Structural plasticity within highly specific neuronal populations identifies a unique parcellation of motor learning in the adult brain.
Cortical networks undergo adaptations during learning, including increases in dendritic complexity and spines. We hypothesized that structural elaborations during learning are restricted to discrete subsets of cells preferentially activated by, and relevant to, novel experience. Accordingly, we examined corticospinal motor neurons segregated on the basis of their distinct descending projection patterns, and their contribution to specific aspects of motor control during a forelimb skilled grasping task in adult rats. Learning-mediated structural adaptations, including extensive expansions of spine density and dendritic complexity, were restricted solely to neurons associated with control of distal forelimb musculature required for skilled grasping; neurons associated with control of proximal musculature were unchanged by the experience. We further found that distal forelimb-projecting and proximal forelimb-projecting neurons are intermingled within motor cortex, and that this distribution does not change as a function of skill acquisition. These findings indicate that representations of novel experience in the adult motor cortex are associated with selective structural expansion in networks of functionally related, active neurons that are distributed across a single cortical domain. These results identify a distinct parcellation of cortical resources in support of learning.
Department of Neurosciences, University of California, La Jolla, CA 92093-0626, USA.
Ling
L
Wang
James M
JM
Conner
Jessica
J
Rickert
Mark H
MH
Tuszynski
D000818:Animals; D003712:Dendrites / Q000502:physiology; D005552:Forelimb / Q000502:physiology; D007858:Learning / Q000502:physiology*; D008297:Male; D009044:Motor Cortex / Q000502:physiology*; D009046:Motor Neurons / Q000502:physiology*; D018482:Muscle, Skeletal / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D051381:Rats; D011916:Rats, Inbred F344
J Neurosci. 2004 Jan 21;24(3):628-33
14736848
Neuroscience. 1989;28(1):3-16
2668782
J Comp Neurol. 2004 Aug 16;476(2):174-85
15248197
Science. 2000 Oct 20;290(5491):533-6
11039938
J Neurosci. 1999 Nov 15;19(22):10153-63
10559423
J Neurosci. 1996 Jul 15;16(14):4529-35
8699262
Neurobiol Learn Mem. 2002 Jul;78(1):35-52
12071666
Nature. 2007 Nov 15;450(7168):425-9
18004384
Behav Neural Biol. 1985 Sep;44(2):301-14
2415103
Nat Neurosci. 1998 Jul;1(3):230-4
10195148
Neuropharmacology. 2000 Mar 3;39(5):788-805
10699445
Nature. 1995 Sep 14;377(6545):155-8
7675082
J Neurophysiol. 1994 Jun;71(6):2543-7
7931533
Nature. 2009 Dec 17;462(7275):915-9
19946267
J Neurosci. 2002 Oct 1;22(19):8597-606
12351733
J Comp Neurol. 2000 Apr 10;419(3):286-96
10723005
Neuron. 2009 Aug 27;63(4):508-22
19709632
Neuropsychologia. 1989;27(1):61-9
2710317
J Anat. 1968 Mar;102(Pt 3):363-74
5656134
J Comp Neurol. 1987 Jan 15;255(3):369-85
2950140
Brain Res. 1996 Apr 1;714(1-2):1-8
8861603
Neuron. 2003 Jun 5;38(5):819-29
12797965
Nature. 2009 Jan 15;457(7227):313-7
19005470
J Anat. 1953 Oct;87(4):387-406
13117757
J Neurophysiol. 1998 Dec;80(6):3321-5
9862925