Dorsal raphe serotonin neurons in mice: Immature hyperexcitability transitions to adult state during first three postnatal weeks suggesting sensitive period for environmental perturbation

Journal of Neuroscience

Volumn 34, Issue 14, 2014, Pages 4809-4821

  Rood, Benjamin D ^a,b   Calizo, Lyngine H ^a   Piel, David ^a   Spangler, Zachary P ^a   Campbell, Kaitlin ^b   Beck, Sheryl G ^a,b  

^a CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; SEROTONIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ANXIETY; ARTICLE; BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; CENTRAL NERVOUS SYSTEM FUNCTION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMOTIONALITY; ENZYME ACTIVITY; GABAERGIC TRANSMISSION; HYPEREXCITABILITY TRANSITION; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL; NERVE EXCITABILITY; NONHUMAN; PERTURBATION THEORY; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SEROTONINERGIC NERVE CELL; SIGNAL TRANSDUCTION; WHOLE CELL PATCH CLAMP;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BACTERIAL PROTEINS; BICUCULLINE; ENVIRONMENT; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA-A RECEPTOR ANTAGONISTS; GUANOSINE 5'-O-(3-THIOTRIPHOSPHATE); LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; QUINOXALINES; RAPHE NUCLEI; SEROTONERGIC NEURONS; SEROTONIN; SEROTONIN RECEPTOR AGONISTS; TRANSCRIPTION FACTORS;

EID: 84899461485     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1498-13.2014     Document Type: Article

References (63)

