Top-down modulation of visual cortical stimulus encoding and gamma independent of firing rates.
Uloženo v:
| Název: | Top-down modulation of visual cortical stimulus encoding and gamma independent of firing rates. |
|---|---|
| Autoři: | Lewis CM; Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, Germany.; Brain Research Institute, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland., Wunderle T; Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, Germany., Fries P; Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, 60528 Frankfurt, Germany.; Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, 6525 EN Nijmegen, Netherlands. |
| Zdroj: | BioRxiv : the preprint server for biology [bioRxiv] 2024 Apr 12. Date of Electronic Publication: 2024 Apr 12. |
| Způsob vydávání: | Preprint; Journal Article |
| Jazyk: | English |
| Informace o časopise: | Country of Publication: United States NLM ID: 101680187 Publication Model: Electronic Cited Medium: Internet ISSN: 2692-8205 (Electronic) Linking ISSN: 26928205 NLM ISO Abbreviation: bioRxiv Subsets: PubMed not MEDLINE |
| Abstrakt: | Neurons in primary visual cortex integrate sensory input with signals reflecting the animal's internal state to support flexible behavior. Internal variables, such as expectation, attention, or current goals, are imposed in a top-down manner via extensive feedback projections from higher-order areas. We optogenetically activated a high-order visual area, area 21a, in the lightly anesthetized cat (OptoTD), while recording from neuronal populations in V1. OptoTD induced strong, up to several fold, changes in gamma-band synchronization together with much smaller changes in firing rate, and the two effects showed no correlation. OptoTD effects showed specificity for the features of the simultaneously presented visual stimuli. OptoTD-induced changes in gamma synchronization, but not firing rates, were predictive of simultaneous changes in the amount of encoded stimulus information. Our findings suggest that one important role of top-down signals is to modulate synchronization and the information encoded by populations of sensory neurons. |
| Competing Interests: | Declaration of Interests P.F. and C.M.L. have a patent on implantation methods for thin-film electrodes, and P.F. is member of the Advisory Board of CorTec GmbH (Freiburg, Germany). |
| References: | Nature. 1995 May 11;375(6527):121-3. (PMID: 7753166) J Comp Neurol. 1984 Oct 10;229(1):1-38. (PMID: 6490972) Nat Neurosci. 2018 May;21(5):757-764. (PMID: 29662217) Neuron. 2015 Jan 21;85(2):390-401. (PMID: 25556836) Proc Natl Acad Sci U S A. 2014 Oct 7;111(40):14332-41. (PMID: 25205811) Physiol Rev. 1995 Jan;75(1):107-54. (PMID: 7831395) Nature. 2010 Apr 22;464(7292):1155-60. (PMID: 20414303) Nat Commun. 2018 Jun 11;9(1):2281. (PMID: 29892057) Neuron. 2019 Feb 6;101(3):500-513.e5. (PMID: 30635232) J Neurophysiol. 1968 Jan;31(1):14-27. (PMID: 4966614) Nature. 2009 Feb 26;457(7233):1142-5. (PMID: 19151697) Nat Neurosci. 2020 Jan;23(1):94-102. (PMID: 31792464) Nature. 1999 Mar 25;398(6725):338-41. (PMID: 10192334) Nature. 1995 Feb 16;373(6515):612-5. (PMID: 7854418) Proc Natl Acad Sci U S A. 2021 Oct 26;118(43):. (PMID: 34663727) J Neurosci. 