Disentangling neuroplasticity mechanisms in post-stroke language recovery.

Anne Billot, Swathi Kiran
Author Information
  1. Anne Billot: Center for Brain Recovery, Boston University, Boston, USA; Department of Psychology, Center for Brain Science, Harvard University, Cambridge, Massachusetts, USA; Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts, USA.
  2. Swathi Kiran: Center for Brain Recovery, Boston University, Boston, USA. Electronic address: kirans@bu.edu.

Abstract

A major objective in post-stroke aphasia research is to gain a deeper understanding of neuroplastic mechanisms that drive language recovery, with the ultimate goal of enhancing treatment outcomes. Subsequent to recent advances in neuroimaging techniques, we now have the ability to examine more closely how neural activity patterns change after a stroke. However, the way these neural activity changes relate to language impairments and language recovery is still debated. The aim of this review is to provide a theoretical framework to better investigate and interpret neuroplasticity mechanisms underlying language recovery in post-stroke aphasia. We detail two sets of neuroplasticity mechanisms observed at the synaptic level that may explain functional neuroimaging findings in post-stroke aphasia recovery at the network level: feedback-based homeostatic plasticity and associative Hebbian plasticity. In conjunction with these plasticity mechanisms, higher-order cognitive control processes dynamically modulate neural activity in other regions to meet communication demands, despite reduced neural resources. This work provides a network-level neurobiological framework for understanding neural changes observed in post-stroke aphasia and can be used to define guidelines for personalized treatment development.

