Early development of the thalamic inhibitory feedback loop in the primary somatosensory system of the newborn mice

Journal of Neuroscience

Volumn 29, Issue 31, 2009, Pages 9930-9940

  Evrard, Alexis ^a   Ropert, Nicole ^a  

^a INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SEROTONIN 1B RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; ELECTROSTIMULATION; EVOKED CORTICAL RESPONSE; FEEDBACK SYSTEM; MOUSE; NEWBORN; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SOMATOSENSORY CORTEX; SYNAPTIC INHIBITION; THALAMUS NUCLEUS;

AGING; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; RECEPTOR, SEROTONIN, 5-HT1B; RECEPTORS, AMPA; RECEPTORS, GABA-A; RECEPTORS, N-METHYL-D-ASPARTATE; SEROTONIN; SOMATOSENSORY CORTEX; THALAMIC NUCLEI; THALAMUS; TIME FACTORS;

EID: 68549092945     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1671-09.2009     Document Type: Article

References (65)

1. Amadeo A, Ortino B, Frassoni C (2001) Parvalbumin and GABA in the developing somatosensory thalamus of the rat: an immunocytochemical ultrastructural correlation. Anat Embryol (Berl) 203:109-119.
2. Belford GR, Killackey HP (1979a) Vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 183:305-321.
3. Belford GR, Killackey HP (1979b) The development of vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 188:63-74.
4. Belford GR, Killackey HP (1980) The sensitive period in the development of the trigeminal system of the neonatal rat. J Comp Neurol 193:335-350.
5. Bourassa J, Pinault D, Deschênes M (1995) Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. Eur J Neurosci 7:19-30.
6. Carvell GE, Simons DJ (1996) Abnormal tactile experience early in life disrupts active touch. J Neurosci 16:2750-2757.
7. Cases O, Vitalis T, Seif I, De Maeyer E, Sotelo C, Gaspar P (1996) Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of a serotonin excess during the critical period. Neuron 16:297-307.
8. Cox CL, Huguenard JR, Prince DA (1997) Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus. Proc Natl Acad Sci U S A 94:8854-8859.
9. Crair MC (1999) Neuronal activity during development: permissive or instructive? Curr Opin Neurobiol 9:88-93.
10. Crair MC, Malenka RC (1995) A critical period for long-term potentiation at thalamocortical synapses. Nature 375:325-328.
11. Datwani A, Iwasato T, Itohara S, Erzurumlu RS (2002a) Lesion-induced thalamocortical axonal plasticity in the S1 cortex is independent of NMDA receptor function in excitatory cortical neurons. J Neurosci 22:9171-9175.
12. Datwani A, Iwasato T, Itohara S, Erzurumlu RS (2002b) NMDA receptor-dependent pattern transfer from afferents to postsynaptic cells and dendritic differentiation in the barrel cortex. Mol Cell Neurosci 21:477-492.
13. Daw MI, Ashby MC, Isaac JT (2007) Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nat Neurosci 10:453-461.
14. Desîlets-Roy B, Varga C, Lavallée P, Deschênes M (2002) Substrate for cross-talk inhibition between thalamic barreloids. J Neurosci 22:RC218(1-4).
15. Erzurumlu RS, Kind PC (2001) Neural activity: sculptor of "barrels" in the neocortex. Trends Neurosci 24:589-595.
16. Feldman DE, Nicoll RA, Malenka RC, Isaac JT (1998) Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron 21:347-357.
17. Fuentealba P, Steriade M (2005) The reticular nucleus revisited: intrinsic and network properties of a thalamic pacemaker. Prog Neurobiol 75:125-141.
18. Gaspar P, Cases O, Maroteaux L (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4:1002-1012.
19. Gentet LJ, Ulrich D (2003) Strong, reliable and precise synaptic connections between thalamic relay cells and neurones of the nucleus reticularis in juvenile rats. J Physiol 546:801-811.
20. Gentet LJ, Ulrich D (2004) Electrophysiological characterization of synaptic connections between layer VI cortical cells and neurons of the nucleus reticularis thalami in juvenile rats. Eur J Neurosci 19:625-633.