1. Agid O, Shapira B, Zislin J, Ritsner M, Hanin B, Murad H, Troudart T, Bloch M, Heresco-Levy U, Lerer B (1999) Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Mol Psychiatry 4:163-172.CrossRef Medline
2. Aitken AR, Törk I (1988) Early development of serotonin-containing neurons and pathways as seen in wholemount preparations of the fetal rat brain. J Comp Neurol 274:32-47.CrossRef Medline
3. Aller MI, Wisden W (2008) Changes in expression of some two-pore domain potassium channel genes (KCNK) in selected brain regions of developing mice. Neuroscience 151:1154-1172.CrossRef Medline
4. Alonso A, Merchán P, Sandoval JE, Sánchez-Arrones L, Garcia-Cazorla A, Artuch R, Ferrán JL, Martínez-de-la-torre M, Puelles L (2013) Development of the serotonergic cells in murine raphe nuclei and their relations with rhombomeric domains. Brain structure and function 218: 1229-1277.CrossRef Medline
5. Altman J, Bayer SA (1981) Development of the brain stem in the rat. V. Thymidine-radiographic study of the time of origin of neurons in the midbrain tegmentum. J Comp Neurol 198:677-716.CrossRef Medline
6. Amilhon B, Lepicard E, Renoir T, Mongeau R, Popa D, Poirel O, Miot S, Gras C, Gardier AM, Gallego J, Hamon M, Lanfumey L, Gasnier B, Giros B, El Mestikawy S (2010) VGluT3 (vesicular glutamate transporter type 3) contribution to the regulation of serotonergic transmission and anxiety. J Neurosci 30:2198-2210.CrossRef Medline
7. Andrade R, Nicoll RA (1987) Pharmacologically distinct actions of serotonin on single pyramidal neurones of the rat hippocampus recorded in vitro. J Physiol 394:99-124. Medline
8. Andrade R, Malenka RC, Nicoll RA (1986) A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 234:1261-1265.CrossRef Medline
9. Beck SG, Pan YZ, Akanwa AC, Kirby LG (2004) Median and dorsal raphe neurons are not electrophysiologically identical. J Neurophysiol 91:994-1005.CrossRef Medline
10. Béïque JC, Campbell B, Perring P, Hamblin MW, Walker P, Mladenovic L, Andrade R (2004) Serotonergic regulation of membrane potential in developing rat prefrontal cortex: coordinated expression of 5-hydroxytryptamine (5-HT)1A, 5-HT2A, and 5-HT7 receptors. J Neurosci 24:4807-4817.CrossRef Medline
11. Ben-Ari Y (2002) Excitatory actions of gaba during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.CrossRef Medline
12. Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa JL (1997) GABAA,NMDAand AMPA receptors: a developmentally regulated "menage a trois." Trends Neurosci 20:523-529. CrossRef
13. Benekareddy M, Goodfellow NM, Lambe EK, Vaidya VA (2010) Enhanced function of prefrontal serotonin 5-HT(2) receptors in a rat model of psychiatric vulnerability. J Neurosci 30:12138-12150.CrossRef Medline
14. Beutler LR, Eldred KC, Quintana A, Keene CD, Rose SE, Postupna N, Montine TJ, Palmiter RD (2011) Severely impaired learning and altered neuronal morphology in mice lacking NMDA receptors in medium spiny neurons. PLoS One 6:e28168.CrossRef Medline
15. Bortone D, Polleux F (2009) KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 62:53-71.CrossRef Medline
16. Calizo LH, Akanwa A, Ma X, Pan YZ, Lemos JC, Craige C, Heemstra LA, Beck SG (2011) Raphe serotonin neurons are not homogenous: electrophysiological, morphological and neurochemical evidence. Neuropharmacology 61:524-543.CrossRef Medline
17. Cameron WE, Núñez-Abades PA, Kerman IA, Hodgson TM (2000) Role of potassium conductances in determining input resistance of developing brain stem motoneurons. J Neurophysiol 84:2330-2339. Medline
18. Carr GV, Lucki I (2011) The role of serotonin receptor subtypes in treating depression: a review of animal studies. Psychopharmacology (Berl) 213: 265-287.CrossRef Medline
19. 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 38:273-281.CrossRef Medline
20. Crawford LK, Craige CP, Beck SG (2010) Increased intrinsic excitability of lateral wing serotonin neurons of the dorsal raphe: a mechanism for selective activation in stress circuits. J Neurophysiol 103:2652-2663.CrossRef Medline
21. Crawford LK, Craige CP, Beck SG (2011) Glutamatergic input is selectively increased in dorsal raphe subfield 5-HT neurons: role of morphology, topography and selective innervation. Eur J Neurosci 34:1794-1806.CrossRef Medline
