Home LiteratureArticle Details
PMID: 12351728 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Refinement of thalamocortical arbors and emergence of barrel domains in the primary somatosensory cortex: a study of normal and monoamine oxidase a knock-out mice.

Rebsam A, Seif I, Gaspar P

Abstract

In the rodent primary somatosensory cortex, the thalamocortical axons (TCAs) are organized into clusters that correspond to functional units in the periphery. Around these axons, neurons in layer IV aggregate as barrels. To understand how this organization emerges, we analyzed TCA development in mice that do not form barrels, the monoamine oxidase A knock-out (MAOA-KO), and in MAOA/5-HT(1B) receptor double-KO mice, which have a restored barrel field. We show that TCAs already attain cortical layer IV on the day of birth. They are uniformly distributed in this layer from postnatal day 0 (P0) to P2 and secondarily coalesce into barrel domains in layer IV, over a 3 d period (P3-P5), with no prepatterning in the deeper layers. In MAOA-KO mice, the uniform distribution of the TC projection is maintained, and no axon clusters emerge. Individual TCA arbors were traced after carbocyanine injections. At P1, TCAs were poorly branched and covered variable tangential widths, encompassing one to two prospective barrels. At P7 the number of TCA branches increased 10-fold in layer IV and became restricted to one barrel. In MAOA-KO mice, there was a 50% reduction of the TCA terminal branches in layer IV, with a 40% increase in their tangential extent. These defects were corrected in the MAOA/5-HT(1B) double knock-out mice, indicating an effect of the presynaptic 5-HT(1B) receptor on axon branching. Our results indicate that the barrel-deficient phenotype of MAOA-KO mice results from an altered refinement of the TCA arbors in their target layer IV, involving branch elaboration and collateral retraction during early postnatal life.