Keywords

References

  1. Cortex. 2018 Nov;108:173-192 [PMID: 30243049]
  2. Brain Lang. 2011 Dec;119(3):206-13 [PMID: 21864891]
  3. Neurobiol Sleep Circadian Rhythms. 2016 Nov 29;2:94-105 [PMID: 31236498]
  4. J Cereb Blood Flow Metab. 2000 Jan;20(1):45-52 [PMID: 10616792]
  5. J Neurosci. 2022 Jan 26;42(4):657-669 [PMID: 34872927]
  6. Front Physiol. 2020 Mar 10;11:200 [PMID: 32210840]
  7. Neuroimage. 2021 Jun;233:117960 [PMID: 33744459]
  8. Restor Neurol Neurosci. 2018;36(3):359-385 [PMID: 29782329]
  9. Proc Natl Acad Sci U S A. 2001 Nov 20;98(24):13763-8 [PMID: 11698650]
  10. Brain. 2015 Apr;138(Pt 4):1097-112 [PMID: 25688082]
  11. Cortex. 2019 Dec;121:147-168 [PMID: 31627014]
  12. Eur J Neurosci. 1995 Feb 1;7(2):180-91 [PMID: 7538854]
  13. Neuron. 2004 Sep 30;44(1):5-21 [PMID: 15450156]
  14. Nat Commun. 2015 Oct 01;6:8414 [PMID: 26423222]
  15. Adv Physiol Educ. 2004 Dec;28(1-4):180-7 [PMID: 15545346]
  16. Neuropsychol Rehabil. 2019 Apr;29(3):395-439 [PMID: 28424029]
  17. Epilepsy Behav. 2012 Jan;23(1):81-6 [PMID: 22197719]
  18. Brain Stimul. 2019 Jan - Feb;12(1):190-191 [PMID: 30318184]
  19. Proc Natl Acad Sci U S A. 2007 Jun 26;104(26):11073-8 [PMID: 17576922]
  20. Brain. 2006 Jun;129(Pt 6):1371-84 [PMID: 16638796]
  21. Trends Cogn Sci. 2014 Mar;18(3):120-6 [PMID: 24440115]
  22. Cold Spring Harb Perspect Biol. 2012 Jan 01;4(1):a005736 [PMID: 22086977]
  23. Nat Neurosci. 2000 Nov;3 Suppl:1178-83 [PMID: 11127835]
  24. Cell. 2008 Oct 31;135(3):422-35 [PMID: 18984155]
  25. J Physiol. 1992;453:525-46 [PMID: 1464843]
  26. J Neurol. 2013 Jan;260(1):166-71 [PMID: 22820721]
  27. Neuron. 2009 Feb 26;61(4):609-20 [PMID: 19249280]
  28. Ann Neurol. 2001 Nov;50(5):561-6 [PMID: 11706960]
  29. Neurobiol Lang (Camb). 2021;2(1):22-82 [PMID: 33884373]
  30. Neuroimage. 2019 Apr 15;190:14-31 [PMID: 29175498]
  31. Neuron. 2017 Jan 18;93(2):281-290 [PMID: 28103477]
  32. Brain. 2019 Oct 1;142(10):3190-3201 [PMID: 31501862]
  33. Neurology. 2018 Apr 3;90(14):e1222-e1230 [PMID: 29523641]
  34. Physiology (Bethesda). 2015 Sep;30(5):358-70 [PMID: 26328881]
  35. J Neurosci. 1982 Jan;2(1):32-48 [PMID: 7054394]
  36. Sleep Med Rev. 2006 Feb;10(1):49-62 [PMID: 16376591]
  37. Nat Rev Neurosci. 2002 Mar;3(3):201-15 [PMID: 11994752]
  38. Proc Natl Acad Sci U S A. 2011 Sep 27;108(39):16428-33 [PMID: 21885736]
  39. Cereb Cortex. 1994 Jan-Feb;4(1):8-26 [PMID: 8180494]
  40. Ann Neurol. 1983 May;13(5):558-66 [PMID: 6870207]
  41. Front Hum Neurosci. 2013 Dec 09;7:832 [PMID: 24368899]
  42. Neuron. 2011 Oct 20;72(2):385-96 [PMID: 22017995]
  43. Front Hum Neurosci. 2017 Feb 28;11:91 [PMID: 28293185]
  44. Nat Rev Neurosci. 2012 Jun 20;13(7):478-90 [PMID: 22714019]
  45. Elife. 2023 Nov 21;12: [PMID: 37986628]
  46. Neurobiol Lang (Camb). 2020 Oct 01;1(4):402-433 [PMID: 37215585]
  47. J Speech Lang Hear Res. 2019 Nov 22;62(11):3973-3985 [PMID: 31756154]
  48. Neuroimage. 2005 Nov 1;28(2):481-9 [PMID: 16099176]
  49. Neurology. 2000 Dec 26;55(12):1883-94 [PMID: 11134389]
  50. Brain Struct Funct. 2017 Apr;222(3):1231-1241 [PMID: 27449063]
  51. Neurobiol Lang (Camb). 2021;2(2):202-225 [PMID: 34585141]
  52. Neuroimage. 2022 May 1;251:119001 [PMID: 35172200]
  53. J Neurosci. 2007 Feb 28;27(9):2349-56 [PMID: 17329432]
  54. Brain. 2016 Apr;139(Pt 4):1152-63 [PMID: 26912641]
  55. Nat Rev Neurosci. 2001 Nov;2(11):820-9 [PMID: 11715058]
