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Vinck M, Bosman CA. More Gamma More Predictions: Gamma-Synchronization as a Key Mechanism for Efficient Integration of Classical Receptive Field Inputs with Surround Predictions. Front Syst Neurosci. 2016;10:35doi: 10.3389/fnsys.2016.00035.
Vinck, M., & Bosman, C. A. (2016). More Gamma More Predictions: Gamma-Synchronization as a Key Mechanism for Efficient Integration of Classical Receptive Field Inputs with Surround Predictions. Frontiers in systems neuroscience, 1035. https://doi.org/10.3389/fnsys.2016.00035
Vinck, Martin, and Bosman, Conrado A. "More Gamma More Predictions: Gamma-Synchronization as a Key Mechanism for Efficient Integration of Classical Receptive Field Inputs with Surround Predictions." Frontiers in systems neuroscience vol. 10 (2016): 35. doi: https://doi.org/10.3389/fnsys.2016.00035
Vinck M, Bosman CA. More Gamma More Predictions: Gamma-Synchronization as a Key Mechanism for Efficient Integration of Classical Receptive Field Inputs with Surround Predictions. Front Syst Neurosci. 2016 Apr 25;10:35. doi: 10.3389/fnsys.2016.00035. eCollection 2016. PMID: 27199684; PMCID: PMC4842768.
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Front Syst Neurosci. 2016 Apr 25;10:35. doi: 10.3389/fnsys.2016.00035. eCollection 2016.

More Gamma More Predictions: Gamma-Synchronization as a Key Mechanism for Efficient Integration of Classical Receptive Field Inputs with Surround Predictions.

Frontiers in systems neuroscience

Martin Vinck, Conrado A Bosman

Affiliations

  1. School of Medicine, Yale University New Haven, CT, USA.
  2. Cognitive and Systems Neuroscience Group, Swammerdam Institute, Center for Neuroscience, University of AmsterdamAmsterdam, Netherlands; Facultad de Ciencias de la Salud, Universidad Autónoma de ChileSantiago, Chile.

PMID: 27199684 PMCID: PMC4842768 DOI: 10.3389/fnsys.2016.00035

Abstract

During visual stimulation, neurons in visual cortex often exhibit rhythmic and synchronous firing in the gamma-frequency (30-90 Hz) band. Whether this phenomenon plays a functional role during visual processing is not fully clear and remains heavily debated. In this article, we explore the function of gamma-synchronization in the context of predictive and efficient coding theories. These theories hold that sensory neurons utilize the statistical regularities in the natural world in order to improve the efficiency of the neural code, and to optimize the inference of the stimulus causes of the sensory data. In visual cortex, this relies on the integration of classical receptive field (CRF) data with predictions from the surround. Here we outline two main hypotheses about gamma-synchronization in visual cortex. First, we hypothesize that the precision of gamma-synchronization reflects the extent to which CRF data can be accurately predicted by the surround. Second, we hypothesize that different cortical columns synchronize to the extent that they accurately predict each other's CRF visual input. We argue that these two hypotheses can account for a large number of empirical observations made on the stimulus dependencies of gamma-synchronization. Furthermore, we show that they are consistent with the known laminar dependencies of gamma-synchronization and the spatial profile of intercolumnar gamma-synchronization, as well as the dependence of gamma-synchronization on experience and development. Based on our two main hypotheses, we outline two additional hypotheses. First, we hypothesize that the precision of gamma-synchronization shows, in general, a negative dependence on RF size. In support, we review evidence showing that gamma-synchronization decreases in strength along the visual hierarchy, and tends to be more prominent in species with small V1 RFs. Second, we hypothesize that gamma-synchronized network dynamics facilitate the emergence of spiking output that is particularly information-rich and sparse.