22. De Bellis MD, Thomas LA (2003) Biologic findings of post-traumatic stress disorder and child maltreatment. Current psychiatry reports 5:108-117.CrossRef Medline
23. De Bellis MD, Keshavan MS, Clark DB, Casey BJ, Giedd JN, Boring AM, Frustaci K, Ryan ND (1999) A.E. Bennett Research Award. Developmental traumatology. Part II: brain development. Biol Psychiatry 45: 1271-1284.CrossRef Medline
24. Donaldson ZR, Piel DA, Santos TL, Richardson-Jones J, Leonardo ED, Beck SG, Champagne FA, Hen R (2014) Developmental effects of serotonin 1A autoreceptors on anxiety and social behavior. Neuropsychopharmacology 39:291-302.CrossRef Medline
25. Enyedi P, Czirják G (2010) Molecular background of leak K_ currents: two-pore domain potassium channels. Physiol Rev 90:559-605.CrossRef Medline
26. Ferreira TA, Iacono LL, Gross CT (2010) Serotonin receptor 1A modulates actin dynamics and restricts dendritic growth in hippocampal neurons. Eur J Neurosci 32:18-26.CrossRef Medline
27. Fremeau RT Jr, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci U S A 99:14488-14493.CrossRef Medline
28. Goodfellow NM, Benekareddy M, Vaidya VA, Lambe EK (2009) Layer II/IIIof the prefrontal cortex: inhibition by the serotonin 5-HT1A receptor in development and stress. J Neurosci 29:10094-10103.CrossRef Medline
29. Hawthorne AL, Wylie CJ, Landmesser LT, Deneris ES, Silver J (2010) Serotonergic neurons migrate radially through the neuroepithelium by dynamin-mediated somal translocation. J Neurosci 30:420-430.CrossRef Medline
30. Hendricks TJ, Fyodorov DV, Wegman LJ, Lelutiu NB, Pehek EA, Yamamoto B, Silver J, Weeber EJ, Sweatt JD, Deneris ES (2003) Pet-1 ETS gene plays a critical role in 5-HT neuron development and is required for normal anxiety-like and aggressive behavior. Neuron 37:233-247.CrossRef Medline
31. Heurteaux C, Lucas G, Guy N, El Yacoubi M, Thümmler S, Peng XD, Noble F, Blondeau N, Widmann C, Borsotto M, Gobbi G, Vaugeois JM, Debonnel G, Lazdunski M (2006) Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype. Nat Neurosci 9:1134-1141.CrossRef Medline
32. Honoré E (2007) The neuronal background K2P channels: focus on TREK1. Nat Rev Neurosci 8:251-261.CrossRef Medline
33. Jensen P, Farago AF, Awatramani RB, Scott MM, Deneris ES, Dymecki SM (2008) Redefining the serotonergic system by genetic lineage. Nat Neurosci 11:417-419.CrossRef Medline
34. Kasper EM, Lübke J, Larkman AU, Blakemore C (1994) Pyramidal neurons in layer 5 of the rat visual cortex. III. Differential maturation of axon targeting, dendritic morphology, and electrophysiological properties. J Comp Neurol 339:495-518.CrossRef Medline
35. Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE (2005) Prevalence, severity, and comorbidity of 12-month DSM-IV disorders in the National Comorbidity Survey Replication. Arch Gen Psychiatry 62:617-627.CrossRef Medline
36. Kim GT, Cho YW, Tak HM, Lee JS, Kim EJ, Han J, Kang D (2012) Agerelated changes in two-pore domain acid-sensitive K(+) channel expression in rat dorsal root ganglion neurons. Clinical and experimental pharmacology and physiology 39:43-48.CrossRef Medline
37. Koen N, Stein DJ (2011) Pharmacotherapy of anxiety disorders: a critical review. Dialogues Clin Neurosci 13:423-437. Medline
38. Leinekugel X (2003) Developmental patterns and plasticities: the hippocampal model. J Physiol Paris 97:27-37.CrossRef Medline
39. Lemos JC, Pan YZ, Ma X, Lamy C, Akanwa AC, Beck SG (2006) Selective 5-HT receptor inhibition of glutamatergic and GABAergic synaptic activity in the rat dorsal and median raphe. Eur J Neurosci 24:3415-3430.CrossRef Medline
40. Lemos JC, Zhang G, Walsh T, Kirby LG, Akanwa A, Brooks-Kayal A, Beck SG (2011) Stress-hyperresponsive WKY rats demonstrate depressed dorsal raphe neuronal excitability and dysregulated CRF-mediated responses. Neuropsychopharmacology 36:721-734.CrossRef Medline
41. Lesage F, Lazdunski M (2000) Molecular and functional properties of twopore- domain potassium channels. Am J Physiol Renal Physiol 279:F793-F801. Medline
42. Lesch KP, Waider J (2012) Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders. Neuron 76:175-191.CrossRef Medline
