The globus pallidus pars interna in goal-oriented and routine behaviors: Resolving a long-standing paradox

被引:26
作者
Piron, Camille [1 ,2 ,3 ]
Kase, Daisuke [1 ,2 ,3 ]
Topalidou, Meropi [1 ,2 ,4 ,5 ,6 ]
Goillandeau, Michel [1 ,2 ]
Orignac, Hugues [1 ,2 ]
Tho-Hai N'Guyen [1 ,2 ]
Rougier, Nicolas [1 ,2 ,4 ,5 ,6 ]
Boraud, Thomas [1 ,2 ,3 ,7 ]
机构
[1] Univ Bordeaux, UMR 5293, IMN, Bordeaux, France
[2] CNRS, UMR 5293, IMN, 146 Rue Leo Saignat, F-33076 Bordeaux, France
[3] CNRS, French Israeli Neurosci Lab, Bordeaux, France
[4] Bordeaux Sud Ouest, INRIA, Talence, France
[5] Univ Bordeaux, UMR 5800, LABRI, IPB, Talence, France
[6] CNRS, UMR 5800, LABRI, IPB, Talence, France
[7] CHU Bordeaux, IMN Clin, Bordeaux, France
关键词
primates; decision making; behavioral task; muscimol; habits; reinforcement learning; pallidotomy; DBS; DEEP BRAIN-STIMULATION; BASAL GANGLIA; PARKINSONS-DISEASE; MATCHING LAW; GENERALIZED DYSTONIA; SUBTHALAMIC NUCLEUS; STRIATUM; MOVEMENT; REPRESENTATIONS; LESIONS;
D O I
10.1002/mds.26542
中图分类号
R74 [神经病学与精神病学];
学科分类号
摘要
BackgroundThere is an apparent contradiction between experimental data showing that the basal ganglia are involved in goal-oriented and routine behaviors and clinical observations. Lesion or disruption by deep brain stimulation of the globus pallidus interna has been used for various therapeutic purposes ranging from the improvement of dystonia to the treatment of Tourette's syndrome. None of these approaches has reported any severe impairment in goal-oriented or automatic movement. MethodTo solve this conundrum, we trained 2 monkeys to perform a variant of a 2-armed bandit-task (with different reward contingencies). In the latter we alternated blocks of trials with choices between familiar rewarded targets that elicit routine behavior and blocks with novel pairs of targets that require an intentional learning process. ResultsBilateral inactivation of the globus pallidus interna, by injection of muscimol, prevents animals from learning new contingencies while performance remains intact, although slower for the familiar stimuli. We replicate in silico these data by adding lateral competition and Hebbian learning in the cortical layer of the theoretical model of the cortex-basal ganglia loop that provided the framework of our experimental approach. ConclusionThe basal ganglia play a critical role in the deliberative process that underlies learning but are not necessary for the expression of routine movements. Our approach predicts that after pallidotomy or during stimulation, patients should have difficulty with complex decision-making processes or learning new goal-oriented behaviors. (c) 2016 Movement Disorder Society
引用
收藏
页码:1146 / 1154
页数:9
相关论文
共 43 条
[1]   THE FUNCTIONAL-ANATOMY OF BASAL GANGLIA DISORDERS [J].
ALBIN, RL ;
YOUNG, AB ;
PENNEY, JB .
TRENDS IN NEUROSCIENCES, 1989, 12 (10) :366-375
[2]   PREPARATION FOR MOVEMENT - NEURAL REPRESENTATIONS OF INTENDED DIRECTION IN 3 MOTOR AREAS OF THE MONKEY [J].
ALEXANDER, GE ;
CRUTCHER, MD .
JOURNAL OF NEUROPHYSIOLOGY, 1990, 64 (01) :133-150
[3]   Separate neural substrates for skill learning and performance in the ventral and dorsal striatum [J].
Atallah, Hisham E. ;
Lopez-Paniagua, Dan ;
Rudy, Jerry W. ;
O'Reilly, Randall C. .
NATURE NEUROSCIENCE, 2007, 10 (01) :126-131
[4]   Bilateral lesions of the subthalamic nucleus induce multiple deficits in an attentional task in rats [J].
Baunez, C ;
Robbins, TW .
EUROPEAN JOURNAL OF NEUROSCIENCE, 1997, 9 (10) :2086-2099
[5]   MOTOR FUNCTION OF THE MONKEY GLOBUS-PALLIDUS .2. COGNITIVE ASPECTS OF MOVEMENT AND PHASIC NEURONAL-ACTIVITY [J].
BROTCHIE, P ;
IANSEK, R ;
HORNE, MK .
BRAIN, 1991, 114 :1685-1702
[6]   Pallidal surgery for the treatment of primary generalized dystonia: Long-term follow-up [J].
Cersosimo, Maria G. ;
Raina, Gabriela B. ;
Piedimonte, Fabian ;
Antico, Julio ;
Graff, Pablo ;
Micheli, Federico E. .
CLINICAL NEUROLOGY AND NEUROSURGERY, 2008, 110 (02) :145-150
[7]   Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control [J].
Daw, ND ;
Niv, Y ;
Dayan, P .
NATURE NEUROSCIENCE, 2005, 8 (12) :1704-1711
[8]  
DELONG MR, 1984, CIBA F SYMP, V107, P64
[9]   Motor Sequences and the Basal Ganglia: Kinematics, Not Habits [J].
Desmurget, Michel ;
Turner, Robert S. .
JOURNAL OF NEUROSCIENCE, 2010, 30 (22) :7685-7690
[10]   SOME PARAMETERS OF BEHAVIORAL-CONTRAST AND ALLOCATION OF INTERIM BEHAVIOR IN RATS [J].
DOUGAN, JD ;
MCSWEENEY, FK ;
FARMER, VA .
JOURNAL OF THE EXPERIMENTAL ANALYSIS OF BEHAVIOR, 1985, 44 (03) :325-335