. Carlos Blanco-Centurion), anatomical (Dr. RodaRani Konadhode) and electrophysiology (Dr. Dheeraj Pelluru) methods are used to trace the network, record activity of neurons, identify gene expression in specific neuronal populations and whether destruction of specific neurons or loss of specific genes affects sleep. To destroy orexin receptor bearing neurons we created a novel compound linking saporin to the ligand orexin. This compound provides a rapid, cost effective method to test specific hypotheses regarding the role of specific brain regions in sleep-wake regulation. Once it is found that loss of a gene or neurons results in a sleep abnormality then novel methods are used to repair the network and determine whether sleep returns to normal. Recently, we demonstrated the first ever use of gene transfer to treat a sleep disorder. Our most recent study identified an hitherto unknown group of neurons in the subthalamus that control cataplexy, an important symptom of narcolepsy (Liu et al., J Neuroscience, 2011).

    The primary focus of the research is on the sleep disorder, narcolepsy. Dr. Shiromani’s research career was started in 1986 by a small grant from the American Narcolepsy Association. Since then the laboratory has been continuously funded by the NIH, the VA and the DoD.

    This lab provides training in long-term (months) recording of sleep and circadian rhythms in rodents. Dr. Shiromani has trained many students who have now established their own labs. Training is also provided in molecular biology, immunohistochemistry, microdialysis, HPLC and single cell recording of neurons in freely-behaving rodents.

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    Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Faculty can login to make corrections and additions.
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    1. Shiromani PJ, Blanco-Centurion C, Vidal-Ortiz A. Mapping Network Activity in Sleep. Front Neurosci. 2021; 15:646468. PMID: 33828453.
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    2. Blanco-Centurion C, Luo S, Vidal-Ortiz A, Swank C, Shiromani PJ. "Activity of a subset of vesicular GABA-transporter neurons in the ventral zona incerta anticipate sleep onset". Sleep. 2020 Dec 03. PMID: 33270105.
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    3. Blanco-Centurion C, Luo S, Spergel DJ, Vidal-Ortiz A, Oprisan SA, Van den Pol AN, Liu M, Shiromani PJ. Dynamic Network Activation of Hypothalamic MCH Neurons in REM Sleep and Exploratory Behavior. J Neurosci. 2019 06 19; 39(25):4986-4998. PMID: 31036764.
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    4. Sun Y, Blanco-Centurion C, Zou B, Bendell E, Shiromani PJ, Liu M. Amygdala GABA Neurons Project To vlPAG And mPFC. IBRO Rep. 2019 Jun; 6:132-136. PMID: 31193158.
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    5. Blanco-Centurion C, Bendell E, Zou B, Sun Y, Shiromani PJ, Liu M. VGAT and VGLUT2 expression in MCH and orexin neurons in double transgenic reporter mice. IBRO Rep. 2018 Jun; 4:44-49. PMID: 30155524.
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    6. Liu M, Blanco-Centurion C, Shiromani PJ. Rewiring brain circuits to block cataplexy in murine models of narcolepsy. Curr Opin Neurobiol. 2017 06; 44:110-115. PMID: 28445807.
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    7. Shiromani PJ, Peever JH. New Neuroscience Tools That Are Identifying the Sleep-Wake Circuit. Sleep. 2017 04 01; 40(4). PMID: 28329204.
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    8. Blanco-Centurion C, Liu M, Konadhode RP, Zhang X, Pelluru D, van den Pol AN, Shiromani PJ. Optogenetic activation of melanin-concentrating hormone neurons increases non-rapid eye movement and rapid eye movement sleep during the night in rats. Eur J Neurosci. 2016 11; 44(10):2846-2857. PMID: 27657541.
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    9. Konadhode RR, Pelluru D, Shiromani PJ. Unihemispheric Sleep: An Enigma for Current Models of Sleep-Wake Regulation. Sleep. 2016 Mar 01; 39(3):491-4. PMID: 26856898.
