Frequency-dependent modulation of retinogeniculate transmission by serotonin

Journal of Neuroscience

Volumn 24, Issue 48, 2004, Pages 10950-10962

  Seeburg, Daniel P ^a   Liu, Xiaojin ^b   Chen, Chinfei ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

High pass filter; Presynaptic modulation; Serotonin; Sleep; Thalamus; Visual system

Indexed keywords

5 CARBOXYTRYPTAMINE; SEROTONIN; SEROTONIN 1 AGONIST; TRYPTAMINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENICULATE BODY; INTERNEURON; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NEUROMUSCULAR TRANSMISSION; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SEROTONINERGIC SYSTEM; SYNAPTIC TRANSMISSION; VISUAL INFORMATION;

ACTION POTENTIALS; ANIMALS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GENICULATE BODIES; LONG-TERM DEPRESSION (PHYSIOLOGY); MICE; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; PYRIMIDINES; RECEPTOR, SEROTONIN, 5-HT1B; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; RETINAL GANGLION CELLS; SEROTONIN; SEROTONIN AGONISTS; SYNAPSES; SYNAPTIC TRANSMISSION; THALAMUS; TRYPTAMINES; VISUAL PATHWAYS;

EID: 10044271917     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3749-04.2004     Document Type: Article

References (74)

