Differential modulation of excitatory and inhibitory striatal synaptic transmission by histamine

Journal of Neuroscience

Volumn 31, Issue 43, 2011, Pages 15340-15351

  Ellender, Tommas J ^a   Huerta Ocampo, Icnelia ^a   Deisseroth, Karl ^b   Capogna, Marco ^a   Paul Bolam, J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; HISTAMINE; HISTAMINE H2 RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN SLICE; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORPUS STRIATUM; DEPOLARIZATION; ELECTROSTIMULATION; FACILITATION; FEMALE; HISTAMINE RELEASE; INTERNEURON; INTRACELLULAR RECORDING; MALE; MEDIUM SPINY PROJECTION NEURON; MOUSE; NERVE CELL; NERVE CELL NETWORK; NERVE CELL STIMULATION; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; OPTOGENETIC STIMULATION; PATCH CLAMP; POSITIVE FEEDBACK; PRIORITY JOURNAL; SENSORY NERVE; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; THALAMUS; WAKEFULNESS; WHOLE CELL;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CORPUS STRIATUM; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGENTS; EXCITATORY POSTSYNAPTIC POTENTIALS; FEEDBACK, PHYSIOLOGICAL; FEMALE; GABA AGENTS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; HISTAMINE; HISTAMINE AGONISTS; HISTAMINE ANTAGONISTS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, TRANSGENIC; MUTATION; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; PIPERIDINES; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; RHODOPSIN; SYNAPTIC TRANSMISSION; THALAMUS; TRANSFECTION; TYROSINE 3-MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 80054933792     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3144-11.2011     Document Type: Article

References (73)