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    10. Liu M, Blanco-Centurion C, Konadhode RR, Luan L, Shiromani PJ. Orexin gene transfer into the amygdala suppresses both spontaneous and emotion-induced cataplexy in orexin-knockout mice. Eur J Neurosci. 2016 Mar; 43(5):681-8. PMID: 26741960.
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    11. Pelluru D, Konadhode RR, Bhat NR, Shiromani PJ. Optogenetic stimulation of astrocytes in the posterior hypothalamus increases sleep at night in C57BL/6J mice. Eur J Neurosci. 2016 05; 43(10):1298-306. PMID: 26369866.
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    12. Konadhode RR, Pelluru D, Shiromani PJ. Neurons containing orexin or melanin concentrating hormone reciprocally regulate wake and sleep. Front Syst Neurosci. 2014; 8:244. PMID: 25620917.
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    13. Pava MJ, den Hartog CR, Blanco-Centurion C, Shiromani PJ, Woodward JJ. Endocannabinoid modulation of cortical up-states and NREM sleep. PLoS One. 2014; 9(2):e88672. PMID: 24520411.
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    14. Pelluru D, Konadhode R, Shiromani PJ. MCH neurons are the primary sleep-promoting group. Sleep. 2013 Dec 01; 36(12):1779-81. PMID: 24293750.
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    15. Konadhode RR, Pelluru D, Blanco-Centurion C, Zayachkivsky A, Liu M, Uhde T, Glen WB, van den Pol AN, Mulholland PJ, Shiromani PJ. Optogenetic stimulation of MCH neurons increases sleep. J Neurosci. 2013 Jun 19; 33(25):10257-63. PMID: 23785141.
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    16. Blanco-Centurion C, Liu M, Konadhode R, Pelluru D, Shiromani PJ. Effects of orexin gene transfer in the dorsolateral pons in orexin knockout mice. Sleep. 2013 Jan 01; 36(1):31-40. PMID: 23288969.
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    17. Liu M, Blanco-Centurion C, Konadhode R, Begum S, Pelluru D, Gerashchenko D, Sakurai T, Yanagisawa M, van den Pol AN, Shiromani PJ. Orexin gene transfer into zona incerta neurons suppresses muscle paralysis in narcoleptic mice. J Neurosci. 2011 Apr 20; 31(16):6028-40. PMID: 21508228.
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    18. Kaur S, Thankachan S, Begum S, Liu M, Blanco-Centurion C, Shiromani PJ. Hypocretin-2 saporin lesions of the ventrolateral periaquaductal gray (vlPAG) increase REM sleep in hypocretin knockout mice. PLoS One. 2009 Jul 22; 4(7):e6346. PMID: 19623260.
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    19. Thankachan S, Kaur S, Shiromani PJ. Activity of pontine neurons during sleep and cataplexy in hypocretin knock-out mice. J Neurosci. 2009 Feb 04; 29(5):1580-5. PMID: 19193905.
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    20. Liu M, Thankachan S, Kaur S, Begum S, Blanco-Centurion C, Sakurai T, Yanagisawa M, Neve R, Shiromani PJ. Orexin (hypocretin) gene transfer diminishes narcoleptic sleep behavior in mice. Eur J Neurosci. 2008 Oct; 28(7):1382-93. PMID: 18973565.
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    21. Greco MA, Fuller PM, Jhou TC, Martin-Schild S, Zadina JE, Hu Z, Shiromani P, Lu J. Opioidergic projections to sleep-active neurons in the ventrolateral preoptic nucleus. Brain Res. 2008 Dec 15; 1245:96-107. PMID: 18840417.
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    22. Murillo-Rodriguez E, Liu M, Blanco-Centurion C, Shiromani PJ. Effects of hypocretin (orexin) neuronal loss on sleep and extracellular adenosine levels in the rat basal forebrain. Eur J Neurosci. 2008 Sep; 28(6):1191-8. PMID: 18783368.
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    23. Gerashchenko D, Wisor JP, Burns D, Reh RK, Shiromani PJ, Sakurai T, de la Iglesia HO, Kilduff TS. Identification of a population of sleep-active cerebral cortex neurons. Proc Natl Acad Sci U S A. 2008 Jul 22; 105(29):10227-32. PMID: 18645184.