Keywords: V1; communication through coherence; efficient coding; gamma oscilations; gamma synchrony; laminar organization; predictive coding; surround suppression

References

  1. Neuron. 2010 Feb 25;65(4):472-9 - PubMed
  2. J Neurosci. 2012 Nov 14;32(46):16256-64 - PubMed
  3. Neuron. 2005 Apr 21;46(2):333-46 - PubMed
  4. J Neurosci. 2013 Jan 30;33(5):1773-89 - PubMed
  5. Front Hum Neurosci. 2010 Nov 02;4:196 - PubMed
  6. PLoS Biol. 2015 Sep 22;13(9):e1002257 - PubMed
  7. Nat Neurosci. 2009 Nov;12(11):1444-9 - PubMed
  8. J Comp Neurol. 1983 May 20;216(3):303-18 - PubMed
  9. Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14332-41 - PubMed
  10. Proc Natl Acad Sci U S A. 1989 Feb;86(3):1071-5 - PubMed
  11. Nat Rev Neurosci. 2001 Apr;2(4):229-39 - PubMed
  12. Cereb Cortex. 2015 Apr;25(4):918-26 - PubMed
  13. Cereb Cortex. 2014 Jan;24(1):119-42 - PubMed
  14. Science. 2001 Feb 23;291(5508):1560-3 - PubMed
  15. Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1867-72 - PubMed
  16. J Neurosci. 1983 May;3(5):1116-33 - PubMed
  17. Psychol Rev. 1974 Nov;81(6):521-35 - PubMed
  18. J Neurosci. 2009 Sep 9;29(36):11283-93 - PubMed
  19. Neuron. 2014 May 7;82(3):682-94 - PubMed
  20. Neural Comput. 1995 May;7(3):469-85 - PubMed
  21. Eur J Neurosci. 2014 Jun;39(11):1982-99 - PubMed
  22. Eur J Neurosci. 2008 Oct;28(7):1286-300 - PubMed
  23. Neuron. 2014 Oct 22;84(2):355-62 - PubMed
  24. Annu Rev Neurosci. 1995;18:555-86 - PubMed
  25. J Neurosci. 1990 Apr;10(4):1134-53 - PubMed
  26. Nat Neurosci. 2013 Dec;16(12):1857-63 - PubMed
  27. Nat Rev Neurosci. 2007 Jan;8(1):45-56 - PubMed
  28. Neuron. 2015 May 6;86(3):740-54 - PubMed
  29. Trends Neurosci. 2007 Jul;30(7):309-16 - PubMed
  30. Neuron. 2015 Sep 23;87(6):1143-61 - PubMed
  31. J Neurophysiol. 1994 Dec;72(6):2743-53 - PubMed
  32. J Vis. 2006 Oct 09;6(11):1148-58 - PubMed
  33. Eur J Neurosci. 1990;2(7):607-619 - PubMed
  34. Proc Natl Acad Sci U S A. 2012 Mar 13;109(11):4302-7 - PubMed
  35. Nat Neurosci. 2006 May;9(5):690-6 - PubMed
  36. Nature. 2009 Jun 4;459(7247):663-7 - PubMed
  37. J Neurophysiol. 2005 Jul;94(1):799-812 - PubMed
  38. Neuron. 2003 Mar 6;37(5):853-63 - PubMed
  39. Vis Neurosci. 2001 Jul-Aug;18(4):527-40 - PubMed
  40. Eur J Neurosci. 2013 Sep;38(6):2864-83 - PubMed
  41. Trends Cogn Sci. 2005 Oct;9(10):474-80 - PubMed
  42. Biol Cybern. 2010 Aug;103(2):151-65 - PubMed
  43. Prog Brain Res. 2002;136:373-88 - PubMed
  44. Annu Rev Neurosci. 2012;35:203-25 - PubMed
  45. Annu Rev Neurosci. 1995;18:193-222 - PubMed
  46. Nature. 2013 Jan 3;493(7430):97-100 - PubMed