21. Golshani P, Warren RA, Jones EG (1998) Progression of change in NMDA, non-NMDA, and metabotropic glutamate receptor function at the developing corticothalamic synapse. J Neurophysiol 80:143-154.
22. Hannan AJ, Blakemore C, Katsnelson A, Vitalis T, Huber KM, Bear M, Roder J, Kim D, Shin HS, Kind PC (2001) PLC-beta1, activated via mGluRs, mediates activity-dependent differentiation in cerebral cortex. Nat Neurosci 4:282-288.
23. Hartings JA, Temereanca S, Simons DJ (2003) Processing of periodic whisker deflections by neurons in the ventroposterior medial and thalamic reticular nuclei. J Neurophysiol 90:3087-3094.
24. Hensch TK (2005) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6:877-888.
25. Huberman AD, Feller MB, Chapman B (2008) Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 31:479-509.
26. Huntsman MM, Huguenard JR (2000) Nucleus-specific differences in GABA(A)-receptor-mediated inhibition are enhanced during thalamic development. J Neurophysiol 83:350-358.
27. Inan M, Crair MC (2007) Development of cortical maps: perspectives from the barrel cortex. Neuroscientist 13:49-61.
28. Inan M, Lu HC, Albright MJ, She WC, Crair MC (2006) Barrel map development relies on protein kinase A regulatory subunit II beta-mediated cAMP signaling. J Neurosci 26:4338-4349.
29. Iwasato T, Erzurumlu RS, Huerta PT, Chen DF, Sasaoka T, Ulupinar E, Tonegawa S (1997) NMDA receptor-dependent refinement of somatotopic maps. Neuron 19:1201-1210.
30. Iwasato T, Datwani A, Wolf AM, Nishiyama H, Taguchi Y, Tonegawa S, Knöpfel T, Erzurumlu RS, Itohara S (2000) Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex. Nature 406:726-731.
31. Iwasato T, Inan M, Kanki H, Erzurumlu RS, Itohara S, Crair MC (2008) Cortical adenylyl cyclase 1 is required for thalamocortical synapse maturation and aspects of layer IV barrel development. J Neurosci 28:5931-5943.
32. Jacobs EC, Campagnoni C, Kampf K, Reyes SD, Kalra V, Handley V, Xie YY, Hong-Hu Y, Spreur V, Fisher RS, Campagnoni AT (2007) Visualization of corticofugal projections during early cortical development in a tau-GFP-transgenic mouse. Eur J Neurosci 25:17-30.
33. Jeanmonod D, Rice FL, Van der Loos H (1981) Mouse somatosensory cortex: alterations in the barrel field following receptor injury at different early postnatal ages. Neuroscience 6:1503-1535.
34. Khazipov R, Sirota A, Leinekugel X, Holmes GL, Ben-Ari Y, Buzsáki G (2004) Early motor activity drives spindle bursts in the developing somatosensory cortex. Nature 432:758-761.
35. Killackey HP, Belford GR (1979) The formation of afferent patterns in the somatosensory cortex of the neonatal rat. J Comp Neurol 183:285-303.
36. Landers M, Philip Zeigler H (2006) Development of rodent whisking: trigeminal input and central pattern generation. Somatosens Mot Res 23:1-10.
37. Laurent A, Goaillard JM, Cases O, Lebrand C, Gaspar P, Ropert N (2002) Activity-dependent presynaptic effect of serotonin 1B receptors on the somatosensory thalamocortical transmission in neonatal mice. J Neurosci 22:886-900.
38. Leamey CA, Ho SM (1998) Afferent arrival and onset of functional activity in the trigeminothalamic pathway of the rat. Brain Res Dev Brain Res 105:195-207.
39. Lee LJ, Iwasato T, Itohara S, Erzurumlu RS (2005) Exuberant thalamocortical axon arborization in cortex-specific NMDAR1 knockout mice. J Comp Neurol 485:280-292.
40. Lee SH, Land PW, Simons DJ (2007) Layer- and cell-type-specific effects of neonatal whisker-trimming in adult rat barrel cortex. J Neurophysiol 97:4380-4385.
41. Li Y, Erzurumlu RS, Chen C, Jhaveri S, Tonegawa S (1994) Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice. Cell 76:427-437.
42. Liu XB, Bolea S, Golshani P, Jones EG (2001) Differentiation of corticothalamic and collateral thalamocortical synapses on mouse reticular nucleus neurons by EPSP amplitude and AMPA receptor subunit composition. Thalamus Relat Syst 1:15-29.
