The roles of the caudate nucleus in human classification learning

Abstract

The caudate nucleus is commonly active when learning relationships between stimuli and responses or categories. Previous research has not differentiated between the contributions to learning in the caudate and its contributions to executive functions such as feedback processing. We used event-related functional magnetic resonance imaging while participants learned to categorize visual stimuli as predicting "rain" or "sun." In each trial, participants viewed a stimulus, indicated their prediction via a button press, and then received feedback. Conditions were defined on the bases of stimulus-outcome contingency (deterministic, probabilistic, and random) and feedback (negative and positive). A region of interest analysis was used to examine activity in the head of the caudate, body/tail of the caudate, and putamen. Activity associated with successful learning was localized in the body and tail of the caudate and putamen; this activity increased as the stimulus-outcome contingencies were learned. In contrast, activity in the head of the caudate and ventral striatum was associated most strongly with processing feedback and decreased across trials. The left superior frontal gyrus was more active for deterministic than probabilistic stimuli; conversely, extrastriate visual areas were more active for probabilistic than deterministic stimuli. Overall, hippocampal activity was associated with receiving positive feedback but not with correct classification. Successful learning correlated positively with activity in the body and tail of the caudate nucleus and negatively with activity in the hippocampus.

Figure 1.

Stimuli used in the experiment.

Figure 2.

Three-dimensional rendering of the eight striatal regions of interest, viewed from the left, from above, and from the front. Green, Body and tail of the caudate; blue, head of the caudate; yellow, putamen; red, ventral striatum. White lines indicate the planes of z = 0, x = 0, y = 0, and y = -20, as used in the brain atlas in the study by Talairach and Tournoux (1988). The putamen ROIs extended inferiorally to superiorally from z = -1 to z = 15, anteriorally to posteriorally from y = -15 to y = +15, and laterally from x = ±15 to ±33. Within the caudate nucleus, the border between the head and the body/tail ROIs was along an oblique plane angled at 45° from horizontal running between the lines defined by y = 0, z = 14 and y = 10, z = 24. The head of the caudate ROIs extended inferiorally to z = -1 and laterally from the ventricles to x = ±13. The body/tail of the caudate ROIs extended superiorally to z = 28, inferiorally in the body portion to z = 16, in the tail portion to z = -3, laterally from approximately x = 9 to x = 22 in the body region, and posteriorally to y = -38 at the tip of the tail. The ventral striatum ROI encompassed the nucleus accumbens and the most inferior portions of the caudate and putamen; it extended in the inferior-superior dimension from z = -2 to z = -10.

Figure 3.

The percentage correct across blocks for deterministic, probabilistic, and random stimuli, with correct defined as classifying the stimulus consistent with its dominant assignment, is shown.

Figure 4.

Percentage of signal change during classification (Det-CP and Prob-CP combined) and baseline trials in the eight striatal ROIs: right head (RH) and left head (LH) of the caudate, right ventral striatum (RV) and left ventral striatum (LV), right body and tail (RBT) and left body and tail (LBT) of the caudate, and right putamen (RP) and left putamen (LP).

Figure 5.

The percentage of signal change in the right and left body and tail of the caudate nucleus and right and left putamen across blocks for classification (Det-CP and Prob-CP combined) and baseline stimulus trials is shown.

Figure 6.

Percentage of signal change in the Ran-P and Ran-N conditions in the eight striatal ROIs: right head (RH) and left head (LH) of the caudate, right ventral striatum (RV) and left ventral striatum (LV), right left body and tail (RBT) and left body and tail (LBT) of the caudate, and right putamen (RP) and left putamen (LP).

Figure 7.

The percentage of signal change in the right and left head of the caudate and right and left ventral striatum across blocks for random stimuli receiving positive feedback and random stimuli receiving negative feedback (Ran-P and Ran-N) is shown.

Figure 8.

A, Areas of the left frontal pole that were more active in Det-CP than Prob-CP (positive t values; red-yellow scale) and areas of the left lingual gyrus that were more active in Prob-CP than Det-CP (negative t values; blue-green scale). B, Right hippocampal and left parahippocampal gyrus clusters that were more active in Ran-P than Ran-N (positive t values; redyellow scale).

Figure 9.

The percentage of signal change in the left frontal pole across blocks for deterministic (Det-CP), probabilistic (Prob-CP), and random (Ran-P) stimuli receiving positive feedback is shown.

Figure 10.

The percentage of signal change in the right hippocampus across blocks for random stimuli receiving positive feedback (Ran-P) and random stimuli receiving negative feedback (Ran-N) is shown.