  47. Nat Neurosci. 2015 Nov;18(11):1648-55 - PubMed
  48. J Neurosci. 1999 Mar 1;19(5):1736-53 - PubMed
  49. Neuron. 2012 Sep 6;75(5):875-88 - PubMed
  50. Neuron. 2009 Sep 24;63(6):727-32 - PubMed
  51. Nature. 1995 Feb 16;373(6515):612-5 - PubMed
  52. Neuron. 2016 Jan 20;89(2):384-97 - PubMed
  53. Isr J Med Sci. 1982 Jan;18(1):83-92 - PubMed
  54. Nat Neurosci. 2012 Feb 26;15(4):607-12 - PubMed
  55. Biosystems. 1998 Sep-Dec;48(1-3):57-65 - PubMed
  56. J Neurosci. 2002 Oct 1;22(19):8633-46 - PubMed
  57. J Neurosci. 2006 Feb 8;26(6):1673-6 - PubMed
  58. Science. 2005 Apr 22;308(5721):529-34 - PubMed
  59. Neuron. 2015 Jan 21;85(2):390-401 - PubMed
  60. Proc Natl Acad Sci U S A. 2000 Jul 5;97(14):8110-5 - PubMed
  61. Neuron. 2015 Jul 1;87(1):179-92 - PubMed
  62. J Neurosci. 1997 May 1;17(9):3239-53 - PubMed
  63. J Neurosci. 2011 Jun 8;31(23):8570-84 - PubMed
  64. Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):6112-7 - PubMed
  65. Proc Natl Acad Sci U S A. 2016 Feb 2;113(5):E606-15 - PubMed
  66. Neuron. 2010 Jan 14;65(1):107-21 - PubMed
  67. Front Comput Neurosci. 2011 Jun 02;5:22 - PubMed
  68. J Neurophysiol. 2003 Mar;89(3):1541-66 - PubMed
  69. Curr Opin Neurobiol. 2007 Aug;17(4):408-16 - PubMed
  70. Nat Neurosci. 2013 Jul;16(7):974-81 - PubMed
  71. Nature. 1989 Mar 23;338(6213):334-7 - PubMed
  72. Neural Comput. 2008 Feb;20(2):383-414 - PubMed
  73. Hippocampus. 1993 Jul;3(3):317-30 - PubMed
  74. Cereb Cortex. 2000 Nov;10(11):1117-31 - PubMed
  75. Nature. 1996 Jun 13;381(6583):607-9 - PubMed
  76. Neuron. 2014 Oct 22;84(2):470-85 - PubMed
  77. J Neurosci. 2012 Nov 14;32(46):16172-80 - PubMed
  78. PLoS Comput Biol. 2012;8(11):e1002760 - PubMed
  79. Neuron. 2012 Nov 21;76(4):695-711 - PubMed
  80. Neuron. 2015 Aug 19;87(4):827-39 - PubMed
  81. Proc Natl Acad Sci U S A. 2011 Jun 28;108(26):10720-5 - PubMed
  82. J Neurophysiol. 2003 Sep;90(3):1910-20 - PubMed
  83. Dev Neurobiol. 2011 Jan 1;71(1):92-106 - PubMed
  84. Exp Brain Res. 1986;63(2):443-8 - PubMed
  85. Proc Natl Acad Sci U S A. 2014 May 6;111(18):6780-5 - PubMed
  86. Science. 1992 Jan 10;255(5041):209-12 - PubMed
  87. Vis Neurosci. 1990 Jan;4(1):11-28 - PubMed
  88. Neuron. 2013 May 8;78(3):523-36 - PubMed
  89. Neuron. 2003 Feb 6;37(3):513-23 - PubMed
  90. J Neurosci. 1999 May 15;19(10):3992-4010 - PubMed
  91. PLoS Biol. 2013;11(2):e1001477 - PubMed
  92. J Neurosci. 2005 Jun 1;25(22):5339-50 - PubMed
  93. Nat Rev Neurosci. 2011 Feb;12(2):105-18 - PubMed
  94. J Neurophysiol. 2008 Mar;99(3):1394-407 - PubMed
  95. Network. 2005 Jun-Sep;16(2-3):139-49 - PubMed