  56. Neuroscientist. 2003 Feb;9(1):64-75 [PMID: 12580341]
  57. Sci Data. 2022 Aug 29;9(1):529 [PMID: 36038572]
  58. Cell. 2014 Mar 27;157(1):163-86 [PMID: 24679534]
  59. Stroke. 2023 Jan;54(1):55-66 [PMID: 36542078]
  60. Annu Rev Psychol. 2013;64:135-68 [PMID: 23020641]
  61. J Neurosci. 2010 Sep 1;30(35):11670-7 [PMID: 20810887]
  62. Neuroinformatics. 2004;2(2):145-62 [PMID: 15319512]
  63. Brain Res. 1992 May 22;581(1):156-60 [PMID: 1498666]
  64. Ann Clin Transl Neurol. 2021 Sep;8(9):1884-1894 [PMID: 34406705]
  65. PLoS Comput Biol. 2009 Jun;5(6):e1000408 [PMID: 19521503]
  66. Front Neurol. 2018 Apr 09;9:225 [PMID: 29686646]
  67. Cortex. 1979 Dec;15(4):627-53 [PMID: 95004]
  68. Brain Struct Funct. 2021 Jun;226(5):1585-1599 [PMID: 33877431]
  69. Brain Lang. 1979 Jul;8(1):34-50 [PMID: 476474]
  70. Brain. 2014 Jan;137(Pt 1):242-54 [PMID: 24163248]
  71. Science. 2004 Jun 25;304(5679):1926-9 [PMID: 15218136]
  72. Brain Lang. 1984 Jan;21(1):72-84 [PMID: 6199078]
  73. Neuropsychol Rehabil. 2010 Apr;20(2):289-305 [PMID: 20077315]
  74. J Neurosci. 2013 Jun 26;33(26):10688-97 [PMID: 23804092]
  75. Annu Rev Physiol. 2001;63:847-69 [PMID: 11181978]
  76. Neuropsychologia. 2015 Sep;76:170-81 [PMID: 25448851]
  77. Nature. 2006 Nov 30;444(7119):610-3 [PMID: 17086200]
  78. Neuroimage. 2012 Apr 2;60(2):854-63 [PMID: 22227052]
  79. Prog Brain Res. 2013;207:141-71 [PMID: 24309254]
  80. J Speech Lang Hear Res. 2008 Feb;51(1):S225-39 [PMID: 18230848]
  81. J Cogn Neurosci. 2018 Apr;30(4):514-525 [PMID: 29211656]
  82. Neuron. 2019 Aug 21;103(4):563-581 [PMID: 31437453]
  83. Nat Neurosci. 2012 Mar 18;15(4):528-36 [PMID: 22426254]
  84. Brain Res. 1996 Sep 9;733(1):142-8 [PMID: 8891261]
  85. Philos Trans R Soc Lond B Biol Sci. 2017 Mar 5;372(1715): [PMID: 28093558]
  86. Arch Phys Med Rehabil. 2019 Jul;100(7):1251-1258 [PMID: 30639272]
  87. Ann Neurol. 2010 Nov;68(5):753-6 [PMID: 20687116]
  88. J Neuroeng Rehabil. 2016 Apr 30;13(1):42 [PMID: 27130577]
  89. Neurol Sci. 2019 Oct;40(10):2141-2146 [PMID: 31183673]
  90. Nat Rev Neurosci. 2009 Dec;10(12):861-72 [PMID: 19888284]
  91. J Neurol. 2019 Jun;266(6):1303-1309 [PMID: 30820740]
  92. Neuropsychologia. 2016 Apr;84:113-26 [PMID: 26775192]
  93. Trends Cogn Sci. 2003 Apr;7(4):151-152 [PMID: 12691761]
  94. Neuron. 2012 Mar 22;73(6):1195-203 [PMID: 22445346]
  95. Trends Cogn Sci. 2016 Nov;20(11):805-817 [PMID: 27707588]
  96. Cortex. 2023 Feb;159:75-100 [PMID: 36610109]
  97. Neurology. 2008 Jan 22;70(4):290-8 [PMID: 18209203]
  98. Neuroimage. 2017 Jul 1;154:23-32 [PMID: 27894889]
  99. Brain. 2003 Feb;126(Pt 2):470-81 [PMID: 12538413]
  100. Med Sci Monit. 2012 Mar;18(3):CR135-7 [PMID: 22367124]
  101. Ann Neurol. 1998 Aug;44(2):255-8 [PMID: 9708549]
  102. Neurology. 2011 May 17;76(20):1726-34 [PMID: 21576689]
  103. Cortex. 2019 Nov;120:394-418 [PMID: 31419597]
  104. Neuron. 2018 Oct 24;100(2):463-475 [PMID: 30359609]
  105. Front Hum Neurosci. 2021 Oct 25;15:680933 [PMID: 34759804]
  106. J Cogn Neurosci. 2011 Feb;23(2):349-61 [PMID: 20146606]
  107. J Neurosci. 2013 Nov 27;33(48):18979-86 [PMID: 24285902]
  108. Neuroimage. 2008 Feb 15;39(4):2038-46 [PMID: 18096407]
  109. Trials. 2022 Aug 17;23(1):668 [PMID: 35978374]
  110. Brain. 2017 Jul 1;140(7):1947-1958 [PMID: 29177494]
  111. Elife. 2017 May 24;6: [PMID: 28537558]
