Presynaptic gating of excitation in the dorsal raphe nucleus by GABA

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 39, 2013, Pages 15800-15805

  Soiza Reilly, Mariano ^a,b   Anderson, Wayne B ^c   Vaughan, Christopher W ^c   Commons, Kathryn G ^a,b  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Axoaxonic; Glutamate decarboxylase 65; Ultrastructure; Vesicular glutamate transporter (VGLUT)

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID;

ANIMAL CELL; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CHANNEL GATING; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; ELECTRON MICROSCOPY; IMMUNOFLUORESCENCE; NERVE CELL STIMULATION; NERVE FIBER; NONHUMAN; PRESYNAPTIC GATING; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNAPSE;

AXOAXONIC; GLUTAMATE DECARBOXYLASE 65; ULTRASTRUCTURE; VESICULAR GLUTAMATE TRANSPORTER (VGLUT);

ANIMALS; AXONS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATES; PRESYNAPTIC TERMINALS; RAPHE NUCLEI; RATS; RECEPTORS, GABA-A; SEROTONERGIC NEURONS; TOMOGRAPHY;

EID: 84884635572     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1304505110     Document Type: Article

References (49)

1. Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72(1):165-229.
2. Amat J, et al. (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8(3):365-371.
3. Nakamura K, Matsumoto M, Hikosaka O (2008) Reward-dependent modulation of neuronal activity in the primate dorsal raphe nucleus. J Neurosci 28(20):5331-5343.
4. Takahashi A, Shimamoto A, Boyson CO, DeBold JF, Miczek KA (2010) GABA(B) receptor modulation of serotonin neurons in the dorsal raphé nucleus and escalation of aggression in mice. J Neurosci 30(35):11771-11780.
5. Bruchas MR, et al. (2011) Selective p38? MAPK deletion in serotonergic neurons produces stress resilience in models of depression and addiction. Neuron 71(3): 498-511.
6. Stockmeier CA (1997) Neurobiology of serotonin in depression and suicide. Ann N Y Acad Sci 836:220-232.
7. Arango V, Underwood MD, Mann JJ (2002) Serotonin brain circuits involved in major depression and suicide. Prog Brain Res 136:443-453.
8. Jolas T, Aghajanian GK (1997) Opioids suppress spontaneous and NMDA-induced inhibitory postsynaptic currents in the dorsal raphe nucleus of the rat in vitro. Brain Res 755(2):229-245.
9. Commons KG (2009) Locally collateralizing glutamate neurons in the dorsal raphe nucleus responsive to substance P contain vesicular glutamate transporter 3 (VGLUT3). J Chem Neuroanat 38(4):273-281.
10. Hioki H, et al. (2010) Vesicular glutamate transporter 3-expressing nonserotonergic projection neurons constitute a subregion in the rat midbrain raphe nuclei. J Comp Neurol 518(5):668-686.
11. Lee HS, Kim MA, Valentino RJ, Waterhouse BD (2003) Glutamatergic afferent projections to the dorsal raphe nucleus of the rat. Brain Res 963(1-2):57-71.
12. Soiza-Reilly M, Commons KG (2011) Glutamatergic drive of the dorsal raphe nucleus. J Chem Neuroanat 41(4):247-255.
13. Gervasoni D, et al. (2000) Role and origin of the GABAergic innervation of dorsal raphe serotonergic neurons. J Neurosci 20(11):4217-4225.
14. Kirouac GJ, Li S, Mabrouk G (2004) GABAergic projection from the ventral tegmental area and substantia nigra to the periaqueductal gray region and the dorsal raphe nucleus. J Comp Neurol 469(2):170-184.
15. Lavezzi HN, Parsley KP, Zahm DS (2012) Mesopontine rostromedial tegmental nucleus neurons projecting to the dorsal raphe and pedunculopontine tegmental nucleus: Psychostimulant-elicited Fos expression and collateralization. Brain Struct Funct 217(3):719-734.
16. Mishchenko Y, et al. (2010) Ultrastructural analysis of hippocampal neuropil from the connectomics perspective. Neuron 67(6):1009-1020.
17. Micheva KD, Smith SJ (2007) Array tomography: A new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55(1):25-36.
18. Micheva KD, Busse B, Weiler NC, O'Rourke N, Smith SJ (2010) Single-synapse analysis of a diverse synapse population: Proteomic imaging methods and markers. Neuron 68(4):639-653.
19. Soiza-Reilly M, Commons KG (2011) Quantitative analysis of glutamatergic innervation of the mouse dorsal raphe nucleus using array tomography. J Comp Neurol 519(18):3802-3814.
20. Peters A, Palay SL (1996) The morphology of synapses. J Neurocytol 25(12):687-700.
21. Descarries L, Watkins KC, Garcia S, Beaudet A (1982) The serotonin neurons in nucleus raphe dorsalis of adult rat: A light and electron microscope radioautographic study. J Comp Neurol 207(3):239-254.
22. Marinelli S, et al. (2004) Serotonergic and nonserotonergic dorsal raphe neurons are pharmacologically and electrophysiologically heterogeneous. J Neurophysiol 92(6): 3532-3537.
