Bilateral whisker trimming during early postnatal life impairs dendritic spine development in the mouse somatosensory barrel cortex

Journal of Comparative Neurology

Volumn 518, Issue 10, 2010, Pages 1711-1723

  Briner, Adrian ^a,b   De Roo, Mathias ^b   Dayer, Alexandre ^a,b   Muller, Dominique ^b   Kiss, Jozsef Z ^b   Vutskits, Laszlo ^a,b  

^a GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

Confocal microscopy; Neural activity; Sensory perception; Yellow fluorescent protein

Indexed keywords

YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CELL DENSITY; CELL SIZE; CELL STRUCTURE; CELL TYPE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC SPINE; DEVELOPMENTAL STAGE; IN VIVO STUDY; NERVE CELL DIFFERENTIATION; NONHUMAN; PERCEPTION; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SENSORY DEPRIVATION; SENSORY EVALUATION; SOMATOSENSORY CORTEX; SYNAPSE; TRANSGENIC MOUSE; VIBRISSA;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; DENDRITIC SPINES; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; NERVE NET; PYRAMIDAL CELLS; SENSORY DEPRIVATION; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 77952194094     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22297     Document Type: Article

References (58)

1. Araya R, Jiang J, Eisenthal KB, Yuste R. 2006. The spine neck filters membrane potentials. Proc Natl Acad Sci U S A 103: 17961-17966. (Pubitemid 44852268)
2. Arellano JI, Benavides-Piccione R, Defelipe J, Yuste R. 2007. UItrastructure of dendritic spines: correlation between synaptic and spine morphologies. Front Neurosci 1: 131-143.
3. Bourgeois JP, Rakic P. 1993. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci 13: 2801-2820. (Pubitemid 23199209)
4. Bourgeois JP, Goldman-Rakic PS, Rakic P. 1994. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex 4: 78-96. (Pubitemid 24066074)
5. Bourne JN, Harris KM. 2008. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31: 47-67.
6. Broser P, Grinevich V, Osten P, Sakmann B, Wallace DJ. 2008. Critical period plasticity of axonal arbors of layer 2/3 pyramidal neurons in rat somatosensory cortex: layer-specific reduction of projections into deprived cortical columns. Cereb Cortex 18: 1588-1603. (Pubitemid 351882037)
7. Bryan GK, Riesen AH. 1989. Deprived somatosensory-motor experience in stumptailed monkey neocortex: dendritic spine density and dendritic branching of layer IIIB pyramidal cells. J Comp Neurol 286: 208-217.
8. Butz M, Worgotter F, van Ooyen A. 2009. Activity-dependent structural plasticity. Brain Res Rev (E-pub ahead of print).
9. Carvell GE, Simons DJ. 1996. Abnormal tactile experience early in life disrupts active touch. J Neurosci 16: 2750-2857.
10. Chagnac-Amitai Y, Luhmann HJ, Prince DA. 1990. Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J Comp Neurol 296: 598-613. (Pubitemid 20191465)
11. Colonnier M. 1968. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9: 268-287.
12. De Felipe J, Marco P, Fairen A, Jones EG. 1997. Inhibitory synaptogenesis in mouse somatosensory cortex. Cereb Cortex 7: 619-634. (Pubitemid 27467974)
13. Feldman D. 2009. Synaptic mechanisms for plasticity in neocortex. Annu Rev Neurosci (in press).
14. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW, Sanes JR. 2000. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28: 41-51.
15. Fox K, Wong RO. 2005. A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48: 465-477. (Pubitemid 41551951)
16. Galal KM, Bradley PM, Drummond P. 1990. The effect of darkrearing on dendritic development in two regions of the forebrain of the domestic chick. Brain Res Dev Brain Res 53: 135-138. (Pubitemid 20101233)
17. Galvez R, Greenough WT. 2005. Sequence of abnormal dendritic spine development in primary somatosensory cortex of a mouse model of the fragile X mental retardation syndrome. Am J Med Genet A 135: 155-160. (Pubitemid 40769965)
18. Harris KM ,Stevens JK. 1989. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci 9: 2982-2997.
19. Heinen K, Baker RE, Spijker S, Rosahl T, van Pelt J, Brussaard AB. 2003. Impaired dendritic spine maturation in GABAA receptor alpha 1 subunit knock out mice. Neuroscienee 122: 699-705. (Pubitemid 37410291)
20. Hensch TK. 2004. Critical period regulation. Annu Rev Neurosci 27: 549-579.
21. Holtmaat A, Wilbrecht L, Knott GW, Welker E, Svoboda K. 2006. Experience-dependent and cell-type-specific spine growth in the neocortex. Nature 441: 979-983. (Pubitemid 43980351)
22. Huttenlocher PR. 1979. Synaptic density in human frontal cortex-developmental changes and effects of aging. Brain Res 163: 195-205.
23. Huttenlocher PR, Dabholkar AS. 1997. Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387: 167-178. (Pubitemid 27430343)
24. Iriki A, Pavlides C, Keller A, Asanuma H. 1991. Long-term potentiation of thalamic input to the motor cortex induced by coactivation of thalamocortical and corticocortical afferents. J Neurophysiol 65: 1435-1441.
25. Jiao Y, Zhang C, Yanagawa Y, Sun QQ 2006. Major effects of sensory experiences on the neocortical inhibitory circuits. J Neurosci 26: 8691-8701. (Pubitemid 44319404)
26. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science 274: 1133-1138.
27. Konur S, Rabinowitz D, Fenstermaker VL,Yuste R. 2003. Systematic regulation of spine sizes and densities in pyramidal neurons. J Neurobiol 56: 95-112. (Pubitemid 36870448)
28. 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.
29. Lendvai B, Stern EA, Chen B, Svoboda K. 2000. Experiencedependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404: 876-881. (Pubitemid 30230339)
30. Lubke J, Feldmeyer D. 2007. Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct Funct 212: 3-17. (Pubitemid 47036752)
31. Majewska A, Brown E, Ross J, Yuste R. 2000. Mechanisms of calcium decay kinetics in hippocampal spines: role of spine calcium pumps and calcium diffusion through the spine neck in biochemical compartmentalization. J Neurosci 20: 1722-1734. (Pubitemid 30220370)
32. Maravall M, Kohl Y, Lindquist WB, Svoboda K. 2004. Experiencedependent changes in basal dendritic branching of layer 2/3 pyramidal neurons during a critical period for developmental plasticity in rat barrel cortex. Cereb Cortex 14: 655-664. (Pubitemid 38669510)
33. Martinez-Tellez RI, Hernandez-Torres E, Gamboa C, Flores G. 2009. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse 63: 794-804.
34. Mataga N, Mizuguchi Y, Hensch TK. 2004. Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44: 1031-1041. (Pubitemid 39643098)
35. Michel AE, Garey LJ. 1984. The development of dendritic spines in the human visual cortex. Hum Neurobiol 3: 223-227. (Pubitemid 15195372)
36. Micheva KD, Beaulieu C. 1995. Neonatal sensory deprivation induces selective changes in the quantitative distribution of GABA-immunoreactive neurons in the rat barrel field cortex. J Comp Neurol 361: 574-584.
37. Nusser Z, Lujan R, Laube G, Roberts JD, Moinar E, Somogyi P. 1998. Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21: 545-559. (Pubitemid 28475506)
38. Pan F, Gan WB. 2008. Two-photon imaging of dendritic spine development in the mouse cortex. Dev Neurobiol 68: 771-778. (Pubitemid 351620770)
39. PetitT L, LeBoutillier JC, Gregorio A, Libstug H. 1988. The pattern of dendritic development in the cerebral cortex of the rat. Brain Res 469: 209-219.
40. Rakic P, Bourgeois JP, Eckenhoff MF, Zecevic N, Goldman-Rakic PS. 1986. Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. Science 232: 232-235. (Pubitemid 16046605)
41. Sakamoto T, Arissian K, Asanuma H. 1989. Functional role of the sensory cortex in learning motor skills in cats. Brain Res 503: 258-264. (Pubitemid 19285517)
42. Schikorski T, Stevens CF. 1999. Quantitative fine-structural analysis of olfactory cortical synapses. Proc Natl Acad Sci U S A 96: 4107-4112. (Pubitemid 29169044)
43. Schikorski T, Stevens CF. 2001. Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4: 391-395. (Pubitemid 32260115)
44. Schubert D, Staiger JF, Cho N, Kotter R, Zilles K, Luhmann HJ. 2001. Layer-specific intracolumnar and transcolumnar functional connectivity of layer V pyramidal cells in rat barrel cortex. J Neurosci 21: 3580-3592. (Pubitemid 32422822)
45. Schubert D, Kotter R, Staiger JF. 2007. Mapping functional connectivity in barrel-related columns reveals layer- and cell typespecific microcircuits. Brain Struct Funct 212: 107-119. (Pubitemid 47394493)
46. 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. (Pubitemid 41691763)
47. Simons DJ, Land PW. 1987. Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326: 694-697.
48. Valverde F. 1967. Apical dendritic spines of the visual cortex and light deprivation in the mouse. Exp Brain Res 3: 337-352.
49. Valverde F. 1971. Rate and extent of recovery from dark rearing in the visual cortex of the mouse. Brain Res 33: 1-11.
50. Vees AM, Micheva KD, Beaulieu C, Descarries L. 1998. Increased number and size of dendritic spines in ipsilateral barrel field cortex following unilateral whisker trimming in postnatal rat. J Comp Neurol 400: 110-124. (Pubitemid 28440757)
51. Welker WI. 1964. Analysis of sniffing of the albino rat. Behavior 22: 223-244.
52. 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.
53. Xu HT, Pan F, Yang G, Gan WB. 2007. Choice of cranial window type for in vivo imaging affects dendritic spine turnover in the cortex. Nat Neurosci 10: 549-551. (Pubitemid 46652440)
54. Yuste R, Majewska A, Holthoff K. 2000. From form to function: calcium compartmentalization in dendritic spines. Nat Neurosci 3: 653-659. (Pubitemid 30437199)
55. Zecevic N, Rakic P. 1991. Synaptogenesis in monkey somatosensory cortex. Cereb Cortex 1: 510-523.
56. Zecevic N, Bourgeois JP, Rakic P. 1989. Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. Brain Res Dev Brain Res 50: 11-32. (Pubitemid 19263894)
57. Zuo Y, Lin A, Chang P, Gan WB. 2005a. Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46: 181-189. (Pubitemid 40545775)
58. Zuo Y, Yang G, Kwon E, Gan WB. 2005b. Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436: 261-265. (Pubitemid 41021277)