title: Combined adaptiveness of specific motor cortical ensembles underlies learning.
abstract: Learning motor skills entails adaptation of neural computations that can generate or modify associations between sensations and actions. Indeed, humans can use different strategies when adapting to dynamic loads depending on available sensory feedback. Here, we examined how neural activity in motor cortex was modified when monkeys made arm reaches to a visual target and locally adapted to curl force field with or without visual trajectory feedback. We found that firing rates of a large subpopulation of cells were consistently modulated depending on the distance of their preferred direction from the learned movement direction. The newly acquired activity followed a cosine-like function, with maximal increase in directions that opposed the perturbing force and decrease in opposite directions. As a result, the combined neuronal activity generated an adapted population vector. The results suggest that this could be achieved without changing the tuning properties of the cells. This population directional signal was however altered in the absence of visual feedback; while the cosine pattern of modulation was maintained, the population distributions of modulated cells differed across feedback consistent with the different trajectory shapes. Finally, we predicted generalization patterns of force-field learning based on the cosine-like modulation. These conformed to reported features of generalization in humans, suggesting that the generalization function was related to the observed rate modulations in the motor cortex. Overall, the findings suggest that the new combined activation of neuronal ensembles could underlie the change in the internal model of movement dynamics in a way that depends on available sensory feedback and chosen strategy.
authors.affiliation: Department of Medical Neurobiology, Institute for Medical Research Israel-Canada, Hadassah Medical School, Hadassah University Hospital, Jerusalem 91120, Israel. fritziea@ekmd.huji.ac.il
authors.forename: Fritzie
authors.initials: F
authors.lastname: Arce
authors.forename: Itai
authors.initials: I
authors.lastname: Novick
authors.forename: Yael
authors.initials: Y
authors.lastname: Mandelblat-Cerf
authors.forename: Zvi
authors.initials: Z
authors.lastname: Israel
authors.forename: Claude
authors.initials: C
authors.lastname: Ghez
authors.forename: Eilon
authors.initials: E
authors.lastname: Vaadia
mesh_terms: D000200:Action Potentials; D000223:Adaptation, Psychological / Q000502:physiology*; D000465:Algorithms; D000818:Animals; D001132:Arm / Q000502:physiology; D030141:Feedback, Psychological / Q000502:physiology*; D007858:Learning / Q000502:physiology*; D008252:Macaca fascicularis; D008959:Models, Neurological; D009044:Motor Cortex / Q000502:physiology*; D018482:Muscle, Skeletal / Q000502:physiology; D009434:Neural Pathways / Q000502:physiology; D009473:Neuronal Plasticity; D009474:Neurons / Q000502:physiology*; D009483:Neuropsychological Tests; D011597:Psychomotor Performance / Q000502:physiology; D014796:Visual Perception / Q000502:physiology*
references.citation: Eur J Neurosci. 2007 Aug;26(4):1055-66
references.pmid: 17714196
references.citation: Curr Opin Neurobiol. 1999 Dec;9(6):718-27
references.pmid: 10607637
references.citation: Science. 1992 Mar 20;255(5051):1517-23
references.pmid: 1549781
references.citation: Neuron. 2003 Jan 23;37(2):347-59
references.pmid: 12546828
references.citation: Exp Brain Res. 1996 Jun;109(3):367-76
references.pmid: 8817266
references.citation: J Neurosci. 1988 Aug;8(8):2928-37
references.pmid: 3411362
references.citation: Nat Neurosci. 2004 Sep;7(9):907-15
references.pmid: 15332089
references.citation: Nature. 2000 Oct 12;407(6805):742-7
references.pmid: 11048720
references.citation: J Neurophysiol. 1995 Feb;73(2):836-54
references.pmid: 7760138
references.citation: Neural Netw. 2009 Nov;22(9):1203-13
references.pmid: 19502004
references.citation: J Neurophysiol. 1968 Jan;31(1):14-27
references.pmid: 4966614
references.citation: Nat Rev Neurosci. 2000 Nov;1(2):125-32