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    24. Kaur S, Thankachan S, Begum S, Blanco-Centurion C, Sakurai T, Yanagisawa M, Shiromani PJ. Entrainment of temperature and activity rhythms to restricted feeding in orexin knock out mice. Brain Res. 2008 Apr 18; 1205:47-54. PMID: 18343358.
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    25. Blanco-Centurion C, Gerashchenko D, Shiromani PJ. Effects of saporin-induced lesions of three arousal populations on daily levels of sleep and wake. J Neurosci. 2007 Dec 19; 27(51):14041-8. PMID: 18094243.
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    26. Zhang S, Lin L, Kaur S, Thankachan S, Blanco-Centurion C, Yanagisawa M, Mignot E, Shiromani PJ. The development of hypocretin (orexin) deficiency in hypocretin/ataxin-3 transgenic rats. Neuroscience. 2007 Aug 10; 148(1):34-43. PMID: 17618058.
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    27. Blanco-Centurion CA, Shiromani A, Winston E, Shiromani PJ. Effects of hypocretin-1 in 192-IgG-saporin-lesioned rats. Eur J Neurosci. 2006 Oct; 24(7):2084-8. PMID: 17067305.
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    28. Blanco-Centurion C, Xu M, Murillo-Rodriguez E, Gerashchenko D, Shiromani AM, Salin-Pascual RJ, Hof PR, Shiromani PJ. Adenosine and sleep homeostasis in the Basal forebrain. J Neurosci. 2006 Aug 02; 26(31):8092-100. PMID: 16885223.
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    29. Salín-Pascual RJ, Valencia-Flores M, Campos RM, Castaño A, Shiromani PJ. Caffeine challenge in insomniac patients after total sleep deprivation. Sleep Med. 2006 Mar; 7(2):141-5. PMID: 16459138.
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    30. Blanco-Centurion CA, Shiromani PJ. Beneficial effects of regular exercise on sleep in old F344 rats. Neurobiol Aging. 2006 Dec; 27(12):1859-69. PMID: 16309796.
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    31. Gerashchenko D, Blanco-Centurion CA, Miller JD, Shiromani PJ. Insomnia following hypocretin2-saporin lesions of the substantia nigra. Neuroscience. 2006; 137(1):29-36. PMID: 16289583.
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    32. Arias-Carrión O, Murillo-Rodriguez E, Xu M, Blanco-Centurion C, Drucker-Colín R, Shiromani PJ. Transplantation of hypocretin neurons into the pontine reticular formation: preliminary results. Sleep. 2004 Dec 15; 27(8):1465-70. PMID: 15683135.
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    33. Gerashchenko D, Chou TC, Blanco-Centurion CA, Saper CB, Shiromani PJ. Effects of lesions of the histaminergic tuberomammillary nucleus on spontaneous sleep in rats. Sleep. 2004 Nov 01; 27(7):1275-81. PMID: 15586780.
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    34. Gerashchenko D, Shiromani PJ. Effects of inflammation produced by chronic lipopolysaccharide administration on the survival of hypocretin neurons and sleep. Brain Res. 2004 Sep 03; 1019(1-2):162-9. PMID: 15306250.
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    35. Desarnaud F, Murillo-Rodriguez E, Lin L, Xu M, Gerashchenko D, Shiromani SN, Nishino S, Mignot E, Shiromani PJ. The diurnal rhythm of hypocretin in young and old F344 rats. Sleep. 2004 Aug 01; 27(5):851-6. PMID: 15453542.
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    36. Blanco-Centurion C, Gerashchenko D, Salin-Pascual RJ, Shiromani PJ. Effects of hypocretin2-saporin and antidopamine-beta-hydroxylase-saporin neurotoxic lesions of the dorsolateral pons on sleep and muscle tone. Eur J Neurosci. 2004 May; 19(10):2741-52. PMID: 15147308.
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    37. Shiromani PJ, Xu M, Winston EM, Shiromani SN, Gerashchenko D, Weaver DR. Sleep rhythmicity and homeostasis in mice with targeted disruption of mPeriod genes. . 2004 Jul; 287(1):R47-57. PMID: 15031135.
