On the benefits of not trying: brain activity and connectivity reflecting the interactions of explicit and implicit sequence learning

Abstract

Under certain circumstances, implicit, automatic learning may be attenuated by explicit memory processes. We explored the brain basis of this phenomenon in a functional magnetic resonance imaging (fMRI) study of motor sequence learning. Using a factorial design that crossed subjective intention to learn (explicit versus implicit) with sequence difficulty (a standard versus a more complex alternating sequence), we show that explicit attempts to learn the difficult sequence produce a failure of implicit learning and, in a follow-up behavioural experiment, that this failure represents a suppression of learning itself rather than of the expression of learning. This suppression is associated with sustained right frontal activation and attenuation of learning-related changes in the medial temporal lobe and the thalamus. Furthermore, this condition is characterized by a reversal of the fronto-thalamic connectivity observed with unimpaired implicit learning. The findings demonstrate a neural basis for a well-known behavioural effect: the deleterious impact of an explicit search upon implicit learning.

Figure 1

Experimental design. An alternating block design was used (30 s blocks alternating between SRT task and visual fixation). Subjects viewed a four-position array on a screen and, as a position became highlighted, pressed the appropriate button on a keypad. Two types of sequence were presented, each with or without instruction to try to discover the repeating sequence. Each sequence lasted consisted of 10 successive position, changing at one position per second. There were thus three presentations of a sequence within a 30 s block.

Figure 2

Reaction time data. The median reaction time was calculated for each sequence repetition and the mean of these was calculated to produce the average reaction time in each of the six blocks. These are presented above for the explicit standard SRT task (EsSRT) and the implicit standard SRT task (IsSRT) in the upper panel, and for the explicit alternating SRT task (EaSRT) and the implicit alternating SRT task (IaSRT) in the lower panel.

Figure 3

Time-indepentdent activations EaSRT versus IaSRT. A maximum intensity projection (MIP) of regions showing greater activation when explicitly trying to learn the sequence during the alternating SRT task, compared with when they were not is shown thresholded at P<0.001, uncorrected for multiple comparisons (right PFC, circled, survives FDR corrected threshold of P<0.05). MIPs are viewed from the right (top left panel), from behind (top right) and from above (bottom left). In addition, the bottom right panel shows a plot of the parameter estimates for a voxel in right PFC (44, 20, 12) for each of the four task conditions compared with its alternating visual fixation baseline. While each task produced time-independent activation in this regions, this was greater in the explicit conditions and maximal in EaSRT.

Figure 4

Learning-related decreases in activation, all sequence learning conditions versus random implicit condition. The upper panel shows a maximum intensity projection of the SPM(t) for regions showing a time-dependent increase in (activation relative to recurring visual fixation) that are significantly greater than any seen during random implicit condition. Left MTL showed a significant effect (FDR < 0.05) and left caudate showed a trend towards a decrease (FDR = 0.08). The SPM is thresholded at P < 0.01 (uncorrected for multiple comparisons) in order to show the small trend towards additional activations on the right. The lower panel shows superimpositions of MTL (left: image sectioned at coordinates x, y, z = −30, −32, −12) and caudate activations (right: x, y, z = −10, 20, 0) on a representative structural MRI rendered into the same anatomical space.

Figure 5

Condition-specific differences in learning-related activation. Upper panel: comparison of EaSRT with IaSRT conditions. Left MTL shows an anttenuation of learning-related reductions in activation when subjects are explicitly trying to learn the sequence. The region showing this interaction is superimposed upon a representative MRI (x, y, z = −30, −30, −16). The inlaid plot shows averaged levels of activity in this region (relative to the fixation condition) for the standard SRT tasks (upper plot) and the alternating SRT (lower plot). The lower plot reflects the significant attenuation of learning-related decrease when explicit instructions are given. Lower panel: posterior thalamic differences in learning-related activation. Activation differences are shown for the direct comparison between EaSRT and IaSRT and are superimposed upon a standard MRI (x, y, z = −22, −24, 4). The accompanying plots shows a time-dependent decrease in activation for this regions during EaSRT. This effect was not seen in any of the other conditions, which showed trends in the opposite direction.

Figure 6

Regions showing condition-dependent differences in functional connectivity with right PFC (EaSRT versus IaSRT). The upper panel shows the maximum intensity projection (thresholded at P < 0.01, uncorrected for multiple comparisons) produced by the comparison between frontal correlations (relative to visual fixation) during EaSRT and IaSRT. The thalamus shows bilaterally a significant difference in task-dependent frontal connectivity, being positively correlated with right PFC during EaSRT and negatively correlated during IaSRT. The lower panel shows the results of the same comparison rendered onto a MRI in standard space (x, y, z = 16, −14, 10).

Figure 7

Data from behavioural study (experiment 2). Learning phase: the data are presented as for RTs in Figure 2. Median RTs for the (alternate) sequence elements across each set of three sequence repetitions was averaged across the twelve subjects. Data for the IaSRT and EaSRT tasks are shown with standard error bars. Re-exposure to sequence post-learning: again, for each subject, we subtracted RTs to each non-sequence element from RT to the neighbouring sequence element to produce a measure of the amount that had been learned. Median values for the first reexposure were calculated for each subject and are presented for re-exposure following IaSRT and EaSRT together with standard error bars. The negative value following IaSRT indicates the impact of prior learning. No such effect was significant following EaSRT.