1. Airaksinen MS, Panula P (1988) The histaminergic system in the guinea pig central nervous system: an immunocytochemical mapping study using an antiserum against histamine. J Comp Neurol 273:163-186.
2. Amphoux A, Vialou V, Drescher E, Brüss M, Mannoury La Cour C, Rochat C, Millan MJ, Giros B, Bönisch H, Gautron S (2006) Differential pharmacological in vitro properties of organic cation transporters and regional distribution in rat brain. Neuropharmacology 50:941-952.
3. Anaclet C, Parmentier R, Ouk K, Guidon G, Buda C, Sastre JP, Akaoka H, Sergeeva OA, Yanagisawa M, Ohtsu H, Franco P, Haas HL, Lin JS (2009) Orexin/hypocretin and histamine: distinct roles in the control of wakefulness demonstrated using knock-out mouse models. J Neurosci 29:14423-14438.
4. Aston-Jones G, Bloom FE (1981) Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1:876-886.
5. Atzori M, Lau D, Tansey EP, Chow A, Ozaita A, Rudy B, McBain CJ (2000) H2 histamine receptor-phosphorylation of Kv3.2 modulates interneuron fast spiking. Nat Neurosci 3:791-798.
6. Bolam JP, Izzo PN (1988) The postsynaptic targets of substance P-immunoreactive terminals in the rat neostriatum with particular reference to identified spiny striatonigral neurons. Exp Brain Res 70:361-377.
7. Brown RE, Haas HL (1999) On the mechanism of histaminergic inhibition of glutamate release in the rat dentate gyrus. J Physiol 515:777-786.
8. Carter AG, Sabatini BL (2004) State-dependent calcium signaling in dendritic spines of striatal medium spiny neurons. Neuron 44:483-493.
9. Chu M, Huang ZL, Qu WM, Eguchi N, Yao MH, Urade Y (2004) Extracellular histamine level in the frontal cortex is positively correlated with the amount of wakefulness in rats. Neurosci Res 49:417-420.
10. Ding J, Peterson JD, Surmeier DJ (2008) Corticostriatal and thalamostriatal synapses have distinctive properties. J Neurosci 28:6483-6492.
11. Ding JB, Guzman JN, Peterson JD, Goldberg JA, Surmeier DJ (2010) Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67:294-307.
12. Doig NM, Moss J, Bolam JP (2010) Cortical and thalamic innervation of direct and indirect pathway medium-sized spiny neurons in mouse striatum. J Neurosci 30:14610-14618.
13. Doreulee N, Yanovsky Y, Flagmeyer I, Stevens DR, Haas HL, Brown RE (2001) Histamine H(3) receptors depress synaptic transmission in the corticostriatal pathway. Neuropharmacology 40:106-113.
14. Ercan-Sencicek AG, Stillman AA, Ghosh AK, Bilguvar K, O'Roak BJ, Mason CE, Abbott T, Gupta A, King RA, Pauls DL, Tischfield JA, Heiman GA, Singer HS, Gilbert DL, Hoekstra PJ, Morgan TM, Loring E, Yasuno K, Fernandez T, Sanders S, et al (2010) L-histidine decarboxylase and Tourette's syndrome. N Engl J Med 362:1901-1908.
15. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma FJ Jr, Sibley DR (1990) D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250:1429-1432.
16. Gittis AH, Nelson AB, Thwin MT, Palop JJ, Kreitzer AC (2010) Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J Neurosci 30:2223-2234.
17. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, HeintzN (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925.
18. Graybiel AM, Aosaki T, Flaherty AW, Kimura M (1994) The basal ganglia and adaptive motor control. Science 265:1826-1831.
19. Grillner S, Hellgren J, Mé nard A, Saitoh K, Wikström MA (2005) Mechanisms for selection of basic motor programs-roles for the striatum and pallidum. Trends Neurosci 28:364-370.
20. Haas H, Panula P (2003) The role of histamine and the tuberomamillary nucleus in the nervous system. Nat Rev Neurosci 4:121-130.
21. Hill SJ, Young JM (1980) Histamine H1-receptors in the brain of the guinea-pig and the rat: differences in ligand binding properties and regional distribution. Br J Pharmacol 68:687-696.
22. Inagaki N, Yamatodani A, Ando-Yamamoto M, Tohyama M, Watanabe T, Wada H (1988) Organization of histaminergic fibers in the rat brain. J Comp Neurol 273:283-300.
23. Jaeger D, Kita H, Wilson CJ (1994) Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. J Neurophysiol 72:2555-2558.
24. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527-535.
25. Kincaid AE, Zheng T, Wilson CJ (1998) Connectivity and convergence of single corticostriatal axons. J Neurosci 18:4722-4731.
26. Kinomura S, Larsson J, Gulyás B, Roland PE (1996) Activation by attention of the human reticular formation and thalamic intralaminar nuclei. Science 271:512-515.
27. Koós T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467-472.
28. Koós T, Tepper JM (2002) Dual cholinergic control of fast-spiking interneurons in the neostriatum. J Neurosci 22:529-535.
29. Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, Deisseroth K, Kreitzer AC (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466:622-626.
30. Kuramoto E, Furuta T, Nakamura KC, Unzai T, Hioki H, Kaneko T (2009) Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb Cortex 19:2065-2077.
31. Lacey CJ, Bolam JP, Magill PJ (2007) Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections. J Neurosci 27:4374-4384.
32. Lin JS, Sakai K, Jouvet M (1988) Evidence for histaminergic arousal mechanisms in the hypothalamus of cat. Neuropharmacology 27:111-122.
33. Mallet N, Le Moine C, Charpier S, Gonon F (2005) Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J Neurosci 25:3857-3869.
34. Martinez-Mir MI, Pollard H, Moreau J, Arrang JM, Ruat M, Traiffort E, Schwartz JC, Palacios JM (1990) Three histamine receptors (H1, H2 and H3) visualized in the brain of human and non-human primates. Brain Res 526:322-327.
35. Mathur BN, Capik NA, Alvarez VA, Lovinger DM (2011) Serotonin induces long-term depression at corticostriatal synapses. J Neurosci 31:7402-7411.
36. Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85:960-976.