MeSH Terms
Animals Axons/metabolism,ultrastructure Carrier Proteins/biosynthesis Coloring Agents Immunohistochemistry Membrane Glycoproteins/biosynthesis Membrane Transport Proteins Mice Mice, Inbred C3H Mice, Knockout Monoamine Oxidase/biosynthesis,deficiency,genetics Nerve Tissue Proteins Neurons/metabolism,ultrastructure Phenotype Receptor, Serotonin, 5-HT1B Receptors, Serotonin/biosynthesis,deficiency,genetics Serotonin Plasma Membrane Transport Proteins Somatosensory Cortex/cytology,growth & development Thalamus/cytology
Chemicals
Carrier Proteins Coloring Agents Membrane Glycoproteins Membrane Transport Proteins Nerve Tissue Proteins Receptor, Serotonin, 5-HT1B Receptors, Serotonin Serotonin Plasma Membrane Transport Proteins Slc6a4 protein, mouse Monoamine Oxidase
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Rebsam Alexandra
Institut National de la Santé et de la Recherche Médicale U106, Hopital Pitié-Salpêtrière, 75013 Paris, France.
Seif Isabelle
Gaspar Patricia
References (49)
49 references, click to expand
  1. Effects of serotonin on neurite outgrowth from thalamic neurons in vitro.
    Neuroscience. 1999 Mar;90(3):967-74 PMID: 10218796
  2. Signal transduction underlying growth cone guidance by diffusible factors.
    Curr Opin Neurobiol. 1999 Jun;9(3):355-63 PMID: 10395576
  3. Serotonin receptor activation enhances neurite outgrowth of thalamic neurones in rodents.
    Neurosci Lett. 1999 Jul 9;269(2):87-90 PMID: 10430511
  4. Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP)-43 knockout mice.
    Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9397-402 PMID: 10430954
  5. Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses.
    J Neurobiol. 1999 Oct;41(1):92-101 PMID: 10504196
  6. BDNF modulates, but does not mediate, activity-dependent branching and remodeling of optic axon arbors in vivo.
    J Neurosci. 1999 Nov 15;19(22):9996-10003 PMID: 10559407
  7. A mapping label required for normal scale of body representation in the cortex.
    Nat Neurosci. 2000 Apr;3(4):358-65 PMID: 10725925
  8. Regulation of area identity in the mammalian neocortex by Emx2 and Pax6.
    Science. 2000 Apr 14;288(5464):344-9 PMID: 10764649
  9. Cortex-restricted disruption of NMDAR1 impairs neuronal patterns in the barrel cortex.
    Nature. 2000 Aug 17;406(6797):726-31 PMID: 10963597
  10. 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. 2001 Feb 1;21(3):884-96 PMID: 11157075
  11. Thalamocortical arbors extend beyond single cortical barrels: an in vivo intracellular tracing study in rat.
    Exp Brain Res. 2001 Jan;136(2):152-68 PMID: 11206278
  12. PLC-beta1, activated via mGluRs, mediates activity-dependent differentiation in cerebral cortex.
    Nat Neurosci. 2001 Mar;4(3):282-8 PMID: 11224545
  13. Neocortex patterning by the secreted signaling molecule FGF8.
    Science. 2001 Nov 2;294(5544):1071-4 PMID: 11567107
  14. Structure and emergence of specific olfactory glomeruli in the mouse.
    J Neurosci. 2001 Dec 15;21(24):9713-23 PMID: 11739580
  15. Activity-dependent presynaptic effect of serotonin 1B receptors on the somatosensory thalamocortical transmission in neonatal mice.
    J Neurosci. 2002 Feb 1;22(3):886-900 PMID: 11826118
  16. Protracted expression of serotonin transporter and altered thalamocortical projections in the barrelfield of hypothyroid rats.
    Eur J Neurosci. 2001 Dec;14(12):1968-80 PMID: 11860492
  17. Barrel construction in rodent neocortex: role of thalamic afferents versus extracellular matrix molecules.
    Proc Natl Acad Sci U S A. 1991 May 15;88(10):4489-93 PMID: 1709743
  18. Growth of thalamic afferents into mouse barrel cortex.
    Cereb Cortex. 1991 Jul-Aug;1(4):308-35 PMID: 1822738
  19. Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro.
    Neuroscience. 1991;41(2-3):365-79 PMID: 1870696
  20. Development and lesion induced reorganization of the cortical representation of the rat's body surface as revealed by immunocytochemistry for serotonin.
    J Comp Neurol. 1990 Mar 8;293(2):190-207 PMID: 19189711
  21. Potential of visual cortex to develop an array of functional units unique to somatosensory cortex.
    Science. 1991 Jun 14;252(5012):1556-60 PMID: 2047863
  22. Thalamic axons confer a blueprint of the sensory periphery onto the developing rat somatosensory cortex.
    Brain Res Dev Brain Res. 1990 Nov 1;56(2):229-34 PMID: 2261684
  23. Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents.
    J Neurosci. 1987 Nov;7(11):3529-43 PMID: 3316525
  24. Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex.
    J Comp Neurol. 1986 Sep 1;251(1):67-83 PMID: 3760259
  25. Distinguishing topography and somatotopy in the thalamocortical projections of the developing rat.
    Brain Res. 1985 Jan;349(1-2):309-13 PMID: 3986598
  26. Microelectrode delineation of fine grain somatotopic organization of (SmI) cerebral neocortex in albino rat.
    Brain Res. 1971 Mar 5;26(2):259-75 PMID: 4100672
  27. Somatosensory cortex: structural alterations following early injury to sense organs.
    Science. 1973 Jan 26;179(4071):395-8 PMID: 4682966
  28. 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. 1970 Jan 20;17(2):205-42 PMID: 4904874
  29. How do thalamic axons find their way to the cortex?
    Trends Neurosci. 1995 Sep;18(9):389-97 PMID: 7482804
  30. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA.
    Science. 1995 Jun 23;268(5218):1763-6 PMID: 7792602
  31. Topological precision in the thalamic projection to neonatal mouse barrel cortex.
    J Neurosci. 1995 Jan;15(1 Pt 2):549-61 PMID: 7823163
  32. Effects of 5-HT on thalamocortical synaptic transmission in the developing rat.
    J Neurophysiol. 1994 Nov;72(5):2438-50 PMID: 7884470
  33. Early development of the somatotopic map and barrel patterning in rat somatosensory cortex.
    J Comp Neurol. 1994 Aug 1;346(1):80-96 PMID: 7962713
  34. Organized growth of thalamocortical axons from the deep tier of terminations into layer IV of developing mouse barrel cortex.
    J Neurosci. 1993 Dec;13(12):5365-82 PMID: 8254380
  35. Development of the barrels and barrel field in the somatosensory cortex of the mouse.
    J Comp Neurol. 1977 Feb 15;171(4):545-60 PMID: 833357
  36. Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade.
    J Neurosci. 1993 Aug;13(8):3549-73 PMID: 8340819
  37. Altered sensory processing in the somatosensory cortex of the mouse mutant barrelless.
    Science. 1996 Mar 29;271(5257):1864-7 PMID: 8596955
  38. Lack of barrels in the somatosensory cortex of monoamine oxidase A-deficient mice: role of a serotonin excess during the critical period.
    Neuron. 1996 Feb;16(2):297-307 PMID: 8789945
  39. Individual axon morphology and thalamocortical topography in developing rat somatosensory cortex.
    J Comp Neurol. 1996 Mar 25;367(1):36-53 PMID: 8867282
  40. Synaptic activity and the construction of cortical circuits.
    Science. 1996 Nov 15;274(5290):1133-8 PMID: 8895456
  41. Transient uptake and storage of serotonin in developing thalamic neurons.
    Neuron. 1996 Nov;17(5):823-35 PMID: 8938116
  42. Silent synapses during development of thalamocortical inputs.
    Neuron. 1997 Feb;18(2):269-80 PMID: 9052797
  43. Timecourse of development of the wallaby trigeminal pathway: III. Thalamocortical and corticothalamic projections.
    J Comp Neurol. 1997 Oct 20;387(2):194-214 PMID: 9336223
  44. NMDA receptor-dependent refinement of somatotopic maps.
    Neuron. 1997 Dec;19(6):1201-10 PMID: 9427244
  45. Serotonin transporter messenger RNA in the developing rat brain: early expression in serotonergic neurons and transient expression in non-serotonergic neurons.
    Neuroscience. 1998 Apr;83(4):1185-201 PMID: 9502257
  46. Effects of monoamine oxidase A inhibition on barrel formation in the mouse somatosensory cortex: determination of a sensitive developmental period.
    J Comp Neurol. 1998 Apr 6;393(2):169-84 PMID: 9548695
  47. The role of the first postmitotic cortical cells in the development of thalamocortical innervation in the reeler mouse.
    J Neurosci. 1998 Aug 1;18(15):5746-65 PMID: 9671664
  48. Plasma membrane transporters of serotonin, dopamine, and norepinephrine mediate serotonin accumulation in atypical locations in the developing brain of monoamine oxidase A knock-outs.
    J Neurosci. 1998 Sep 1;18(17):6914-27 PMID: 9712661
  49. Transient developmental expression of monoamine transporters in the rodent forebrain.
    J Comp Neurol. 1998 Nov 30;401(4):506-24 PMID: 9826275
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-10-01
Pages
8541-52
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6757778
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]