1. Atluri PP, Regehr WG (1998) Delayed release of neurotransmission from cerebellar granule cells. J Neurosci 18:8214-8227.
2. Baxter G, Kennett G, Blaney F, Blackburn T (1995) 5-HT2 receptor sub-types: a family re-united? Trends Pharmacol Sci 16:105-110.
3. Blitz D, Regehr WG (2003) Retinogeniculate synaptic properties controlling spike number and timing in relay neurons. J Neurophysiol 90:2438-2450.
4. 1B receptor is localized predominantly on axon terminals. Neuroscience 58:167-182.
5. Brenowitz S, Trussell LO (2001) Minimizing synaptic depression by control of release probability. J Neurosci 21:1857-1867.
6. B receptors. Neuron 20:135-141.
7. Castro-Alamancos MA (2002) Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. J Neurophysiol 87:946-953.
8. Castro-Alamancos MA, Calcagnotto ME (2001) High-pass filtering of corticothalamic activity by neuromodulators released in the thalamus during arousal: in vitro and in vivo. J Neurophysiol 85:1489-1497.
9. Chen C, Regehr WG (2000) Developmental remodeling of the retinogeniculate synapse. Neuron 28:955-966.
10. Chen C, Regehr WG (2003) Presynaptic modulation of the retinogeniculate synapse. J Neurosci 23:3130-3135.
11. Chen C, Blitz DM, Regehr WG (2002) Contributions of receptor desensitization and saturation to plasticity at the retinogeniculate synapse. Neuron 33:779-788.
12. Curtis DR, Davis R (1962) Pharmacological studies upon neurones of the lateral geniculate nucleus of the cat. Br J Pharmacol 18:217-246.
13. Delaney KR, Zucker RS, Tank DW (1989) Calcium in motor nerve terminals associated with posttetanic potentiation. J Neurosci 9:3558-3567.
14. De Lima AD, Singer W (1987) The serotoninergic fibers in the dorsal lateral geniculate nucleus of the cat: distribution and synaptic connections demonstrated with immunocytochemistry. J Comp Neurol 258:339-351.
15. Dinopoulos A, Dori I, Parnavelas JG (1995) Serotonergic innervation of the lateral geniculate nucleus of the rat during postnatal development: a light and electron microscopic immunocytochemical analysis. J Comp Neurol 363:532-544.
16. Engel G, Gothert M, Hoyer D, Schlicker E, Hillenbrand K (1986) Identity of inhibitory presynaptic 5-hydroxytryptamine (5-HT) autoreceptors in the rat brain cortex with 5-HT1B binding sites. Naunyn-Schmiedebergs Arch Pharmacol 332:1-7.
17. Eysel UT, Pipe HC, Van Schayck R (1986) Excitatory and differential disinhibitory actions of acetylcholine in the lateral geniculate nucleus of the cat. J Physiol (Lond) 370:233-254.
18. Fjeld IT, Ruksenas O, Heggelund P (2002) Brainstem modulation of visual response properties of single cells in the dorsal lateral geniculate nucleus of cat. J Physiol (Lond) 543:541-554.
19. Funke K, Eysel UT (1993) Modulatory effects of acetylcholine, serotonin and nor adrenaline on the activity of cat perigeniculate neurons. Exp Brain Res 95:409-420.
20. Gerard C, Martres MP, Lefevre K, Miquel MC, Verge D, Lanfumey L, Doucet E, Hamon M, el Mestikawy S (1997) Immuno-localization of serotonin 5-HT6 receptor-like material in the rat central nervous system. Brain Res 746:207-219.
21. Glennon RA, Hong SS, Bondarev M, Law H, Dukat M, Rakhi S, Power P, Fan E, Kinneau D, Kamboj R, Teitler M, Herrick-Davis K, Smith C (1996) Binding of O-alkyl derivatives of serotonin at human 5-HT1Db receptors. J Med Chem 39:314-322.
22. Guido W, Lu SM, Vaughan JW, Godwin DW, Sherman SM (1995) Receiver operating characteristic (ROC) analysis of neurons in the cat's lateral geniculate nucleus during tonic and burst response mode. Vis Neurosci 12:723-741.
23. Gustafson EL, Durkin MM, Bard JA, Zgombick J, Branchek TA (1996) A receptor autoradiographic and in situ hybridization analysis of the distribution of the 5-ht7 receptor in rat brain. Br J Pharmacol 117:657-666.
24. Guzman-Marin R, Alam M, Szymusiak R, Drucker-Colin R, Gong H, McGinty D (2000) Discharge modulation of rat dorsal raphe neurons during sleep and waking: effects of preoptic/basal forebrain warming. Brain Res 875:23-34.
25. Jacobs BL, Fornal CA (1999) Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21:9S-15S.
26. Kayama Y (1985) Ascending, descending and local control of neuronal activity in the rat lateral geniculate nucleus. Vision Res 25:339-347.
27. Kayama Y, Shimada S, Hishikawa Y, Ogawa T (1989) Effects of stimulating the doi sal raphe nucleus of the rat on neuronal activity in the dorsal lateral geniculate nucleus. Brain Res 489:1-11.
28. 1A receptors in the rat central nervous system. J Comp Neurol 365:289-305.
29. Lee KH, McCormick DA (1996) Abolition of spindle oscillations by serotonin and norepinephrine in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuron 17:309-321.
30. Lopez-Gimenez JF, Mengod G, Palacios JM, Vilaro MT (2001a) Regional distribution and cellular localization of 5-HT2C receptor mRNA in monkey brain: comparison with [3H]mesulergine binding sites and choline acetyltransferase mRNA. Synapse 42:12-26.
31. Lopez-Gimenez JF, Vilaro MT, Palacios JM, Mengod G (2001b) Mapping of 5-HT2A receptors and their mRNA in monkey brain: [3H]MDL100,907 autoradiography and in situ hybridization studies. J Comp Neurol 429:571-589.
32. Lydic R, McCarley RW, Hobson JA (1983) The time-course of dorsal raphe discharge, PGO waves, and muscle tone averaged across multiple sleep cycles. Brain Res 274:365-370.
33. Marks GA, Speciale SG, Cobbey K, Roffwarg HP (1987) Serotonergic inhibition of the dorsal lateral geniculate nucleus. Brain Res 418:76-84.
34. Mastronarde DN (1987) Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. J Neurophysiol 57:381-413.
35. McCormick DA (1992a) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 39:337-388.
36. McCormickDA (1992b) Neurotransmitter actions in the thalamus and cerebral cortex. J Clin Neurophysiol 9:212-223.
