Postnatal Dendritic Growth and Spinogenesis of Layer-V Pyramidal Cells Differ between Visual, Inferotemporal, and Prefrontal Cortex of the Macaque Monkey.

Tomofumi Oga, Guy N Elston, Ichiro Fujita
Author Information
  1. Tomofumi Oga: Laboratory for Cognitive Neuroscience, Graduate School of Frontier Biosciences, Osaka University Suita, Japan.
  2. Guy N Elston: Centre for Cognitive Neuroscience Sunshine Coast, QLD, Australia.
  3. Ichiro Fujita: Laboratory for Cognitive Neuroscience, Graduate School of Frontier Biosciences, Osaka UniversitySuita, Japan; Center for Information and Neural Networks, National Institute of Information and Communications Technology and Osaka UniversitySuita, Japan.

Abstract

Pyramidal cells in the primate cerebral cortex, particularly those in layer III, exhibit regional variation in both the time course and magnitude of postnatal growth and pruning of dendrites and spines. Less is known about the development of pyramidal cell dendrites and spines in other cortical layers. Here we studied dendritic morphology of layer-V pyramidal cells in primary visual cortex (V1, sensory), cytoarchitectonic area TE in the inferotemporal cortex (sensory association), and granular prefrontal cortex (Walker's area 12, executive) of macaque monkeys at the ages of 2 days, 3 weeks, 3.5 months, and 4.5 years. We found that changes in the basal dendritic field area of pyramidal cells were different across the three areas. In V1, field size became smaller over time (largest at 2 days, half that size at 4.5 years), in TE it did not change, and in area 12 it became larger over time (smallest at 2 days, 1.5 times greater at 4.5 years). In V1 and TE, the total number of branch points in the basal dendritic trees was similar between 2 days and 4.5 years, while in area 12 the number was greater in the adult monkeys than in the younger ones. Spine density peaked at 3 weeks and declined in all areas by adulthood, with V1 exhibiting a faster decline than area TE or area 12. Estimates of the total number of spines in the dendritic trees revealed that following the onset of visual experience, pyramidal cells in V1 lose more spines than they grow, whereas those in TE and area 12 grow more spines than they lose during the same period. These data provide further evidence that the process of synaptic refinement in cortical pyramidal cells differs not only according to time, but also location within the cortex. Furthermore, given the previous finding that layer-III pyramidal cells in all these areas exhibit the highest density and total number of spines at 3.5 months, the current results indicate that pyramidal cells in layers III and V develop spines at different rates.