43. Lidov HG, Molliver ME (1982) Immunohistochemical study of the development of serotonergic neurons in the rat CNS. Brain Res Bull 9:559-604.CrossRef Medline
44. Liu RJ, Lambe EK, Aghajanian GK (2005) Somatodendritic autoreceptor regulation of serotonergic neurons: dependence on L-tryptophan and tryptophan hydroxylase-activating kinases. Eur J Neurosci 21:945-958.CrossRef Medline
45. 2+/calmodulin-dependent protein kinase II contributes to the developmental programming of anxiety in serotonin receptor 1A knock-out mice. J Neurosci 28:6250-6257.CrossRef Medline
46. Ma XY, Yu JM, Zhang SZ, Liu XY, Wu BH, Wei XL, Yan JQ, Sun HL, Yan HT, Zheng JQ (2011) External Ba2+ block of the two-pore domain potassium channel TREK-1 defines conformational transition in its selectivity filter. J Biol Chem 286:39813-39822.CrossRef Medline
47. Marinelli S, Schnell SA, Hack SP, Christie MJ, Wessendorf MW, Vaughan CW (2004) Serotonergic and nonserotonergic dorsal raphe neurons are pharmacologically and electrophysiologically heterogeneous. J Neurophysiol 92:3532-3537.CrossRef Medline
48. Migliarini S, Pacini G, Pelosi B, Lunardi G, Pasqualetti M (2013) Lack of brain serotonin affects postnatal development and serotonergic neuronal circuitry formation. Mol Psychiatry 18:1106-1118.CrossRef Medline
49. Okuhara DY, Beck SG (1998) Corticosteroids alter 5-hydroxytryptamine1A receptor-effector pathway in hippocampal subfield CA3 pyramidal cells. J Pharmacol Exp Ther 284:1227-1233. Medline
50. Päsler D, Gabriel S, Heinemann U (2007) Two-pore-domain potassium channels contribute to neuronal potassium release and glial potassium buffering in the rat hippocampus. Brain Res 1173:14-26.CrossRef Medline
51. Ramboz S, Oosting R, Amara DA, Kung HF, Blier P, Mendelsohn M, Mann JJ, Brunner D, Hen R (1998) Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc Natl Acad Sci U S A 95:14476-14481.CrossRef Medline
52. Richardson-Jones JW, Craige CP, Guiard BP, Stephen A, Metzger KL, Kung HF, Gardier AM, Dranovsky A, David DJ, Beck SG, Hen R, Leonardo ED (2010) 5-HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron 65:40-52.CrossRef Medline
53. Scott MM, Wylie CJ, Lerch JK, Murphy R, Lobur K, Herlitze S, Jiang W, Conlon RA, Strowbridge BW, Deneris ES (2005) A genetic approach to access serotonin neurons for in vivo and in vitro studies. Proc Natl Acad Sci U S A 102:16472-16477.CrossRef Medline
54. Shutoh F, Ina A, Yoshida S, Konno J, Hisano S (2008) Two distinct subtypes of serotonergic fibers classified by co-expression with vesicular glutamate transporter 3 in rat forebrain. Neurosci Lett 432:132-136.CrossRef Medline
55. Sodhi MS, Sanders-Bush E (2004) Serotonin and brain development. International review of neurobiology 59:111-174.CrossRef Medline
56. Spitzer NC (2006) Electrical activity in early neuronal development. Nature 444:707-712.CrossRef Medline
57. Srivastava DP, Woolfrey KM, Jones KA, Anderson CT, Smith KR, Russell TA, Lee H, Yasvoina MV, Wokosin DL, Ozdinler PH, Shepherd GM, Penzes P (2012) An autism-associated variant of Epac2 reveals a role for Ras/ Epac2 signaling in controlling basal dendrite maintenance in mice. PLoS Biol 10:e1001350.CrossRef Medline
58. Talley EM, Sirois JE, Lei Q, Bayliss DA (2003) Two-pore-Domain (KCNK) potassium channels: dynamic roles in neuronal function. Neuroscientist 9:46-56.CrossRef Medline
59. van der Velden L, van Hooft JA, Chameau P (2012) Altered dendritic complexity affects firing properties of cortical layer 2/3 pyramidal neurons in mice lacking the 5-HT3A receptor. J Neurophysiol 108:1521-1528.CrossRef Medline
60. Vandermaelen CP, Aghajanian GK (1983) Electrophysiological and pharmacological characterization of serotonergic dorsal raphe neurons recorded extracellularly and intracellularly in rat brain slices. Brain Res 289:109-119.CrossRef Medline
61. Vitalis T, Parnavelas JG (2003) The role of serotonin in early cortical development. Dev Neurosci 25:245-256.CrossRef Medline
62. Wallace JA, Lauder JM (1983) Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res Bull 10:459-479.CrossRef Medline
63. + conductance. J Neurosci 22:1256-1265. Medline