  96. Eur J Neurosci. 2008 Aug;28(3):447-59 - PubMed
  97. J Neurosci. 2008 Apr 2;28(14):3759-68 - PubMed
  98. Trends Cogn Sci. 2014 Oct;18(10):507-9 - PubMed
  99. J Comput Neurosci. 2012 Aug;33(1):53-75 - PubMed
  100. Neuron. 1999 Sep;24(1):67-77, 111-25 - PubMed
  101. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):745-9 - PubMed
  102. Proc Natl Acad Sci U S A. 2008 Nov 18;105(46):18023-8 - PubMed
  103. Science. 2000 Feb 18;287(5456):1273-6 - PubMed
  104. Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3263-8 - PubMed
  105. Nat Neurosci. 2002 Jun;5(6):598-604 - PubMed
  106. J Neurosci. 2010 Mar 3;30(9):3531-43 - PubMed
  107. J Neurophysiol. 1996 Jun;75(6):2467-85 - PubMed
  108. J Neurosci Methods. 2013 Feb 15;213(1):43-62 - PubMed
  109. J Vis. 2008 Dec 18;8(14):21.1-18 - PubMed
  110. Nat Neurosci. 2015 Apr;18(4):484-9 - PubMed
  111. J Neurosci. 2008 Jul 23;28(30):7520-36 - PubMed
  112. Annu Rev Neurosci. 2009;32:209-24 - PubMed
  113. Front Neural Circuits. 2012 Jul 05;6:43 - PubMed
  114. Neural Comput. 2006 Sep;18(9):2256-81 - PubMed
  115. Science. 2007 Jun 15;316(5831):1609-12 - PubMed
  116. Nature. 2009 Jun 4;459(7247):698-702 - PubMed
  117. J Neurosci. 2008 Aug 13;28(33):8273-84 - PubMed
  118. PLoS Comput Biol. 2015 Feb 13;11(2):e1004072 - PubMed
  119. Front Syst Neurosci. 2016 Jan 22;9:187 - PubMed
  120. Neuron. 1999 Sep;24(1):49-65, 111-25 - PubMed
  121. Trends Cogn Sci. 2015 Feb;19(2):78-85 - PubMed
  122. Nature. 2013 Apr 4;496(7443):96-100 - PubMed
  123. Nat Rev Neurosci. 2011 Aug 10;12(9):509-23 - PubMed
  124. Eur J Neurosci. 1993 May 1;5(5):501-8 - PubMed
  125. J Neurosci. 2004 Sep 29;24(39):8441-53 - PubMed
  126. Neuron. 1999 Sep;24(1):95-104, 111-25 - PubMed
  127. Cereb Cortex. 2015 Sep;25(9):2951-9 - PubMed
  128. Nat Neurosci. 2004 Sep;7(9):982-91 - PubMed
  129. Neuroimage. 2013 Sep;78:439-47 - PubMed
  130. Neuroscience. 1992;46(2):275-86 - PubMed
  131. Neuron. 2005 Aug 4;47(3):423-35 - PubMed
  132. Neuron. 2013 Nov 20;80(4):1077-89 - PubMed
  133. Science. 1996 Oct 4;274(5284):109-13 - PubMed
  134. J Neurosci. 2015 Jul 15;35(28):10236-51 - PubMed
  135. Neuron. 1992 Jul;9(1):1-13 - PubMed
  136. Cereb Cortex. 2000 Nov;10(11):1105-16 - PubMed
  137. Cereb Cortex. 2003 Jan;13(1):15-24 - PubMed
  138. Neuron. 1999 Sep;24(1):19-29, 111-25 - PubMed
  139. J Physiol Paris. 2004 Jul-Nov;98(4-6):296-314 - PubMed
  140. J Neurosci. 1998 Aug 15;18(16):6395-410 - PubMed
  141. Proc Natl Acad Sci U S A. 2012 Aug 21;109(34):13871-6 - PubMed
  142. Nat Rev Neurosci. 2001 Aug;2(8):539-50 - PubMed