43. Lu HC, Gonzalez E, Crair MC (2001) Barrel cortex critical period plasticity is independent of changes in NMDA receptor subunit composition. Neuron 32:619-634.
44. Minlebaev M, Ben-Ari Y, Khazipov R (2007) Network mechanisms of spindle-burst oscillations in the neonatal rat barrel cortex in vivo. J Neurophysiol 97:692-700.
45. Minlebaev M, Ben-Ari Y, Khazipov R (2009) NMDAreceptors pattern early activity in the developing barrel cortex in vivo. Cereb Cortex 19:688-696.
46. Mitrofanis J, Baker GE (1993) Development of the thalamic reticular and perireticular nuclei in rats and their relationship to the course of growing corticofugal and corticopetal axons. J Comp Neurol 338:575-587.
47. Peden DR, Petitjean CM, Herd MB, Durakoglugil MS, Rosahl TW, Wafford K, Homanics GE, Belelli D, Fritschy JM, Lambert JJ (2008) Developmental maturation of synaptic and extrasynaptic GABAA receptors in mouse thalamic ventrobasal neurones. J Physiol 586:965-987.
48. Pinault D, Deschênes M (1998) Anatomical evidence for a mechanism of lateral inhibition in the rat thalamus. Eur J Neurosci 10:3462-3469.
49. Rebsam A, Seif I, Gaspar P (2005) Dissociating barrel development and lesion-induced plasticity in the mouse somatosensory cortex. J Neurosci 25:706-710.
50. Rema V, Armstrong-James M, Ebner FF (2003) Experience-dependent plasticity is impaired in adult rat barrel cortex after whiskers are unused in early postnatal life. J Neurosci 23:358-366.
51. Rheims S, Minlebaev M, Ivanov A, Represa A, Khazipov R, Holmes GL, Ben-Ari Y, Zilberter Y (2008) Excitatory GABA in rodent developing neocortex in vitro. J Neurophysiol 100:609-619.
52. Salichon N, Gaspar P, Upton AL, Picaud S, Hanoun N, Hamon M, De Maeyer E, Murphy DL, Mossner R, Lesch KP, Hen R, Seif I (2001) Excessive activation of serotonin (5-HT) 1B receptors disrupts the formation of sensory maps in monoamine oxidase a and 5-ht transporter knock-out mice. J Neurosci 21:884-896.
53. Scanziani M, Gähwiler BH, Charpak S (1998) Target cell-specific modulation of transmitter release at terminals from a single axon. Proc Natl Acad Sci U S A 95:12004-12009.
54. Schofield CM, Huguenard JR (2007) GABA affinity shapes IPSCs in thalamic nuclei. J Neurosci 27:7954-7962.
55. Shoykhet M, Land PW, Simons DJ (2005) Whisker trimming begun at birth or on postnatal day 12 affects excitatory and inhibitory receptive fields of layer IV barrel neurons. J Neurophysiol 94:3987-3995.
56. Simons DJ, Land PW (1987) Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326:694-697.
57. Steriade M (2005) Sleep, epilepsy and thalamic reticular inhibitory neurons. Trends Neurosci 28:317-324.
58. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79.
59. Tyzio R, Ivanov A, Bernard C, Holmes GL, Ben-Ari Y, Khazipov R (2003) Membrane potential of CA3 hippocampal pyramidal cells during postnatal development. J Neurophysiol 90:2964-2972.
60. Van der Loos H, Woolsey TA (1973) Somatosensory cortex: structural alterations following early injury to sense organs. Science 179:395-398.
61. Warren RA, Jones EG (1997) Maturation of neuronal form and function in a mouse thalamo-cortical circuit. J Neurosci 17:277-295.
62. Warren RA, Golshani P, Jones EG (1997) GABA(B)-receptor-mediated inhibition in developing mouse ventral posterior thalamic nucleus. J Neurophysiol 78:550-553.
63. Watson RF, Abdel-Majid RM, Barnett MW, Willis BS, Katsnelson A, Gillingwater TH, McKnight GS, Kind PC, Neumann PE (2006) Involvement of protein kinase A in patterning of the mouse somatosensory cortex. J Neurosci 26:5393-5401.
64. Woolsey TA, Van der Loos H (1970) The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res 17:205-242.
65. - currents in rat thalamic reticular and relay neurons. J Neurophysiol 78:2280-2286.