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    38. Gerashchenko D, Shiromani PJ. Different neuronal phenotypes in the lateral hypothalamus and their role in sleep and wakefulness. Mol Neurobiol. 2004 Feb; 29(1):41-59. PMID: 15034222.
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    39. Murillo-Rodriguez E, Blanco-Centurion C, Gerashchenko D, Salin-Pascual RJ, Shiromani PJ. The diurnal rhythm of adenosine levels in the basal forebrain of young and old rats. Neuroscience. 2004; 123(2):361-70. PMID: 14698744.
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    40. Murillo-Rodriguez E, Blanco-Centurion C, Sanchez C, Piomelli D, Shiromani PJ. Anandamide enhances extracellular levels of adenosine and induces sleep: an in vivo microdialysis study. Sleep. 2003 Dec 15; 26(8):943-7. PMID: 14746372.
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    41. Gerashchenko D, Murillo-Rodriguez E, Lin L, Xu M, Hallett L, Nishino S, Mignot E, Shiromani PJ. Relationship between CSF hypocretin levels and hypocretin neuronal loss. Exp Neurol. 2003 Dec; 184(2):1010-6. PMID: 14769395.
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    42. Gerashchenko D, Blanco-Centurion C, Greco MA, Shiromani PJ. Effects of lateral hypothalamic lesion with the neurotoxin hypocretin-2-saporin on sleep in Long-Evans rats. Neuroscience. 2003; 116(1):223-35. PMID: 12535955.
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    43. Goulet M, Shiromani PJ, Ware CM, Strong RA, Boismenu R, Rusche JR. A secretin i.v. infusion activates gene expression in the central amygdala of rats. Neuroscience. 2003; 118(4):881-8. PMID: 12732234.
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    44. Salin-Pascual RJ, Upadhyay U, Shiromani PJ. Effects of hypocaloric diet on sleep in young and old rats. Neurobiol Aging. 2002 Sep-Oct; 23(5):771-6. PMID: 12392780.
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    45. Lu J, Bjorkum AA, Xu M, Gaus SE, Shiromani PJ, Saper CB. Selective activation of the extended ventrolateral preoptic nucleus during rapid eye movement sleep. J Neurosci. 2002 Jun 01; 22(11):4568-76. PMID: 12040064.
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    46. Salin-Pascual R, Gerashchenko D, Greco M, Blanco-Centurion C, Shiromani PJ. Hypothalamic regulation of sleep. Neuropsychopharmacology. 2001 Nov; 25(5 Suppl):S21-7. PMID: 11682269.
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    47. Gerashchenko D, Kohls MD, Greco M, Waleh NS, Salin-Pascual R, Kilduff TS, Lappi DA, Shiromani PJ. Hypocretin-2-saporin lesions of the lateral hypothalamus produce narcoleptic-like sleep behavior in the rat. J Neurosci. 2001 Sep 15; 21(18):7273-83. PMID: 11549737.
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    48. Gerashchenko D, Salin-Pascual R, Shiromani PJ. Effects of hypocretin-saporin injections into the medial septum on sleep and hippocampal theta. Brain Res. 2001 Sep 14; 913(1):106-15. PMID: 11532254.
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    49. Lu J, Zhang YH, Chou TC, Gaus SE, Elmquist JK, Shiromani P, Saper CB. Contrasting effects of ibotenate lesions of the paraventricular nucleus and subparaventricular zone on sleep-wake cycle and temperature regulation. J Neurosci. 2001 Jul 01; 21(13):4864-74. PMID: 11425913.
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    50. Basheer R, Shiromani PJ. Effects of prolonged wakefulness on c-fos and AP1 activity in young and old rats. Brain Res Mol Brain Res. 2001 Apr 18; 89(1-2):153-7. PMID: 11311986.
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    51. Greco MA, Shiromani PJ. Hypocretin receptor protein and mRNA expression in the dorsolateral pons of rats. Brain Res Mol Brain Res. 2001 Mar 31; 88(1-2):176-82. PMID: 11295245.