  112. Arch Neurol. 2012 Feb;69(2):161-7 [PMID: 21987395]
  113. PLoS One. 2014 Jul 18;9(7):e102557 [PMID: 25036386]
  114. Brain Lang. 2017 Apr;167:94-105 [PMID: 27036946]
  115. Nat Commun. 2021 Mar 31;12(1):1994 [PMID: 33790281]
  116. Brain Topogr. 2023 Mar;36(2):135-171 [PMID: 36749552]
  117. J Neurophysiol. 2005 Sep;94(3):1668-75 [PMID: 15872061]
  118. Neuron. 2013 Apr 24;78(2):364-75 [PMID: 23562541]
  119. Cogn Process. 2006 Jun;7(2):73-88 [PMID: 16683170]
  120. Curr Opin Neurobiol. 2019 Feb;54:186-193 [PMID: 30017789]
  121. Handb Clin Neurol. 2022;185:131-150 [PMID: 35078595]
  122. J Int Neuropsychol Soc. 2002 Mar;8(3):448-60 [PMID: 11939702]
  123. Brain Res Brain Res Rev. 2004 Jan;44(1):1-12 [PMID: 14739000]
  124. Ann Neurol. 2017 Jul;82(1):147-151 [PMID: 28628946]
  125. Lancet. 2017 Apr 15;389(10078):1528-1538 [PMID: 28256356]
  126. Proc Natl Acad Sci U S A. 2016 Jul 26;113(30):E4367-76 [PMID: 27402738]
  127. Neurosci Lett. 1995 Jun 30;193(2):101-4 [PMID: 7478151]
  128. Brain Lang. 2006 Jul;98(1):118-23 [PMID: 16564566]
  129. Neurosci Lett. 2016 Mar 23;617:88-93 [PMID: 26872852]
  130. Trends Neurosci. 2000 Oct;23(10):475-83 [PMID: 11006464]
  131. J Neurosci. 2010 Mar 3;30(9):3297-303 [PMID: 20203189]
  132. Stroke. 2014 Feb;45(2):545-52 [PMID: 24309584]
  133. Neuron. 1995 Mar;14(3):477-85 [PMID: 7695894]
  134. Neuroimage. 2016 Mar;128:264-272 [PMID: 26801604]
  135. Cereb Cortex. 2021 Jul 29;31(9):4006-4023 [PMID: 33895807]
  136. Alzheimers Res Ther. 2021 Aug 31;13(1):146 [PMID: 34465384]
  137. Brain. 2023 Mar 1;146(3):1021-1039 [PMID: 35388420]
  138. Annu Rev Neurosci. 1990;13:25-42 [PMID: 2183676]
  139. Neuropsychologia. 2021 Nov 12;162:108047 [PMID: 34610342]
  140. Neuroreport. 2001 Oct 29;12(15):3341-7 [PMID: 11711883]
  141. Trends Cogn Sci. 2002 Oct 1;6(10):416-421 [PMID: 12413574]
  142. Annu Rev Neurosci. 2001;24:167-202 [PMID: 11283309]
  143. Neuron. 2011 Nov 17;72(4):665-78 [PMID: 22099467]
  144. Science. 1992 Sep 4;257(5075):1412-5 [PMID: 1529342]
  145. Philos Trans R Soc Lond B Biol Sci. 2017 Mar 5;372(1715): [PMID: 28093552]
  146. J Neurosci. 2016 Jun 8;36(23):6147-55 [PMID: 27277793]
  147. J Neurosci. 2012 Oct 3;32(40):14010-21 [PMID: 23035108]
  148. Stroke. 1995 Nov;26(11):2135-44 [PMID: 7482662]
  149. Front Hum Neurosci. 2015 Jun 09;9:316 [PMID: 26106314]
  150. Brain Lang. 2022 Sep;232:105163 [PMID: 35921727]
  151. Cortex. 2018 Apr;101:44-59 [PMID: 29414460]
  152. Trends Cogn Sci. 2010 Apr;14(4):172-9 [PMID: 20171926]
  153. Hum Brain Mapp. 2014 Aug;35(8):3919-31 [PMID: 24453137]
  154. Brain. 2020 Mar 1;143(3):844-861 [PMID: 32068789]
  155. Neural Plast. 2016;2016:4796906 [PMID: 26881111]
  156. Biol Psychiatry. 2013 Sep 1;74(5):340-7 [PMID: 23290495]
  157. Neuroimage. 1995 Dec;2(4):296-305 [PMID: 9343614]
  158. Brain. 2002 Aug;125(Pt 8):1896-907 [PMID: 12135979]
  159. Hum Brain Mapp. 2017 Mar;38(3):1636-1658 [PMID: 27981674]
  160. Neuroimage. 2013 Oct 1;79:162-71 [PMID: 23631993]
  161. Annu Rev Neurosci. 2015 Jul 8;38:269-89 [PMID: 25897871]
  162. eNeuro. 2016 Apr 04;3(2): [PMID: 27088127]
  163. J Neurophysiol. 2008 Dec;100(6):3328-42 [PMID: 18799601]
  164. J Neurosci. 2015 Oct 28;35(43):14602-11 [PMID: 26511249]
  165. BMC Neurosci. 2009 Sep 22;10:118 [PMID: 19772660]
  166. Neurorehabil Neural Repair. 2016 Mar;30(3):244-57 [PMID: 26150146]