2004 Oct 13;24(41):9067-75. (PMID: 15483125) Cell Rep. 2021 Dec 7;37(10):110086. (PMID: 34879273) Philos Trans R Soc Lond B Biol Sci. 2002 Dec 29;357(1428):1695-708. (PMID: 12626004) Biol Cybern. 1988;60(2):121-30. (PMID: 3228555) Nat Rev Neurosci. 2001 Oct;2(10):704-16. (PMID: 11584308) Nature. 1996 Feb 22;379(6567):728-32. (PMID: 8602219) Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14748-53. (PMID: 11121074) Cereb Cortex. 1991 Jan-Feb;1(1):1-47. (PMID: 1822724) Nat Rev Neurosci. 2014 Feb;15(2):111-22. (PMID: 24434912) Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):17083-8. (PMID: 12477930) J Neurosci. 1995 Feb;15(2):1463-83. (PMID: 7869111) Cereb Cortex. 1993 Jan-Feb;3(1):1-25. (PMID: 8439738) Science. 1996 Apr 12;272(5259):271-4. (PMID: 8602512) Science. 2007 Mar 30;315(5820):1860-2. (PMID: 17395832) Nat Neurosci. 2019 Oct;22(10):1677-1686. (PMID: 31551604) J Comp Neurol. 1984 Oct 10;229(1):39-47. (PMID: 6490975) Comput Intell Neurosci. 2011;2011:156869. (PMID: 21253357) Perception. 1972;1(4):371-94. (PMID: 4377168) Science. 2015 Jun 19;348(6241):1352-5. (PMID: 26089513) Neuron. 2012 Sep 6;75(5):875-88. (PMID: 22958827) Nat Neurosci. 2023 Feb;26(2):295-305. (PMID: 36536242) Neuroimage. 2010 May 15;51(1):112-22. (PMID: 20114076) Elife. 2021 Aug 24;10:. (PMID: 34473058) Science. 2014 Aug 8;345(6197):660-5. (PMID: 25104383) Annu Rev Neurosci. 2004;27:419-51. (PMID: 15217339) Neuron. 2022 Aug 17;110(16):2545-2570. (PMID: 35643077) Nature. 2023 May;617(7962):769-776. (PMID: 37138089) Nature. 1998 Aug 20;394(6695):784-7. (PMID: 9723617) Nat Commun. 2022 Mar 1;13(1):1099. (PMID: 35232956) Nat Neurosci. 2005 Sep;8(9):1263-8. (PMID: 16116447) J Neurophysiol. 1972 Jul;35(4):560-74. (PMID: 4624740) Science. 1991 May 24;252(5009):1177-9. (PMID: 2031188) Proc Natl Acad Sci U S A. 2011 Jul 5;108(27):11262-7. (PMID: 21690410) J Neurosci. 2005 Nov 16;25(46):10577-97. (PMID: 16291931) Nat Neurosci. 2017 Jul;20(7):1014-1022. (PMID: 28530664) Neuron. 2016 Oct 5;92(1):240-251. (PMID: 27667008) Neuron. 2010 Apr 15;66(1):114-25. (PMID: 20399733) Science. 2023 Feb 3;379(6631):468-473. (PMID: 36730414) Nature. 1993 Nov 11;366(6451):153-6. (PMID: 8232553) Nature. 2010 Jun 10;465(7299):788-92. (PMID: 20473285) Cell Rep. 2021 May 4;35(5):109083. (PMID: 33951439) J Neurosci. 2011 Nov 2;31(44):15919-31. (PMID: 22049435) Curr Opin Neurobiol. 2015 Apr;31:62-6. (PMID: 25217807) J Neurosci. 2017 Jul 12;37(28):6698-6711. (PMID: 28592697) J Neurosci. 2013 May 8;33(19):8504-17. (PMID: 23658187) iScience. 2024 Jan 06;27(2):108816. (PMID: 38323011) Nat Rev Neurosci. 2009 Feb;10(2):113-25. (PMID: 19145235) Nature. 1989 Mar 23;338(6213):334-7. (PMID: 2922061) Elife. 2022 Nov 23;11:. (PMID: 36416886) Science. 1985 Aug 23;229(4715):782-4. (PMID: 4023713) Philos Trans R Soc Lond B Biol Sci. 2002 Dec 29;357(1428):1739-52. (PMID: 12626008) Science. 1988 Jun 17;240(4859):1627-31. (PMID: 3289116) Annu Rev Neurosci. 2020 Jul 8;43:391-415. (PMID: 32250724) Neuron. 2018 Feb 7;97(3):698-715.e10. (PMID: 29420935) Nature. 2013 Jul 25;499(7459):476-80. (PMID: 23803766) Science. 2001 Feb 23;291(5508):1560-3. (PMID: 11222864) Neuron. 2019 Apr 3;102(1):249-259.e4. (PMID: 30770252) Annu Rev Neurosci. 2012;35:203-25. (PMID: 22443509) Neuron. 2017 Jul 5;95(1):209-220.e3. (PMID: 28625487) Elife. 2019 Feb 11;8:. (PMID: 30741160) Nat Neurosci. 2013 Jul;16(7):824-31. (PMID: 23799475) Nat Neurosci. 