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    52. Shiromani PJ, Basheer R, Thakkar J, Wagner D, Greco MA, Charness ME. Sleep and wakefulness in c-fos and fos B gene knockout mice. Brain Res Mol Brain Res. 2000 Aug 14; 80(1):75-87. PMID: 11039731.
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    53. Lu J, Greco MA, Shiromani P, Saper CB. Effect of lesions of the ventrolateral preoptic nucleus on NREM and REM sleep. J Neurosci. 2000 May 15; 20(10):3830-42. PMID: 10804223.
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    54. Greco MA, Lu J, Wagner D, Shiromani PJ. c-Fos expression in the cholinergic basal forebrain after enforced wakefulness and recovery sleep. Neuroreport. 2000 Feb 28; 11(3):437-40. PMID: 10718290.
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    55. Shiromani PJ, Lu J, Wagner D, Thakkar J, Greco MA, Basheer R, Thakkar M. Compensatory sleep response to 12 h wakefulness in young and old rats. . 2000 Jan; 278(1):R125-33. PMID: 10644630.
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    56. Wagner D, Salin-Pascual R, Greco MA, Shiromani PJ. Distribution of hypocretin-containing neurons in the lateral hypothalamus and C-fos-immunoreactive neurons in the VLPO. Sleep Res Online. 2000; 3(1):35-42. PMID: 11382898.
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    57. Lu J, Shiromani P, Saper CB. Retinal input to the sleep-active ventrolateral preoptic nucleus in the rat. Neuroscience. 1999; 93(1):209-14. PMID: 10430484.
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    58. Greco MA, McCarley RW, Shiromani PJ. Choline acetyltransferase expression during periods of behavioral activity and across natural sleep-wake states in the basal forebrain. Neuroscience. 1999; 93(4):1369-74. PMID: 10501461.
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    59. Basheer R, Magner M, McCarley RW, Shiromani PJ. REM sleep deprivation increases the levels of tyrosine hydroxylase and norepinephrine transporter mRNA in the locus coeruleus. Brain Res Mol Brain Res. 1998 Jun 15; 57(2):235-40. PMID: 9675421.
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    60. Greco MA, Magner M, Overstreet D, Shiromani PJ. Expression of cholinergic markers in the pons of Flinders rats. Brain Res Mol Brain Res. 1998 Apr; 55(2):232-6. PMID: 9582425.
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    61. Basheer R, Sherin JE, Saper CB, Morgan JI, McCarley RW, Shiromani PJ. Effects of sleep on wake-induced c-fos expression. J Neurosci. 1997 Dec 15; 17(24):9746-50. PMID: 9391027.
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    62. Shiromani PJ, Winston S, McCarley RW. Pontine cholinergic neurons show Fos-like immunoreactivity associated with cholinergically induced REM sleep. Brain Res Mol Brain Res. 1996 May; 38(1):77-84. PMID: 8737670.
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    63. Sherin JE, Shiromani PJ, McCarley RW, Saper CB. Activation of ventrolateral preoptic neurons during sleep. Science. 1996 Jan 12; 271(5246):216-9. PMID: 8539624.
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    64. Shiromani PJ, Malik M, Winston S, McCarley RW. Time course of Fos-like immunoreactivity associated with cholinergically induced REM sleep. J Neurosci. 1995 May; 15(5 Pt 1):3500-8. PMID: 7751925.
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    65. Shiromani PJ, Magner M, Winston S, Charness ME. Time course of phosphorylated CREB and Fos-like immunoreactivity in the hypothalamic supraoptic nucleus after salt loading. Brain Res Mol Brain Res. 1995 Mar; 29(1):163-71. PMID: 7769993.
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    66. Shiromani PJ, Schwartz WJ. Towards a molecular biology of the circadian clock and sleep of mammals. Adv Neuroimmunol. 1995; 5(2):217-30. PMID: 7496615.