37. Morisset S, Rouleau A, Ligneau X, Gbahou F, Tardivel-Lacombe J, Stark H, Schunack W, Ganellin CR, Schwartz JC, Arrang JM (2000) High constitutive activity of native H3 receptors regulates histamine neurons in brain. Nature 408:860-864.
38. + conductance by histamine H1 and H2 receptors in neurones dissociated from rat neostriatum. J Physiol 480:233-245.
39. Pakhotin P, Bracci E (2007) Cholinergic interneurons control the excitatory input to the striatum. J Neurosci 27:391-400.
40. Parent M, Wallman MJ, Gagnon D, Parent A (2011) Serotonin innervation of basal ganglia in monkeys and humans. J Chem Neuroanat 41:256-265.
41. Parmentier R, Ohtsu H, Djebbara-Hannas Z, Valatx JL, Watanabe T, Lin JS (2002) Anatomical, physiological, and pharmacological characteristics of histidine decarboxylase knock-out mice: evidence for the role of brain histamine in behavioral and sleep-wake control. J Neurosci 22:7695-7711.
42. Petzold GC, Hagiwara A, Murthy VN (2009) Serotonergic modulation of odor input to the mammalian olfactory bulb. Nat Neurosci 12:784-791.
43. Pillot C, Heron A, Cochois V, Tardivel-Lacombe J, Ligneau X, Schwartz JC, Arrang JM (2002) A detailed mapping of the histamine H(3) receptor and its gene transcripts in rat brain. Neuroscience 114:173-193.
44. Planert H, Szydlowski SN, Hjorth JJ, Grillner S, Silberberg G (2010) Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways. J Neurosci 30:3499-3507.
45. Plenz D (2003) When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function. Trends Neurosci 26:436-443.
46. Ponzi A, Wickens J (2010) Sequentially switching cell assemblies in random inhibitory networks of spiking neurons in the striatum. J Neurosci 30:5894-5911.
47. Prast H, Tran MH, Lamberti C, Fischer H, Kraus M, Grass K, Philippu A (1999) Histaminergic neurons modulate acetylcholine release in the ventral striatum: role of H1 and H2 histamine receptors. Naunyn Schmiedebergs Arch Pharmacol 360:552-557.
48. Reiner PB, McGeer EG (1987) Electrophysiological properties of cortically projecting histamine neurons of the rat hypothalamus. Neurosci Lett 73:43-47.
49. Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241-263.
50. Schwartz JC (2011) The histamine H3 receptor: from discovery to clinical trials with pitolisant. Br J Pharmacol 163:713-721.
51. Schwartz JC, Arrang JM, Garbarg M, Pollard H, Ruat M (1991) Histaminergic transmission in the mammalian brain. Physiol Rev 71:1-51.
52. Smeal RM, Gaspar RC, Keefe KA, Wilcox KS (2007) A rat brain slice preparation for characterizing both thalamostriatal and corticostriatal afferents. J Neurosci Methods 159:224-235.
53. Smith Y, Bevan MD, Shink E, Bolam JP (1998) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86:353-387.
54. Somogyi P, Bolam JP, Smith AD (1981) Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure. J Comp Neurol 195:567-584.
55. Steinbusch HW (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6:557-618.
56. Steininger TL, Alam MN, Gong H, Szymusiak R, McGinty D (1999) Sleepwaking discharge of neurons in the posterior lateral hypothalamus of the albino rat. Brain Res 840:138-147.
57. Stern EA, Jaeger D, Wilson CJ (1998) Membrane potential synchrony of simultaneously recorded striatal spiny neurons in vivo. Nature 394:475-478.
58. Sugita S, Uchimura N, Jiang ZG, North RA (1991) Distinct muscarinic receptors inhibit release of gamma-aminobutyric acid and excitatory amino acids in mammalian brain. Proc Natl Acad Sci U S A 88:2608-2611.
59. Surmeier DJ, Ding J, Day M, Wang Z, Shen W (2007) D1 and D2 dopaminereceptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 30:228-235.
60. Takagi H, Morishima Y, Matsuyama T, Hayashi H, Watanabe T, Wada H (1986) Histaminergic axons in the neostriatum and cerebral cortex of the rat: a correlated light and electron microscopic immunocytochemical study using histidine decarboxylase as a marker. Brain Res 364:114-123.
61. Takahashi K, Lin JS, Sakai K (2006) Neuronal activity of histaminergic tuberomammillary neurons during wake-sleep states in the mouse. J Neurosci 26:10292-10298.
62. Tepper JM, Bolam JP (2004) Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 14:685-692.
63. Tepper JM, Plenz D (2006) Microcircuits in the striatum: striatal cell types and their interaction. In: Microcircuits: the interface between neurons and global brain function (Grillner S, Graybiel AM, eds), pp 127-148. Cambridge, MA: MIT.
64. Tepper JM, Koós T, Wilson CJ (2004) GABAergic microcircuits in the neostriatum. Trends Neurosci 27:662-669.
65. Thomson AM (2000) Molecular frequency filters at central synapses. Prog Neurobiol 62:159-196.
66. Threlfell S, Cragg SJ (2011) Dopamine signaling in dorsal versus ventral striatum: the dynamic role of cholinergic interneurons. Front Syst Neurosci 5:11.
67. Threlfell S, Cragg SJ, Kalló I, Turi GF, Coen CW, Greenfield SA (2004) Histamine H3 receptors inhibit serotonin release in substantia nigra pars reticulata. J Neurosci 24:8704-8710.
68. Ungless MA (2004) Dopamine: the salient issue. Trends Neurosci 27:702-706.
69. Vizuete ML, Traiffort E, Bouthenet ML, Ruat M, Souil E, Tardivel-Lacombe J, Schwartz JC (1997) Detailed mapping of the histamine H2 receptor and its gene transcripts in guinea-pig brain. Neuroscience 80:321-343.
70. Wilson CJ (2007) GABAergic inhibition in the neostriatum. Prog Brain Res 160:91-110.
71. Yanovsky Y, Li S, Klyuch BP, Yao Q, Blandina P, Passani MB, Lin JS, Haas H, Sergeeva OA (2011) L-Dopa activates histaminergic neurons. J Physiol 589:1349-1366.
72. Yin HH, Knowlton BJ (2006) The role of the basal ganglia in habit formation. Nat Rev Neurosci 7:464-476.
73. Yoshitake T, Yamaguchi M, Nohta H, Ichinose F, Yoshida H, Yoshitake S, Fuxe K, Kehr J (2003) Determination of histamine in microdialysis samples from rat brain by microbore column liquid chromatography following intramolecular excimer-forming derivatization with pyrene-labeling reagent. J Neurosci Methods 127:11-17.