2017 Jul;20(7):951-959. (PMID: 28481348) Curr Biol. 2013 Jan 21;23(2):156-61. (PMID: 23260469) Proc Natl Acad Sci U S A. 2014 Mar 4;111(9):3626-31. (PMID: 24554080) Cereb Cortex. 2011 Jun;21(6):1254-72. (PMID: 21045004) Nature. 1998 Sep 24;395(6700):376-81. (PMID: 9759726) Neuron. 2010 Feb 25;65(4):472-9. (PMID: 20188652) Neuroreport. 1997 Mar 24;8(5):1263-6. (PMID: 9175126) Neuron. 2023 Feb 1;111(3):405-417.e5. (PMID: 36384143) J Physiol. 1959 Oct;148:574-91. (PMID: 14403679) Spat Vis. 1997;10(4):433-6. (PMID: 9176952) Cereb Cortex. 2000 Feb;10(2):149-59. (PMID: 10667983) Cereb Cortex. 2000 Dec;10(12):1217-32. (PMID: 11073871) Neuron. 2015 Oct 7;88(1):220-35. (PMID: 26447583) Proc Natl Acad Sci U S A. 2016 Feb 2;113(5):E606-15. (PMID: 26787906) Nat Neurosci. 2023 Nov;26(11):1953-1959. (PMID: 37828227) Cell. 2014 Mar 13;156(6):1139-1152. (PMID: 24630718) Elife. 2024 Nov 19;12:. (PMID: 39560660) Nat Rev Neurosci. 2013 May;14(5):350-63. (PMID: 23595013) Nature. 2020 Jun;582(7813):545-549. (PMID: 32499655) Science. 2019 Apr 19;364(6437):255. (PMID: 31000656) J Neurosci. 2012 Nov 14;32(46):16172-80. (PMID: 23152601) Science. 2002 Mar 8;295(5561):1907-10. (PMID: 11884759) J Neurosci. 2002 Oct 1;22(19):8633-46. (PMID: 12351737) Front Neuroanat. 2017 Aug 22;11:71. (PMID: 28878631) Nat Rev Neurosci. 2001 Aug;2(8):539-50. (PMID: 11483997) Nat Neurosci. 2013 Aug;16(8):1068-76. (PMID: 23817549) Annu Rev Neurosci. 2017 Jul 25;40:425-451. (PMID: 28471714) J Neurophysiol. 1993 Sep;70(3):909-19. (PMID: 8229178) Cereb Cortex. 2004 Oct;14(10):1059-70. (PMID: 15115747) Nature. 2003 Jan 23;421(6921):370-3. (PMID: 12540901) Physiol Rev. 1985 Jan;65(1):37-100. (PMID: 3880898) |
| Grant Information: | U54 MH091657 United States MH NIMH NIH HHS |
| Contributed Indexing: | Keywords: cortex; feedback; gamma; optogenetics; stimulus decoding; synchronization; top-down; vision |
| Entry Date(s): | Date Created: 20240422 Latest Revision: 20241120 |
| Update Code: | 20250114 |
| PubMed Central ID: | PMC11030389 |
| DOI: | 10.1101/2024.04.11.589006 |
| PMID: | 38645050 |
| Databáze: | MEDLINE |
| Abstrakt: | Neurons in primary visual cortex integrate sensory input with signals reflecting the animal's internal state to support flexible behavior. Internal variables, such as expectation, attention, or current goals, are imposed in a top-down manner via extensive feedback projections from higher-order areas. We optogenetically activated a high-order visual area, area 21a, in the lightly anesthetized cat (OptoTD), while recording from neuronal populations in V1. OptoTD induced strong, up to several fold, changes in gamma-band synchronization together with much smaller changes in firing rate, and the two effects showed no correlation. OptoTD effects showed specificity for the features of the simultaneously presented visual stimuli. OptoTD-induced changes in gamma synchronization, but not firing rates, were predictive of simultaneous changes in the amount of encoded stimulus information. Our findings suggest that one important role of top-down signals is to modulate synchronization and the information encoded by populations of sensory neurons. |
|---|---|
| ISSN: | 2692-8205 |
| DOI: | 10.1101/2024.04.11.589006 |
Full Text Finder
Nájsť tento článok vo Web of Science