  167. Neurorehabil Neural Repair. 2020 Oct;34(10):945-953 [PMID: 32924765]
  168. Front Hum Neurosci. 2016 Mar 16;10:109 [PMID: 27014039]
  169. Science. 1997 May 2;276(5313):821-4 [PMID: 9115211]
  170. J Physiol. 2016 Aug 15;594(16):4485-98 [PMID: 27524792]
  171. Front Behav Neurosci. 2014 May 12;8:167 [PMID: 24860452]
  172. Arch Phys Med Rehabil. 2009 Dec;90(12):2026-33 [PMID: 19969164]
  173. Neuroimage Clin. 2013 Mar 22;2:424-33 [PMID: 24179796]
  174. Neuropsychologia. 2016 Dec;93(Pt B):413-424 [PMID: 27063061]
  175. Proc Natl Acad Sci U S A. 2006 Jun 27;103(26):10046-51 [PMID: 16788060]
  176. Nat Neurosci. 2009 Nov;12(11):1370-1 [PMID: 19820707]
  177. J Anat. 2004 Dec;205(6):433-42 [PMID: 15610392]
  178. Arch Neurol. 1987 Jan;44(1):73-82 [PMID: 3800725]
  179. Brain Res Cogn Brain Res. 1999 Jan;7(3):285-94 [PMID: 9838166]
  180. Nature. 2001 Jul 12;412(6843):150-7 [PMID: 11449264]
  181. Cereb Cortex. 2016 Aug;26(8):3580-3590 [PMID: 27242027]
  182. Brain Lang. 2015 Nov;150:103-16 [PMID: 26398158]
  183. JAMA Neurol. 2018 Dec 1;75(12):1470-1476 [PMID: 30128538]
  184. Brain Lang. 1994 Nov;47(4):684-98 [PMID: 7859059]
  185. Neurology. 2022 Jul 12;99(2):e119-e128 [PMID: 35508398]
  186. Stroke. 2017 Oct;48(10):2855-2864 [PMID: 28904232]
  187. Neuroscience. 2012 Mar 15;205:81-90 [PMID: 22249158]
  188. Front Neurol. 2019 Apr 02;10:295 [PMID: 31001187]
  189. Nat Neurosci. 2015 May;18(5):744-51 [PMID: 25849989]
  190. Restor Neurol Neurosci. 2013;31(6):693-705 [PMID: 23963339]
  191. Front Syst Neurosci. 2022 Jan 10;15:806544 [PMID: 35082606]
  192. Brain Lang. 1993 Feb;44(2):153-64 [PMID: 8428309]
  193. Nature. 2009 Dec 17;462(7275):920-4 [PMID: 19946265]
  194. Alzheimers Dement. 2020 Sep;16(9):1305-1311 [PMID: 30222945]
  195. Proc Natl Acad Sci U S A. 2020 Dec 22;117(51):32779-32790 [PMID: 33273118]
  196. Hum Brain Mapp. 2017 Jun;38(6):3151-3162 [PMID: 28345282]
  197. J Neurosci. 2018 Jul 11;38(28):6399-6410 [PMID: 29884739]
  198. Sci Rep. 2021 May 18;11(1):10497 [PMID: 34006902]
  199. Nat Hum Behav. 2017;1: [PMID: 28713861]
  200. Brain Lang. 2017 Apr;167:106-113 [PMID: 27291336]
  201. Ann Neurol. 2018 Mar;83(3):612-622 [PMID: 29451321]
  202. Top Stroke Rehabil. 2012 Nov-Dec;19(6):523-35 [PMID: 23192717]
  203. J Neurosci. 2020 Jun 3;40(23):4536-4550 [PMID: 32317387]
  204. J Neurosci. 2010 Sep 1;30(35):11558-64 [PMID: 20810877]
  205. J Neurosci. 2012 Jan 25;32(4):1395-407 [PMID: 22279224]
  206. Nat Rev Neurol. 2020 Jan;16(1):43-55 [PMID: 31772339]
  207. Neuropsychopharmacology. 2008 Jun;33(7):1704-12 [PMID: 17851541]
  208. J Neurosci. 2006 Aug 2;26(31):8069-73 [PMID: 16885220]
  209. Neural Plast. 2013;2013:103949 [PMID: 23840970]
  210. Annu Rev Neurosci. 2008;31:25-46 [PMID: 18275283]
  211. Arch Phys Med Rehabil. 2016 Dec;97(12):2188-2201.e8 [PMID: 27063364]
  212. Front Neuroanat. 2014 Oct 16;8:115 [PMID: 25360087]
  213. Proc Natl Acad Sci U S A. 2016 Oct 25;113(43):E6679-E6685 [PMID: 27729529]
  214. Neuron. 2013 May 8;78(3):545-53 [PMID: 23583623]
  215. Brain. 2014 Sep;137(Pt 9):2408-22 [PMID: 24871646]
  216. J Neurosci. 2005 Nov 2;25(44):10167-79 [PMID: 16267224]
  217. Neuron. 2015 Jun 3;86(5):1290-303 [PMID: 26050045]
  218. Front Synaptic Neurosci. 2010 Jul 30;2:34 [PMID: 21423520]
  219. J Neurosci. 2017 Aug 9;37(32):7606-7618 [PMID: 28676576]

