Brain Structure and Function

, Volume 217, Issue 2, pp 435–446 | Cite as

Sensory deprivation differentially impacts the dendritic development of pyramidal versus non-pyramidal neurons in layer 6 of mouse barrel cortex

Original Article

Abstract

Early postnatal sensory experience can have profound impacts on the structure and function of cortical circuits affecting behavior. Using the mouse whisker-to-barrel system we chronically deprived animals of normal sensory experience by bilaterally trimming their whiskers every other day from birth for the first postnatal month. Brain tissue was then processed for Golgi staining and neurons in layer 6 of barrel cortex were reconstructed in three dimensions. Dendritic and somatic parameters were compared between sensory-deprived and normal sensory experience groups. Results demonstrated that layer 6 non-pyramidal neurons in the chronically deprived group showed an expansion of their dendritic arbors. The pyramidal cells responded to sensory deprivation with increased somatic size and basilar dendritic arborization but overall decreased apical dendritic parameters. In sum, sensory deprivation impacted on the neuronal architecture of pyramidal and non-pyramidal neurons in layer 6, which may provide a substrate for observed physiological and behavioral changes resulting from whisker trimming.

Keywords

Neocortex layer 6 Golgi Neuronal morphology Barrel cortex Sensory deprivation Dendrites 

References

  1. Andolina IM, Jones HE, Wang W, Sillito AM (2007) Corticothalamic feedback enhances stimulus response precision in the visual system. PNAS 104(5):1685–1690PubMedCrossRefGoogle Scholar
  2. Bestman J, Santos da Silva J, Cline HT (2008) Dendrite development. In: Stuart G, Spruston N, Häusser M (eds) Dendrites. Oxford University Press, NY, pp 35–67Google Scholar
  3. Briner A, De Roo M, Dayer A, Muller D, Kiss JZ, Vutskits L (2010) Bilateral whisker trimming during early postnatal life impairs dendritic spine development in the mouse somatosensory barrel cortex. J Comp Neurol 518(10):1711–1723PubMedCrossRefGoogle Scholar
  4. Bruno RM, Hahn TT, Wallace DJ, de Kock CP, Sakmann B (2009) Sensory experience alters specific branches of individual corticocortical axons during development. J Neurosci 29(10):3172–3181PubMedCrossRefGoogle Scholar
  5. Buonomano DV, Merzenich MM (1998) Cortical plasticity: from synapses to maps. Ann Rev Neurosci 21:149–186PubMedCrossRefGoogle Scholar
  6. Carvell GE, Simons DJ (1996) Abnormal tactile experience early in life disrupts active touch. J Neurosci 16(8):2750–2757PubMedGoogle Scholar
  7. Chen CC, Abrams S, Pinhas A, Brumberg JC (2009) Morphological heterogeneity of layer VI neurons in mouse barrel cortex. J Comp Neurol 512(6):726–746PubMedCrossRefGoogle Scholar
  8. Cline H, Haas K (2008) The regulation of dendritic arbor development and plasticity by glutamatergic synaptic input: a review of the synaptotrophic hypothesis. J Physiol 586(6):1509–1517PubMedCrossRefGoogle Scholar
  9. Crick FC, Koch C (2005) What is the function of the claustrum? Philo Trans Roy Soc Lond Ser B: Biol Sci 360(1458):1271–1279CrossRefGoogle Scholar
  10. Datwani A, Iwasato T, Itohara S, Erzurumlu RS (2002) NMDA receptor-dependent pattern transfer from afferents to postsynaptic cells and dentritic differentiation in the barrel cortex. Mol Cell Neurosci 21(3):477–492Google Scholar
  11. de Lorente Nó R (1949) Cerebral cortex: architecture, intracortical connections, motor projections. Physiology of the nervous system. Oxford University Press, New York, pp 288–330Google Scholar
  12. Denton DA, McKinley MJ, Farrell M, Egan GF (2009) The role of primordial emotions in the evolutionary origin of consciousness. Conscious Cogn 18(2):500–514PubMedCrossRefGoogle Scholar
  13. Feldman DE, Brecht M (2005) Map plasticity in somatosensory cortex. Science 310(5749):810–815PubMedCrossRefGoogle Scholar
  14. Fox K, Wong RO (2005) A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48(3):465–477PubMedCrossRefGoogle Scholar
  15. Garrett JE, Wellman CL (2009) Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 162(1):195–207PubMedCrossRefGoogle Scholar