  143. Biosystems. 1998 Sep-Dec;48(1-3):105-12 - PubMed
  144. J Physiol Paris. 1996;90(3-4):221-2 - PubMed
  145. J Neurosci. 2006 May 3;26(18):4826-34 - PubMed
  146. Trends Neurosci. 1992 Jun;15(6):218-26 - PubMed
  147. Cereb Cortex. 2010 Jul;20(7):1556-73 - PubMed
  148. J Neurosci. 2008 Apr 30;28(18):4823-35 - PubMed
  149. J Neurosci. 1989 Jul;9(7):2432-42 - PubMed
  150. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9136-40 - PubMed
  151. J Comput Neurosci. 1996 Jun;3(2):91-110 - PubMed
  152. Curr Opin Neurobiol. 2000 Apr;10(2):172-9 - PubMed
  153. Neuron. 1999 Sep;24(1):31-47, 111-25 - PubMed
  154. PLoS Biol. 2016 Feb 18;14(2):e1002383 - PubMed
  155. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11569-73 - PubMed
  156. Nat Neurosci. 1999 Jan;2(1):79-87 - PubMed
  157. J Neurosci. 2013 Jan 2;33(1):17-25 - PubMed
  158. Curr Opin Neurobiol. 2015 Apr;31:133-40 - PubMed
  159. Neuron. 2010 Sep 9;67(5):885-96 - PubMed
  160. Science. 2001 Aug 10;293(5532):1159-63 - PubMed
  161. Curr Opin Neurobiol. 2015 Apr;31:173-80 - PubMed
  162. Nature. 2012 Oct 11;490(7419):226-31 - PubMed
  163. Proc Natl Acad Sci U S A. 2011 Jul 5;108(27):11262-7 - PubMed
  164. Cereb Cortex. 1997 Sep;7(6):534-45 - PubMed
  165. Neuron. 2006 Dec 21;52(6):1073-83 - PubMed
  166. Neuron. 2014 Oct 22;84(2):457-69 - PubMed
  167. Neuron. 2015 Oct 7;88(1):220-35 - PubMed
  168. Eur J Neurosci. 2009 Mar;29(5):1035-46 - PubMed
  169. Nature. 1996 Feb 22;379(6567):728-32 - PubMed
  170. Cereb Cortex. 2005 Sep;15(9):1424-37 - PubMed
  171. Trends Neurosci. 1996 Apr;19(4):130-7 - PubMed
  172. J Neurosci. 2012 Mar 7;32(10):3388-92 - PubMed
  173. Neuron. 2013 Feb 20;77(4):762-74 - PubMed
  174. Cereb Cortex. 2000 Sep;10(9):840-50 - PubMed
  175. Science. 1996 Apr 12;272(5259):271-4 - PubMed
  176. Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3626-31 - PubMed
  177. J Neurosci. 2010 Jan 27;30(4):1250-7 - PubMed
  178. Neuron. 2010 Apr 15;66(1):114-25 - PubMed
  179. J Vis. 2008 Nov 20;8(14):18.1-26 - PubMed
  180. Annu Rev Neurosci. 2001;24:1193-216 - PubMed
  181. J Neurophysiol. 2001 May;85(5):1969-85 - PubMed
  182. J Neurosci. 1993 Aug;13(8):3252-65 - PubMed
  183. J Comp Neurol. 1989 Jul 1;285(1):54-72 - PubMed
  184. Int J Psychophysiol. 2000 Dec 1;38(3):315-36 - PubMed
  185. Eur J Neurosci. 1990;2(4):344-357 - PubMed
  186. Nature. 2015 Feb 19;518(7539):399-403 - PubMed
  187. Science. 2009 May 29;324(5931):1207-10 - PubMed
  188. Neuron. 2014 Jul 16;83(2):455-66 - PubMed

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