Keywords

References

  1. Cereb Cortex. 1994 Jan-Feb;4(1):78-96 [PMID: 8180493]
  2. Annu Rev Neurosci. 2002;25:127-49 [PMID: 12052906]
  3. J Comp Neurol. 1992 Feb 22;316(4):485-96 [PMID: 1577996]
  4. PLoS One. 2013 Dec 23;8(12):e82954 [PMID: 24376616]
  5. Acta Neuropathol. 1985;65(3-4):281-4 [PMID: 3976364]
  6. Brain Res. 2010 Feb 26;1316:35-42 [PMID: 20043887]
  7. Cereb Cortex. 2001 Jun;11(6):558-71 [PMID: 11375917]
  8. Neuroscience. 2007 Mar 16;145(2):464-9 [PMID: 17240073]
  9. J Anat. 1959 Oct;93:385-402 [PMID: 13819134]
  10. Biochem Biophys Res Commun. 2014 Feb 14;444(3):302-6 [PMID: 24485715]
  11. Cereb Cortex. 2016 Apr 24;:null [PMID: 27114175]
  12. Exp Brain Res. 2001 May;138(2):141-52 [PMID: 11417455]
  13. J Neuropathol Exp Neurol. 1980 Jul;39(4):487-501 [PMID: 7217997]
  14. J Comp Neurol. 1996 May 13;368(4):467-86 [PMID: 8744437]
  15. Elife. 2016 Oct 06;5:null [PMID: 27710767]
  16. Brain Res. 1994 Aug 8;653(1-2):173-82 [PMID: 7982051]
  17. Front Neural Circuits. 2013 Mar 08;7:31 [PMID: 23483808]
  18. Science. 1986 Apr 11;232(4747):232-5 [PMID: 3952506]
  19. Nat Rev Neurosci. 2008 Mar;9(3):206-21 [PMID: 18270515]
  20. Brain Res. 1995 Apr 24;678(1-2):233-43 [PMID: 7542541]
  21. J Comp Neurol. 1991 Aug 22;310(4):429-74 [PMID: 1939732]
  22. J Comp Neurol. 1997 Oct 20;387(2):167-78 [PMID: 9336221]
  23. Biochem Biophys Res Commun. 2014 Feb 14;444(3):307-10 [PMID: 24440696]
  24. Neuroreport. 1999 Jun 23;10(9):1925-9 [PMID: 10501534]
  25. J Neurosci. 1997 May 15;17(10):3684-709 [PMID: 9133391]
  26. Neuron. 2015 Dec 16;88(6):1253-67 [PMID: 26671462]
  27. Nature. 2016 Jul 13;535(7612):367-75 [PMID: 27409810]
  28. Exp Brain Res. 1967;3(4):337-52 [PMID: 6031165]
  29. J Comp Neurol. 1999 Dec 6;415(1):33-51 [PMID: 10540356]
  30. Cereb Cortex. 1996 Nov-Dec;6(6):807-13 [PMID: 8922337]
  31. Cereb Cortex. 1997 Jul-Aug;7(5):432-52 [PMID: 9261573]
  32. Anat Rec A Discov Mol Cell Evol Biol. 2006 Jan;288(1):26-35 [PMID: 16342214]
  33. J Comp Neurol. 1979 Aug 1;186(3):473-89 [PMID: 110852]
  34. J Neurosci. 2000 Dec 15;20(24):RC117 [PMID: 11125016]
  35. J Comp Neurol. 1977 Nov 15;176(2):149-88 [PMID: 410850]
  36. Front Neuroanat. 2011 Feb 10;5:2 [PMID: 21347276]
  37. J Comp Neurol. 1997 Oct 6;386(4):661-80 [PMID: 9378859]
  38. Cereb Cortex. 2010 Jun;20(6):1398-408 [PMID: 19846470]
  39. J Neurosci. 2012 Oct 3;32(40):13644-60 [PMID: 23035077]
  40. Cereb Cortex. 1998 Apr-May;8(3):278-94 [PMID: 9617923]
  41. Cereb Cortex. 2013 Oct;23(10):2429-36 [PMID: 22875862]
  42. Proc Natl Acad Sci U S A. 2011 Aug 9;108(32):13281-6 [PMID: 21788513]
  43. Brain Res. 1978 Jun 23;149(1):1-24 [PMID: 418850]
  44. J Neurosci. 2009 Mar 11;29(10):3271-5 [PMID: 19279264]
  45. Neuroscience. 1995 Jul;67(1):7-22 [PMID: 7477911]
  46. Brain Behav Evol. 2005;66(1):10-21 [PMID: 15821345]
  47. Neuron. 1993 Jun;10(6):991-1006 [PMID: 8318235]
  48. Brain Res. 2006 Aug 23;1106(1):99-110 [PMID: 16854386]
  49. Cereb Cortex. 2008 Apr;18(4):915-29 [PMID: 17652464]
  50. Brain Res. 1984 Mar;315(1):117-24 [PMID: 6722572]
  51. Eur J Neurosci. 2002 Jul;16(2):291-310 [PMID: 12169111]
  52. Front Neural Circuits. 2016 Sep 21;10 :74 [PMID: 27708563]
  53. Front Neuroanat. 2011 May 16;5:29 [PMID: 21647212]
  54. J Anat. 1953 Oct;87(4):387-406 [PMID: 13117757]
  55. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4297-301 [PMID: 2726773]
  56. J Neurosci. 2016 May 25;36(21):5736-47 [PMID: 27225764]
  57. J Cell Sci. 1969 Sep;5(2):509-29 [PMID: 5362339]
  58. Cereb Cortex. 2005 Dec;15(12 ):1887-99 [PMID: 15758199]
  59. J Neurosci. 1993 Jul;13(7):2801-20 [PMID: 8331373]
  60. Front Neuroanat. 2011 Jul 21;5:42 [PMID: 21811440]
  61. Front Neuroanat. 2014 Aug 12;8:78 [PMID: 25161611]

Word Cloud

Created with Highcharts 10.0.0areacellscortexspinespyramidal5TE12V1timedendritic2days34yearsnumbervisualbasalareastotalPyramidalIIIexhibitpostnataldendritesdevelopmentcorticallayerssensorymonkeysweeksmonthsfielddifferentsizebecamegreatertreesdensitylosegrowprimatecerebralparticularlylayerregionalvariationcoursemagnitudegrowthpruningLessknowncellstudiedmorphologylayer-VprimarycytoarchitectonicinferotemporalassociationgranularprefrontalWalker'sexecutivemacaqueagesfoundchangesacrossthreesmallerlargesthalfchangelargersmallest1timesbranchpointssimilaradultyoungeronesSpinepeakeddeclinedadulthoodexhibitingfasterdeclineEstimatesrevealedfollowingonsetexperiencewhereasperioddataprovideevidenceprocesssynapticrefinementdiffersaccordingalsolocationwithinFurthermoregivenpreviousfindinglayer-IIIhighestcurrentresultsindicateVdevelopratesPostnatalDendriticGrowthSpinogenesisLayer-VCellsDifferVisualInferotemporalPrefrontalCortexMacaqueMonkeydendriteinferiortemporalspinesynaptogenesis

Similar Articles

Cited By (19)