  16. Hardingham N, Wright N, Dachtler J, Fox K (2008) Sensory deprivation unmasks a PKA-dependent synaptic plasticity mechanism that operates in parallel with CaMKII. Neuron 60(5):861–874PubMedCrossRefGoogle Scholar
  17. Harris RM, Woolsey TA (1981) Dendritic plasticity in mouse barrel cortex following postnatal vibrissa follicle damage. J Comp Neurol 196(3):357–376PubMedCrossRefGoogle Scholar
  18. Hickmott PW, Steen PA (2005) Large-scale changes in dendritic structure during reorganization of adult somatosensory cortex. Nature Neurosci 8(2):140–142PubMedCrossRefGoogle Scholar
  19. Jiao Y, Zhang C, Yanagawa Y, Sun QQ (2006) Major effects of sensory experiences on the neocortical inhibitory circuits. J Neurosci 26(34):8691–8701PubMedCrossRefGoogle Scholar
  20. Katz LC (1987) Local circuitry of identified projection neurons in cat visual cortex brain slices. J Neurosci 7(4):1223–1249PubMedGoogle Scholar
  21. Komendantov AO, Ascoli GA (2009) Dendritic excitability and neuronal morphology as determinants of synaptic efficacy. J Neurophysiol 101(4):1847–1866PubMedCrossRefGoogle Scholar
  22. Kossel A, Löwel S, Bolz J (1995) Relationships between dendritic fields and functional architecture in striate cortex of normal and visually deprived cats. J Neurosci 15(5 Pt 2):3913–3926PubMedGoogle Scholar
  23. Krichmar JL, Nasuto SJ, Scorcioni R, Washington SD, Ascoli GA (2002) Effects of dendritic morphology on CA3 pyramidal cell electrophysiology: a simulation study. Brain Res 941(1–2):11–28PubMedCrossRefGoogle Scholar
  24. Lee LJ, Chen WJ, Chuang YW, Wang YC (2009) Neonatal whisker trimming causes long-lasting changes in structure and function of the somatosensory system. Exp Neurol 219(2):524–532PubMedCrossRefGoogle Scholar
  25. 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(6):4380–4385PubMedCrossRefGoogle Scholar
  26. López-Aranda MF, López-Téllez JF, Navarro-Lobato I, Masmudi-Martín M, Gutiérrez A, Khan ZU (2009) Role of layer 6 of V2 visual cortex in object-recognition memory. Science 325(5936):87–89PubMedCrossRefGoogle Scholar
  27. Lübke J, Albus K (1989) The postnatal development of layer VI pyramidal neurons in the cat’s striate cortex, as visualized by intracellular Lucifer yellow injections in aldehyde-fixed tissue. Brain Res: Dev Brain Res 45(1):29–38CrossRefGoogle Scholar
  28. Lund JS, Wu CQ (1997) Local circuit neurons of macaque monkey striate cortex: IV. Neurons of laminae 1-3A. J Comp Neurol 384(1):109–126PubMedCrossRefGoogle Scholar
  29. Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382(6589):363–366PubMedCrossRefGoogle Scholar
  30. Maravall M, Koh IY, Lindquist WB, Svoboda K (2004) Experience-dependent 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(6):655–664PubMedCrossRefGoogle Scholar
  31. Marik SA, Yamahachi H, McManus JN, Szabo G, Gilbert CD (2010) Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. Plos Biology 8(6):e1000395PubMedCrossRefGoogle Scholar
  32. McRae PA, Rocco MM, Kelly G, Brumberg JC, Matthews RT (2007) Sensory deprivation alters aggrecan and perineuronal net expression in the mouse barrel cortex. J Neurosci 27(20):5405–5413Google Scholar
  33. Mendizabal-Zubiaga JL, Reblet C, Bueno-Lopez JL (2007) The underside of the cerebral cortex: layer V/VI spiny inverted neurons. J Anat 211(2):223–236PubMedCrossRefGoogle Scholar
  34. Neal JW, Winfield DA, Powell TP (1985) The effect of visual deprivation upon the basal dendrites of Meynert cells in the striate cortex of the monkey. Philos Trans Roy Soc Lond, Ser B: Biol Sci 225(1241):411–423CrossRefGoogle Scholar
  35. Oray S, Majewska A, Sur M (2004) Dendritic spine dynamics are regulated by monocular deprivation and extracellular matrix degradation. Neuron 44(6):1021–1030PubMedCrossRefGoogle Scholar
  36. Pasternak JF, Woolsey TA (1975) On the “selectivity” of the Golgi-Cox method. J Comp Neurol 160(3):307–312PubMedCrossRefGoogle Scholar
  37. Petersen CCH (2007) The functional organization of the barrel cortex. Neuron 56:339–354Google Scholar
  38. Popescu MV, Ebner FF (2010) Neonatal sensory deprivation and the development of cortical function: Unilateral and bilateral sensory deprivation result in different functional outcomes. J Neurophysiol 104(1):98–107Google Scholar
