Failure to consolidate the consolidation theory of learning for sensorimotor adaptation tasks

Abstract

An influential idea in human motor learning is that there is a consolidation period during which motor memories are transformed from a fragile to a permanent state, no longer susceptible to interference from new learning. The evidence supporting this idea comes from studies showing that the motor memory of a task (A) is lost when an opposing task (B) is experienced soon after, but not if sufficient time is allowed to pass (approximately 6 hr). We report results from three laboratories challenging this consolidation idea. We used an ABA paradigm in the context of a reaching task to assess the influence of experiencing B after A on the retention of A. In two experiments using visuomotor rotations, we found that B fully interferes with the retention of A even when B is experienced 24 hr after A. Contrary to previous reports, in four experiments on learning force fields, we also observed full interference between A and B when they are separated by 24 hr or even 1 week. This latter result holds for both position-dependent and velocity-dependent force fields. For both the visuomotor and force-field tasks, complete interference is still observed when the possible affects of anterograde interference are controlled through the use of washout trials. Our results fail to support the idea that motor memories become consolidated into a protected state. Rather, they are consistent with recent ideas of memory formation, which propose that memories can shift between active and inactive states.

Figure 1.

Adaptation to visuomotor rotations. Curves show mean angular error as a function of block on different days. The height of the shaded areas represents ±1 SE. For clarity, we have shaded the area formed by joining confidence intervals between adjacent blocks. The top panel shows results for the control group who adapted to the same visuomotor rotation (A) on days 1 and 3. The bottom panels show results for the test group who also adapted to the opposing visuomotor rotation (B) on day 2.

Figure 2.

Adaptation to visuomotor rotations with washout trials. Curves show mean angular error as a function of block on different days. Curves to the left of the dashed vertical line show performance in null trials; those to the right show adaptation to the visuomotor rotation. The height of the shaded areas represents ±1 SE. The top panel shows results for the control group who adapted to the same visuomotor rotation (A) on days 1-3. The bottom panels show results for the test group who also experienced A on days 1 and 3 but adapted to the opposing visuomotor rotation (B) on day 2.

Figure 3.

Adaptation to position-dependent force fields. Curves show mean perpendicular distance as a function of block on different days. The height of the shaded areas represents ±1 SE. The top panel shows results for the control group who adapted to the same force field (A) on days 1 and 3. The middle and bottom panels show results for the 5 min test group and the 24 hr test group who also adapted to the opposing force field (B) either 5 min after A on day 1 or on day 2, respectively.

Figure 4.

Adaptation to velocity-dependent force fields. Curves show mean area enclosed by the hand path as a function of block on different days. The height of the shaded areas represents ±1 SE. The left panel shows results for the 5 min test group who adapted to opposing force fields (A and then B) separated by 5 min on day 1 and then were retested on A on day 2. The middle panels show results for the 24 hr control and test groups who adapted to A on day 1 and were retested on A 2 d later. The 24 hr test group also adapted to the opposing force field B on day 2. The right panels show results for the 1 week control and test groups who adapted to A on day 1 and were retested on A 2 weeks later. The 1 week test group also adapted to the opposing force field B a week after first adapting to A on day 1.

Figure 5.

Adaptation to velocity-dependent force fields with the arm supported. Curves show mean area enclosed by the hand path as a function of block on different days. The height of the shaded areas represents ±1 SE. The top panel shows results for the control group who trained on null trials on day 1 and then adapted to the same force field A on days 2 and 4. The bottom panel shows results for the test group who also adapted to the opposing force field B on day 3.

Figure 6.

Adaptation to velocity-dependent force fields with the arm supported. Curves in the left panels show mean area enclosed by the hand path as a function of block on different days. Curves in the right panels show the vector correlation measure (see Materials and Methods for details) as a function of block on different days. Curves to the left of the dashed vertical line show performance in null trials performed at the start of each session. The height of the shaded areas represents ±1 SE. The top panel shows results for the control group who adapted to the same force field A on days 2 and 4 and experienced a full set of null trials on day 3. The bottom panel shows results for the test group who adapted to A on days 2 and 4 and the opposing force field B on day 3. Both groups trained on a full set of null trials on day 1 (data not shown).