23. Isaacson JS, Solís JM, Nicoll RA (1993) Local and diffuse synaptic actions of GABA in the hippocampus. Neuron 10(2):165-175.
24. Belin MF, et al. (1979) GABA-accumulating neurons in the nucleus raphe dorsalis and periaqueductal gray in the rat: A biochemical and radioautographic study. Brain Res 170(2):279-297.
25. Allers KA, Sharp T (2003) Neurochemical and anatomical identification of fast-and slow-firing neurones in the rat dorsal raphe nucleus using juxtacellular labelling methods in vivo. Neuroscience 122(1):193-204.
26. Fu W, et al. (2010) Chemical neuroanatomy of the dorsal raphe nucleus and adjacent structures of the mouse brain. J Comp Neurol 518(17):3464-3494.
27. Lemos JC, et al. (2006) Selective 5-HT receptor inhibition of glutamatergic and GABAergic synaptic activity in the rat dorsal and median raphe. Eur J Neurosci 24(12):3415-3430.
28. Abellán MT, Jolas T, Aghajanian GK, Artigas F (2000) Dual control of dorsal raphe serotonergic neurons by GABA(B) receptors. Electrophysiological and microdialysis studies. Synapse 36(1):21-34.
29. Vaughan CW, Christie MJ (1996) Increase by the ORL1 receptor (opioid receptor-like1) ligand, nociceptin, of inwardly rectifying K conductance in dorsal raphe nucleus neurones. Br J Pharmacol 117(8):1609-1611.
30. Colmers WF, Williams JT (1988) Pertussis toxin pretreatment discriminates between pre-and postsynaptic actions of baclofen in rat dorsal raphe nucleus in vitro. Neurosci Lett 93(2-3):300-306.
31. Jang IS, Jeong HJ, Akaike N (2001) Contribution of the Na-K-Cl cotransporter on GABA(A) receptor-mediated presynaptic depolarization in excitatory nerve terminals. J Neurosci 21(16):5962-5972.
32. Jang IS, Nakamura M, Ito Y, Akaike N (2006) Presynaptic GABAA receptors facilitate spontaneous glutamate release from presynaptic terminals on mechanically dissociated rat CA3 pyramidal neurons. Neuroscience 138(1):25-35.
33. Stell BM, Rostaing P, Triller A, Marty A (2007) Activation of presynaptic GABA(A) receptors induces glutamate release from parallel fiber synapses. J Neurosci 27(34): 9022-9031.
34. Pugh JR, Jahr CE (2011) Axonal GABAA receptors increase cerebellar granule cell excitability and synaptic activity. J Neurosci 31(2):565-574.
35. Price GD, Trussell LO (2006) Estimate of the chloride concentration in a central glutamatergic terminal: A gramicidin perforated-patch study on the calyx of Held. J Neurosci 26(44):11432-11436.
36. Awatramani GB, Price GD, Trussell LO (2005) Modulation of transmitter release by presynaptic resting potential and background calcium levels. Neuron 48(1):109-121.
37. Nitz D, Siegel J (1997) GABA release in the dorsal raphe nucleus: Role in the control of REM sleep. Am J Physiol 273(1 Pt 2):R451-R455.
38. Levine ES, Jacobs BL (1992) Neurochemical afferents controlling the activity of serotonergic neurons in the dorsal raphe nucleus: Microiontophoretic studies in the awake cat. J Neurosci 12(10):4037-4044.
39. Herzog E, et al. (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21(22):RC181.
40. Tao R, Auerbach SB (2003) Influence of inhibitory and excitatory inputs on serotonin efflux differs in the dorsal and median raphe nuclei. Brain Res 961(1):109-120.
41. Krystal JH, et al. (2002) Glutamate and GABA systems as targets for novel antidepressant and mood-stabilizing treatments. Mol Psychiatry 7(Suppl 1):S71-S80.
42. Kalueff AV, Nutt DJ (2007) Role of GABA in anxiety and depression. Depress Anxiety 24(7):495-517.
43. Liu GX, et al. (2007) Reduced anxiety and depression-like behaviors in mice lacking GABA transporter subtype 1. Neuropsychopharmacology 32(7):1531-1539.
44. Jindal RD, Thase ME (2004) Treatment of insomnia associated with clinical depression. Sleep Med Rev 8(1):19-30.
45. Thévenaz P, Ruttimann UE, Unser M (1998) A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7(1):27-41.
46. Bolte S, Cordelières FP (2006) A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224(Pt 3):213-232.
47. van Steensel B, et al. (1996) Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons. J Cell Sci 109(Pt 4):787-792.
48. Commons KG, Beck SG, Bey VW (2005) Two populations of glutamatergic axons in the rat dorsal raphe nucleus defined by the vesicular glutamate transporters 1 and 2. Eur J Neurosci 21(6):1577-1586.
49. Drew GM, Mitchell VA, Vaughan CW (2008) Glutamate spillover modulates GABAergic synaptic transmission in the rat midbrain periaqueductal grey via metabotropic glutamate receptors and endocannabinoid signaling. J Neurosci 28(4): 808-815.