  39. Prieto JJ, Winer JA (1999) Layer VI in cat primary auditory cortex: Golgi study and sublaminar origins of projection neurons. J Comp Neurol 404:332–358PubMedCrossRefGoogle Scholar
  40. Rakic P (2009) Evolution of the neocortex: a perspective from developmental biology. Nature Rev Neurosci 10(10):724–735CrossRefGoogle Scholar
  41. Rall W, Rinzel J (1973) Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. Biophysical J 13(7):648–687CrossRefGoogle Scholar
  42. Ramos RL, Tam DM, Brumberg JC (2008) Physiology and morphology of callosal projection neurons in mouse. Neuroscience 153(3):654–663PubMedCrossRefGoogle Scholar
  43. Rocco MM, Brumberg JC (2007) The sensorimotor slice. J Neurosci Methods 162(1–2):139–147PubMedCrossRefGoogle Scholar
  44. Samsonovich AV, Ascoli GA (2006) Morphological homeostasis in cortical dendrites. PNAS 103(5):1569–1574PubMedCrossRefGoogle Scholar
  45. Schaefer AT, Larkum ME, Sakmann B, Roth A (2003) Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. J Neurophysiol 89(6):3143–3154PubMedCrossRefGoogle Scholar
  46. Sherman SM, Guillery RW (2002) The role of the thalamus in the flow of information to the cortex. Philos Trans Roy Soc Lond Ser B: Biol Sci 357(1428):1695–1708CrossRefGoogle Scholar
  47. Sholl DA (1956) The organization of the cerebral cortex. John Wiley Press, New YorkGoogle Scholar
  48. Simons DJ, Land PW (1987) Early experience of tactile stimulation influences organization of somatic sensory cortex. Nature 326(6114):694–697PubMedCrossRefGoogle Scholar
  49. Sun QQ (2009) Experience-dependent intrinsic plasticity in interneurons of barrel cortex layer IV. J Neurophysiol 102(5):2955–2973PubMedCrossRefGoogle Scholar
  50. Sur M, Rubenstein JLR (2005) Patterning and plasticity of the cerebral cortex. Science 310(5749):805–810PubMedCrossRefGoogle Scholar
  51. Tailby C, Wright LL, Metha AB, Calford MB (2005) Activity-dependent maintenance and growth of dendrites in adult cortex. PNAS 102(12):4631–4636PubMedCrossRefGoogle Scholar
  52. Takasaki C, Okada R, Mitani A, Fukaya M, Yamasaki M, Fujihara Y, Shirakawa T, Tanaka K, Watanabe M (2008) Glutamate transporters regulate lesion-induced plasticity in the developing somatosensory cortex. J Neurosci 28(19):4995–5006PubMedCrossRefGoogle Scholar
  53. Thomson AM (2010) Neocortical layer 6, a review. Frontiers Neuroanat 4:1–14Google Scholar
  54. Tian N, Copenhagen DR (2003) Visual stimulation is required for refinement of ON and OFF pathways in postnatal retina. Neuron 39(1):85–96PubMedCrossRefGoogle Scholar
  55. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, Welker E, Svoboda K (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420(6917):788–794PubMedCrossRefGoogle Scholar
  56. Tran TS, Rubio ME, Clem RL, Johnson D, Case L, Tessier-Lavigne M, Huganir RL, Ginty DD, Kolodkin AL (2009) Secreted semaphorins control spine distribution and morphogenesis in the postnatal CNS. Nature 462(7276):1065–1069PubMedCrossRefGoogle Scholar
  57. Valverde F (1998) Golgi atlas of the postnatal mouse. Springer-Verlag, AustriaGoogle Scholar
  58. Van der Loos H, Woolsey TA (1973) Somatosensory cortex: structural alterations following early injury to sense organs. Science 179(71):395–398PubMedCrossRefGoogle Scholar
  59. van Ooyen A, Duijnhouwer J, Remme MW, van Pelt J (2002) The effect of dendritic topology on firing patterns in model neurons. Network 13(3):311–325PubMedCrossRefGoogle Scholar
  60. White EL (1978) Identified neurons in mouse Sml cortex which are postsynaptic to thalamocortical axon terminals: a combined Golgi-electron microscopic and degeneration study. J Comp Neurol 181(3):627–661PubMedCrossRefGoogle Scholar
  61. Woolsey TA, Dierker ML, Wann DF (1975) Mouse SmI cortex: qualitative and quantitative classification of Golgi-impregnated barrel neurons. PNAS 72(6):2165–2169PubMedCrossRefGoogle Scholar
  62. Zuo Y, Yang G, Kwon E, Gan WB (2005) Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex. Nature 436(7048):261–265PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Chia-Chien Chen
    • 1
  • Danny Tam
    • 1
  • Joshua C. Brumberg
    • 1
    • 2
  1. 1.Neuropsychology Doctoral SubprogramThe Graduate CenterNew YorkUSA
  2. 2.Department of PsychologyQueens CollegeFlushingUSA

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