The differential role of premotor frontal cortex and basal ganglia in motor sequence learning: evidence from focal basal ganglia lesions

Abstract

There has been a growing interest in the differential role of various neural structures in implicit learning processes. The goal of our study was to clarify how focal lesions restricted to the basal ganglia interfere with different aspects of implicit visuo-motor sequence learning. A version of the Serial Reaction Time Task (SRTT) of Nissen and Bullemer using a 12-trial sequence was administered. A total of 20 subjects with focal basal ganglia lesions caused by ischemic or hemorrhagic infarction and 20 matched control subjects participated in this study. The results indicate that subjects with focal basal ganglia lesions showed unimpaired implicit learning of a 12-item motor sequence. Subjects with basal ganglia lesions, however, had more difficulties improving their general proficiency with the reaction-time task independent of sequence-specific learning. We observed a tendency toward smaller regional volumes in the cerebellum and left pre-supplementary motor area (pre-SMA) of subjects with basal ganglia lesions. Smaller cerebellar and pre-SMA volumes were related to lower implicit learning performance in the lesion group. The size of lesions in the basal ganglia was not related to sequence-specific implicit learning but had a significant influence on subjects' general proficiency for execution of the reaction-time task. We propose that implicit learning is achieved by a distributed network of cortical and subcortical structures. The basal ganglia seem to be responsible for adjusting to the general requirements of a task rather than for learning specific associations between stimuli that might be accomplished by premotor frontal areas and the cerebellum instead.

Figure 1

Magnetic resonance scan of subject no. 102 of the basal ganglia group, showing an infarction involving parts of both the caudate nucleus and the putamen.

Figure 2

(A) Schematic representation of lesion location in the subgroup of basal ganglia subjects (group 1A) with additional lesions in frontal motor areas superimposed on a sagittal slice of a control subject and (B) sagittal slice of the same control subject showing segmented volumes of the pre-SMA and SMA-proper; (Pre-SMA) plane A–plane B; (SMA-proper) plane B–plane C; (CC) corpus callosum; (PaCS) paracentral sulcus; (PCS) medial part of the precentral sulcus.

Figure 3

(A) Mean reaction times across blocks of basal ganglia subjects and controls in the SRTT. In blocks 1 and 6 the sequence of stimuli was random (R). Block 2–5, 7, and 8 contained a 12-item repeating sequence. (B) Mean reaction times across blocks of basal ganglia subjects with (group 1A) and without (group 1B) frontal lacunar lesions and control subjects.

Figure 4

(A) Relationship between lesion size in the basal ganglia and general RT improvement in the SRTT (r = −0.52; P = 0.022) for the basal ganglia group. (B) Relationship between volume of the left pre-SMA and sequence-specific implicit learning in the SRTT (r = 0.56; P = 0.029; partial correlation coefficient adjusted for total brain volume) for the basal ganglia group. (C) Relationship between volume of the cerebellum and sequence-specific implicit learning in the SRTT (r = 0.73; P = 0.002; partial correlation coefficient adjusted for total brain volume) for the basal ganglia group.