The centre of the brain: topographical model of motor, cognitive, affective, and somatosensory functions of the basal ganglia

Abstract

The basal ganglia have traditionally been viewed as motor processing nuclei; however, functional neuroimaging evidence has implicated these structures in more complex cognitive and affective processes that are fundamental for a range of human activities. Using quantitative meta-analysis methods we assessed the functional subdivisions of basal ganglia nuclei in relation to motor (body and eye movements), cognitive (working-memory and executive), affective (emotion and reward) and somatosensory functions in healthy participants. We document affective processes in the anterior parts of the caudate head with the most overlap within the left hemisphere. Cognitive processes showed the most widespread response, whereas motor processes occupied more central structures. On the basis of these demonstrated functional roles of the basal ganglia, we provide a new comprehensive topographical model of these nuclei and insight into how they are linked to a wide range of behaviors.

Keywords: Activation Likelihood Estimate method; caudate; functional subdivision; globus pallidus; putamen.

Figure 1

Source datasets. (a) Number of fMRI studies that reported activity on basal ganglia and passed selection criteria as a function of year, (b) the distribution of datasets, and (c) number of foci that contributed to the analysis of each functional category. A single contrast from each study was selected for a category; in a few instances two contrasts were selected and entered in different categories (e.g., a contrast for reward and working‐memory categories; see Table 1 for more details on functional categorization of contrast and selection).

Figure 2

Brain maps demonstrating significant concordance across studies centered over the peak ALE value for each category. A voxel‐wise likelihood of activation was determined using false discovery rate (FDR) q = 0.001 multiple comparison control. Left = Left.

Figure 3

Conjunction display of ALE maps showing concordance over basal ganglia nuclei for motor, cognitive, and affective functions. A voxel‐wise likelihood of activation was determined using false discovery rate (FDR) q = 0.001 multiple comparison control. Left = Left.

Figure 4

Laterality indices for basal ganglia structures. Region of interest masks were applied to the thresholded ALE maps and hemispheric dominance was calculated for each region. Laterality index (LI = [Left – Right]/[Left + Right]) of >0.20 was deemed left dominance and <−0.20 right dominance, values in between were considered bilateral. Bars represent proportion of activity in each hemisphere.

Figure 5

Topographical model of the functions of the basal ganglia. We illustrate the basal ganglia structures in a schematic representation. Using color codes we illustrate (a) basal ganglia regions concordant across studies and (b) hemispheric dominance for each functional category; thicker stripes indicate larger hemispheric contribution. Left = Left.