Grants

  1. R01 DC016950/NIDCD NIH HHS
  2. R01 DC020653/NIDCD NIH HHS
  3. U01 DC014922/NIDCD NIH HHS

MeSH Term

Humans
Stroke
Aphasia
Neuroimaging
Language
Neuronal Plasticity
Recovery of Function

Word Cloud

Created with Highcharts 10.0.0post-strokemechanismslanguagerecoveryneuralplasticityaphasiaactivityneuroplasticityunderstandingtreatmentneuroimagingchangesframeworkobservedHebbianmajorobjectiveresearchgaindeeperneuroplasticdriveultimategoalenhancingoutcomesSubsequentrecentadvancestechniquesnowabilityexaminecloselypatternschangestrokeHoweverwayrelateimpairmentsstilldebatedaimreviewprovidetheoreticalbetterinvestigateinterpretunderlyingdetailtwosetssynapticlevelmayexplainfunctionalfindingsnetworklevel:feedback-basedhomeostaticassociativeconjunctionhigher-ordercognitivecontrolprocessesdynamicallymodulateregionsmeetcommunicationdemandsdespitereducedresourcesworkprovidesnetwork-levelneurobiologicalcanuseddefineguidelinespersonalizeddevelopmentDisentanglingAphasiaControlHomeostaticNeuroplasticityRecoveryRehabilitationStrokefMRI

Similar Articles

Cited By