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    67. Shiromani PJ, Overstreet D. Free-running period of circadian rhythms is shorter in rats with a genetically upregulated central cholinergic system. Biol Psychiatry. 1994 Nov 01; 36(9):622-6. PMID: 7833429.
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    68. Zoltoski RK, Velazquez-Moctezuma J, Shiromani PJ, Gillin JC. The relative effects of selective M1 muscarinic antagonists on rapid eye movement sleep. Brain Res. 1993 Apr 16; 608(2):186-90. PMID: 8495352.
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    69. Gillin JC, Salin-Pascual R, Velazquez-Moctezuma J, Shiromani P, Zoltoski R. Cholinergic receptor subtypes and REM sleep in animals and normal controls. Prog Brain Res. 1993; 98:379-87. PMID: 8248526.
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    70. Giovannelli L, Shiromani PJ, Jirikowski GF, Bloom FE. Expression of c-fos protein by immunohistochemically identified oxytocin neurons in the rat hypothalamus upon osmotic stimulation. Brain Res. 1992 Aug 14; 588(1):41-8. PMID: 1393570.
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    71. Shiromani PJ, Kilduff TS, Bloom FE, McCarley RW. Cholinergically induced REM sleep triggers Fos-like immunoreactivity in dorsolateral pontine regions associated with REM sleep. Brain Res. 1992 May 15; 580(1-2):351-7. PMID: 1504815.
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    72. Shiromani PJ. Cholinergic mechanisms in sleep and circadian rhythms. Clin Neuropharmacol. 1992; 15 Suppl 1 Pt A:292A-293A. PMID: 1498846.
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    73. Gillin JC, Sutton L, Ruiz C, Golshan S, Hirsch S, Warmann C, Shiromani P. Dose dependent inhibition of REM sleep in normal volunteers by biperiden, a muscarinic antagonist. Biol Psychiatry. 1991 Jul 15; 30(2):151-6. PMID: 1912107.
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    74. Siegel JM, Nienhuis R, Fahringer HM, Paul R, Shiromani P, Dement WC, Mignot E, Chiu C. Neuronal activity in narcolepsy: identification of cataplexy-related cells in the medial medulla. Science. 1991 May 31; 252(5010):1315-8. PMID: 1925546.
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    75. Shiromani PJ, Klemfuss H, Lucero S, Overstreet DH. Diurnal rhythm of core body temperature is phase advanced in a rodent model of depression. Biol Psychiatry. 1991 May 01; 29(9):923-30. PMID: 2049491.
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    76. Shiromani PJ, Velazquez-Moctezuma J, Overstreet D, Shalauta M, Lucero S, Floyd C. Effects of sleep deprivation on sleepiness and increased REM sleep in rats selectively bred for cholinergic hyperactivity. Sleep. 1991 Apr; 14(2):116-20. PMID: 1650958.
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    77. Velazquez-Moctezuma J, Shalauta M, Gillin JC, Shiromani PJ. Cholinergic antagonists and REM sleep generation. Brain Res. 1991 Mar 08; 543(1):175-9. PMID: 2054672.
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    78. Shiromani PJ, Floyd C, Velázquez-Moctezuma J. Pontine cholinergic neurons simultaneously innervate two thalamic targets. Brain Res. 1990 Nov 05; 532(1-2):317-22. PMID: 2282524.
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    79. Giovannelli L, Shiromani PJ, Jirikowski GF, Bloom FE. Oxytocin neurons in the rat hypothalamus exhibit c-fos immunoreactivity upon osmotic stress. Brain Res. 1990 Oct 29; 531(1-2):299-303. PMID: 2126973.
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    80. Velazquez-Moctezuma J, Shalauta MD, Gillin JC, Shiromani PJ. Microinjections of nicotine in the medial pontine reticular formation elicits REM sleep. Neurosci Lett. 1990 Jul 31; 115(2-3):265-8. PMID: 2234504.
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    81. Shiromani PJ, Lai YY, Siegel JM. Descending projections from the dorsolateral pontine tegmentum to the paramedian reticular nucleus of the caudal medulla in the cat. Brain Res. 1990 May 28; 517(1-2):224-8. PMID: 1695862.