37. McCormick DA, Bal T (1994) Sensory gating mechanisms of the thalamus. Curr Opin Neurobiol 4:550-556.
38. McCormick DA, Bal T (1997) Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci 20:185-215.
39. McCormick DA, Pape HC (1990a) Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones. J Physiol (Lond) 431:319-342.
40. McCormick DA, Pape HC (1990b) Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J Physiol (Lond) 431:291-318.
41. McCormick DA, Wang Z (1991) Serotonin and noradrenaline excite GABAergic neurones of the guinea-pig and cat nucleus reticularis thalami. J Physiol (Lond) 442:235-255.
42. McGinty DJ, Harper RM (1976) Dorsal raphe neurons: depression of firing during sleep in cats. Brain Res 101:569-575.
43. Middlemiss DN, Fozard JR (1983) 8-Hydroxy-2-(di-n-propylamino)-tetralin discriminates between subtypes of the 5-HT1 recognition site. Eur J Pharmacol 90:151-153.
44. Monckton JE, McCormick DA (2002) Neuromodulatory role of serotonin in the ferret thalamus. J Neurophysiol 87:2124-2136.
45. 1B receptors in the superior colliculus of the adult hamster. J Neurophysiol 72:3-13.
46. Mooney RD, Huang X, Shi MY, Bennett-Clarke CA, Rhoades RW (1996) Serotonin modulates retinotectal and corticotectal convergence in the superior colliculus. Prog Brain Res 112:57-69.
47. Mukherjee P, Kaplan E (1995) Dynamics of neurons in the cat lateral geniculate nucleus: in vivo electrophysiology and computational modeling. J Neurophysiol 74:1222-1243.
48. Nirenberg S, Meister M (1997) The light response of retinal ganglion cells is truncated by a displaced amacrine circuit. Neuron 18:637-650.
49. Norton TT, Holdefer RN, Godwin DW (1989) Effects of bicuculline on receptive field center sensitivity of relay cells in the lateral geniculate nucleus. Brain Res 488:348-352.
50. Otis TS, Trussell LO (1996) Inhibition of transmitter release shortens the duration of the excitatory synaptic current at a calyceal synapse. J Neurophysiol 76:3584-3588.
51. Pang JJ, Gao F, Wu SM (2003) Light-evoked excitatory and inhibitory synaptic inputs to ON and OFF alpha ganglion cells in the mouse retina. J Neurosci 23:6063-6073.
52. Papadopoulos GC, Parnavelas JG (1990) Distribution and synaptic organization of serotoninergic and noradrenergic axons in the lateral geniculate nucleus of the rat. J Comp Neurol 294:345-355.
53. Pape HC, McCormick DA (1989) Noradrenaline and serotonin selectively modulate thalamic burst firing by enhancing a hyperpolarization-activated cation current. Nature 340:715-718.
54. Pape HC, McCormick DA (1995) Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral geniculate nucleus. Neuroscience 68:1105-1125.
55. Park D, Dunlap K (1998) Dynamic regulation of calcium influx by G-proteins, action potential waveform, and neuronal firing frequency. J Neurosci 18:6757-6766.
56. 1B receptor-mediated presynaptic inhibition of retinal input to the suprachiasmatic nucleus. J Neurosci 19:4034-4045.
57. Pompeiano M, Palacios JM, Mengod G (1994) Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res Mol Brain Res 23:163-178.
58. Rahamimoff R, Yaari Y (1973) Delayed release of transmitter at the frog neuromuscular junction. J Physiol (Lond) 228:241-257.
59. 2+ and asynchronous transmitter release from the same crayfish bouton. J Physiol (Lond) 501 2:251-262.
60. Richardson BP, Engel G, Donatsch P, Stadler PA (1985) Identification of serotonin M-receptor subtypes and their specific blockade by a new class of drugs. Nature 316:126-131.
61. Rogawski MA, Aghajanian GK (1980) Norepinephrine and serotonin: opposite effects on the activity of lateral geniculate neurons evoked by optic pathway stimulation. Exp Neurol 69:678-694.
62. Sanchez-Vives MV, Bal T, Kim U, von Krosigk M, McCormick DA (1996) Are the interlaminar zones of the ferret dorsal lateral geniculate nucleus actually part of the perigeniculate nucleus? J Neurosci 16:5923-5941.
63. Sari Y, Miquel MC, Brisorgueil MJ, Ruiz G, Doucet E, Hamon M, Verge D (1999) Cellular and subcellular localization of 5-hydroxytryptamine1B receptors in the rat central nervous system: immunocytochemical, autoradiographic and lesion studies. Neuroscience 88:899-915.
64. Schlicker E, Werner U, Hamon M, Gozlan H, Nickel B, Szelenyi I, Gothert M (1992) Anipirtoline, a novel, highly potent 5-HT1B receptor agonist with antinociceptive/antidepressant-like actions in rodents. Br J Pharmacol 105:732-738.
65. Sherman SM (1996) Dual response modes in lateral geniculate neurons: mechanisms and functions. Vis Neurosci 13:205-213.
66. Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679-685.
67. Steriade M, Jones EG, McCormick DA ( 1997) Thalamus. Oxford: Elsevier.
68. Stone C, Pinto LH (1993) Response properties of ganglion cells in the isolated mouse retina. Vis Neurosci 10:31-39.
69. Upton AL, Salichon N, Lebrand C, Ravary A, Blakely R, Seif I, Gaspar P (1999) Excess of serotonin (5-HT) alters the segregation of ipsilateral and contralateral retinal projections in monoamine oxidase A knock-out mice: possible role of 5-HT uptake in retinal ganglion cells during development. J Neurosci 19:7007-7024.
70. Usrey WM, Reppas JB, Reid RC (1998) Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 395:384-387.
71. Van Der Kloot W, Molgo J (1993) Facilitation and delayed release at ∼0°C at the frog neuromuscular junction: effects of calcium chelators, calcium transport inhibitors, and okadaic acid. J Neurophysiol 69:717-729.
72. Wood M, Chaubey M, Atkinson P, Thomas DR (2000) Antagonist activity of meta-chlorophenylpiperazine and partial agonist activity of 8-OH-DPAT at the 5-HT(7) receptor. Eur J Pharmacol 396:1-8.
73. Yoshida M, Sasa M, Takaori S (1984) Serotonin-mediated inhibition from dorsal raphe nucleus of neurons in dorsal lateral geniculate and thalamic reticular nuclei. Brain Res 290:95-105.
74. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.