references.pmid: 11252775
references.citation: J Neurosci. 1989 Jun;9(6):2080-102
references.pmid: 2723767
references.citation: Neuroscience. 1991;44(3):521-35
references.pmid: 1754050
references.citation: J Neurosci. 2002 Nov 15;22(22):9656-60
references.pmid: 12427820
references.citation: J Neurosci. 1982 Nov;2(11):1527-37
references.pmid: 7143039
references.citation: Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19486-91
references.pmid: 19047633
references.citation: J Neurosci. 2000 Oct 15;20(20):7807-15
references.pmid: 11027245
references.citation: J Neurophysiol. 2007 Dec;98(6):3600-13
references.pmid: 17913996
references.citation: J Neurosci. 2004 Sep 29;24(39):8551-61
references.pmid: 15456829
references.citation: J Neurosci. 1990 Jul;10(7):2039-58
references.pmid: 2376768
references.citation: J Neurosci. 1994 May;14(5 Pt 2):3208-24
references.pmid: 8182467
references.citation: Nature. 2002 Jun 27;417(6892):938-41
references.pmid: 12087402
references.citation: J Neurosci. 2007 May 9;27(19):5105-14
references.pmid: 17494696
references.citation: Exp Brain Res. 1998 Aug;121(3):285-99
references.pmid: 9746135
references.citation: J Neurophysiol. 2007 Dec;98(6):3321-9
references.pmid: 17928561
references.citation: Nature. 2004 Oct 14;431(7010):768-74
references.pmid: 15483597
references.citation: Curr Opin Neurobiol. 2003 Apr;13(2):225-31
references.pmid: 12744978
references.citation: Nat Neurosci. 2006 Nov;9(11):1404-11
references.pmid: 17028585
references.citation: J Neurophysiol. 1995 Jan;73(1):361-72
references.pmid: 7714578
references.citation: PLoS One. 2009;4(1):e4214
references.pmid: 19148302
references.citation: J Neurosci. 1997 Jan 1;17(1):409-19
references.pmid: 8987766
references.citation: Neural Netw. 2009 Nov;22(9):1224-34
references.pmid: 19525091
references.citation: Proc Natl Acad Sci U S A. 2000 Feb 29;97(5):2259-63
references.pmid: 10681435
references.citation: J Neurophysiol. 1993 Nov;70(5):2097-116
references.pmid: 8294972
references.citation: J Neurophysiol. 2001 Jun;85(6):2576-89
references.pmid: 11387402
references.citation: J Neurophysiol. 1992 Aug;68(2):528-41
references.pmid: 1527573
references.citation: Science. 1991 Jul 19;253(5017):287-91
references.pmid: 1857964
references.citation: Cold Spring Harb Symp Quant Biol. 1990;55:899-910
references.pmid: 2132866
references.citation: Nat Neurosci. 2005 Apr;8(4):498-504
references.pmid: 15768037
references.citation: J Neurosci. 2003 Oct 8;23(27):9032-45
references.pmid: 14534237
references.citation: Science. 1999 Sep 24;285(5436):2136-9
references.pmid: 10497133
references.citation: Eur J Neurosci. 1999 Dec;11(12):4433-45
references.pmid: 10594670
references.citation: Science. 2004 Jan 16;303(5656):380-3
references.pmid: 14726593
references.citation: Neuron. 2001 May;30(2):593-607
references.pmid: 11395017
references.citation: Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7534-8
references.pmid: 8052615
references.citation: J Neurosci. 1988 Aug;8(8):2913-27
references.pmid: 3411361
references.citation: J Neurophysiol. 2003 Jan;89(1):168-76
references.pmid: 12522169
references.citation: Nat Neurosci. 2000 Nov;3 Suppl:1192-8
references.pmid: 11127837
references.citation: Nat Rev Neurosci. 2004 Jul;5(7):532-46
references.pmid: 15208695
references.citation: Cereb Cortex. 1994 Nov-Dec;4(6):590-600
references.pmid: 7703686
references.citation: Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2909-14
references.pmid: 16473936
references.citation: Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3843-6
references.pmid: 8632977
references.citation: J Neurophysiol. 1999 Nov;82(5):2676-92
references.pmid: 10561437
references.citation: Trends Neurosci. 2004 Aug;27(8):496-503
references.pmid: 15271498
references.citation: Exp Brain Res. 2006 Jan;168(1-2):106-19
references.pmid: 16177830
references.citation: Nat Neurosci. 2003 Aug;6(8):882-90
references.pmid: 12872127
references.citation: J Neurosci. 2004 Oct 6;24(40):8662-71
references.pmid: 15470131
references.citation: Curr Opin Neurobiol. 2008 Dec;18(6):573-81
references.pmid: 19054663