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    82. Velazquez-Moctezuma J, Shiromani PJ, Gillin JC. Acetylcholine and acetylcholine receptor subtypes in REM sleep generation. Prog Brain Res. 1990; 84:407-13. PMID: 2267312.
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    83. Velazquez-Moctezuma J, Shalauta MD, Gillin JC, Shiromani PJ. Differential effects of cholinergic antagonists on REM sleep components. Psychopharmacol Bull. 1990; 26(3):349-53. PMID: 2274635.
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    84. Velazquez-Moctezuma J, Gillin JC, Shiromani PJ. Effect of specific M1, M2 muscarinic receptor agonists on REM sleep generation. Brain Res. 1989 Nov 27; 503(1):128-31. PMID: 2482113.
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    85. Shiromani PJ, Armstrong DM, Gillin JC. Cholinergic neurons from the dorsolateral pons project to the medial pons: a WGA-HRP and choline acetyltransferase immunohistochemical study. Neurosci Lett. 1988 Dec 19; 95(1-3):19-23. PMID: 2465510.
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    86. Shiromani PJ, Overstreet D, Levy D, Goodrich CA, Campbell SS, Gillin JC. Increased REM sleep in rats selectively bred for cholinergic hyperactivity. Neuropsychopharmacology. 1988 May; 1(2):127-33. PMID: 3251494.
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    87. Shiromani PJ, Armstrong DM, Berkowitz A, Jeste DV, Gillin JC. Distribution of choline acetyltransferase immunoreactive somata in the feline brainstem: implications for REM sleep generation. Sleep. 1988 Feb; 11(1):1-16. PMID: 2896380.
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    88. Shiromani PJ, Armstrong DM, Bruce G, Hersh LB, Groves PM, Gillin JC. Relation of pontine choline acetyltransferase immunoreactive neurons with cells which increase discharge during REM sleep. Brain Res Bull. 1987 Mar; 18(3):447-55. PMID: 3580914.
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    89. Shiromani PJ, Gillin JC, Henriksen SJ. Acetylcholine and the regulation of REM sleep: basic mechanisms and clinical implications for affective illness and narcolepsy. Annu Rev Pharmacol Toxicol. 1987; 27:137-56. PMID: 3579239.
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    90. Sutin EL, Shiromani PJ, Kelsoe JR, Storch FI, Gillin JC. Rapid-eye movement sleep and muscarinic receptor binding in rats are augmented during withdrawal from chronic scopolamine treatment. Life Sci. 1986 Dec 22; 39(25):2419-27. PMID: 3796202.
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    91. Shiromani PJ, Fishbein W. Continuous pontine cholinergic microinfusion via mini-pump induces sustained alterations in rapid eye movement (REM) sleep. Pharmacol Biochem Behav. 1986 Dec; 25(6):1253-61. PMID: 3809228.
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    92. Shiromani PJ, McGinty DJ. Pontine neuronal response to local cholinergic infusion: relation to REM sleep. Brain Res. 1986 Oct 29; 386(1-2):20-31. PMID: 3779410.
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    93. Overstreet DH, Janowsky DS, Gillin JC, Shiromani PJ, Sutin EL. Stress-induced immobility in rats with cholinergic supersensitivity. Biol Psychiatry. 1986 Jun; 21(7):657-64. PMID: 3708037.
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    94. Shiromani PJ, Siegel JM, Tomaszewski KS, McGinty DJ. Alterations in blood pressure and REM sleep after pontine carbachol microinfusion. Exp Neurol. 1986 Feb; 91(2):285-92. PMID: 3943576.
      Citations:    
    95. Gutwein BM, Shiromani PJ, Fishbein W. Paradoxical sleep and memory: long-term disruptive effects of Anisomycin. Pharmacol Biochem Behav. 1980 Mar; 12(3):377-84. PMID: 7393935.
      Citations:    
    96. Shiromani P, Gutwein BM, Fishbein W. Development of learning and memory in mice after brief paradoxical sleep deprivation. Physiol Behav. 1979 May; 22(5):971-8. PMID: 228327.
      Citations:    
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