Off-line processing: reciprocal interactions between declarative and procedural memories

Abstract

The acquisition of declarative (i.e., facts) and procedural (i.e., skills) memories may be supported by independent systems. This same organization may exist, after memory acquisition, when memories are processed off-line during consolidation. Alternatively, memory consolidation may be supported by interactive systems. This latter interactive organization predicts interference between declarative and procedural memories. Here, we show that procedural consolidation, expressed as an off-line motor skill improvement, can be blocked by declarative learning over wake, but not over a night of sleep. The extent of the blockade on procedural consolidation was correlated to participants' declarative word recall. Similarly, in another experiment, the reciprocal relationship was found: declarative consolidation was blocked by procedural learning over wake, but not over a night of sleep. The decrease in declarative recall was correlated to participants' procedural learning. These results challenge the concept of fixed independent memory systems; instead, they suggest a dynamic relationship, modulated by when consolidation takes place, allowing at times for a reciprocal interaction between memory systems.

Figure 1.

Experimental design. A, In the first experiment, we examined the capacity of declarative learning to disrupt procedural consolidation. Participants learned a motor skill and performed a secondary task, and 12 h later their motor skill was retested. We contrasted the effects of two secondary tasks, word-list learning versus vowel counting, on procedural consolidation over wake, and then examined whether word-list learning had a differential capacity to interfere with procedural consolidation over wake or a night of sleep. The difference between motor skill at testing (skill₁) and retesting (skill₂) provided a measure of procedural consolidation) (skill₂ − skill₁) (Walker et al., 2002; Robertson et al., 2004b; Cohen et al., 2005; Spencer et al., 2006). B, In the second experiment, we examined the capacity of motor skill learning to disrupt declarative consolidation. Participants learned a list of words and performed a secondary task, and 12 h later their word recall was retested. We contrasted the effects of two secondary tasks, motor skill learning (i.e., SRTT) versus motor performance (i.e., RRTT), on declarative consolidation and examined whether motor skill learning had a differential capacity to interfere with declarative consolidation over wake or a night of sleep. The difference between initial (recall₁) and subsequent recall (recall₂) of the word list provided a measure of declarative consolidation (recall₂ − recall₁) (Ellenbogen et al., 2006).

Figure 2.

In experiment 1, after the acquisition of a motor skill (8:00 A.M., SRTT, skill₁; gray bars ± SEM) participants performed a secondary task (vowel counting vs word-list learning) and were retested 12 h later on the motor skill (8:00 P.M., skill₂, black bars ± SEM). Over the interval, there was a general improvement in performance: response times to the random trials (gray triangle ± SEM) preceding the sequential trials fell significantly (vowel-counting task, paired t test, t₍₉₎ = 4.6, p = 0.001; word-list learning task, paired t test, t₍₉₎ = 4.0, p = 0.003). This fall in response time did not differ significantly between the groups (unpaired t test, t₍₁₈₎ = 0.04; p = 0.966). A similar general performance improvement was observed in the sequential (square ± SEM) and subsequent random response times (circle ± SEM) after word-list learning (sequential, paired t test, t₍₉₎ = 2.39, p = 0.04; random, paired t test, paired t test, t₍₉₎ = 6.23, p < 0.001). Thus, with little change in the differential between the sequential and subsequent random response times, which is a widely used measure of skill in this motor task, there were no significant off-line skill improvements after word-list learning (−22 ± 14 ms; paired t test, t₍₉₎ = 1.589; p = 0.146) (Nissen and Bullemer, 1987; Willingham et al., 1989; Willingham and Goedert-Eschmann, 1999). In contrast, there was a decrease in sequential response times (paired t test, t₍₉₎ = 4.13; p = 0.002), but no significant change in the random response times (paired t test, t₍₉₎ < 1; p = 0.985) after vowel counting. The absence of a decrease in these latter random response times indicated the off-line development of skill (20 ± 7 ms; paired t test, t₍₉₎ = 2.86; p = 0.019). The development of skill encourages participants to play out the sequence even when this is inappropriate during the unexpected introduction of random trials after the sequential trials (postrandom trials). This proactive interference from the sequential onto the random trials increases as skill increases, and causes an increase in postrandom response times whereas the sequential response times decrease (Robertson, 2007). The increase in postrandom response times counteracts the general improvement in task performance, causing there to be no change in the postrandom response times. Thus, off-line skill improvements, which normally develop over wake, were present after vowel counting, but were blocked by word-list learning (Robertson et al., 2004b; Cohen et al., 2005; Press et al., 2005).

Figure 3.

A, In experiment 1, off-line skill improvements were differentially affected by the performance of another task immediately after skill acquisition: vowel counting allowed off-line skill improvements to develop as normal (gray bar ± SEM), whereas word-list learning prevented the development of significant off-line improvements (black bar ± SEM). B, The decline in motor skill after word-list learning was correlated with participants' word recall (r = 0.767; F = 11.42; p = 0.01). In contrast, there was no relationship between the declarative component of the SRTT (free recall of the 12-item sequence) and word recall. Thus, the effect of word-list learning on motor skill performance was not mediated via an influence of word-list learning on the declarative component of the SRTT. Instead, there was a direct effect of declarative learning on procedural consolidation.

Figure 4.

A, In experiment 1, off-line skill improvements developed over a night of sleep (8:00 P.M. to 8:00 A.M.) even although participants had earlier learned a word list (21 ± 8 ms; paired t test, t₍₉₎ = 2.799; p = 0.021). Producing this off-line skill improvement was a decrease in sequential response times (square ± SEM; paired t test, t₍₉₎ = 2.785; p = 0.021) combined with no significant change in the random response times (circle ± SEM; paired t test, t₍₉₎ < 1; p = 0.363). B, After word-list learning, off-line skill improvements were blocked over wake but developed over a night of sleep (bars ± SEM). This differential pattern cannot be attributed to changes in the expression of skill at particular times of day. There was no significant difference in motor skill between the groups at the initial testing (8:00 A.M. vs 8:00 P.M.). Similar off-line skill improvements are expressed at 8:00 A.M. and 8:00 P.M. after a night of sleep and a day awake, respectively (Robertson et al., 2004b, 2005; Cohen et al., 2005; Spencer et al., 2006). Furthermore, off-line skill improvements can be expressed at 8:00 P.M., after an interval of wake, when participants counted vowels within nonsense letter strings immediately after motor skill learning. Thus, declarative learning has a differential capacity to block procedural consolidation over wake and a night of sleep.

Figure 5.

In experiment 2, after word-list learning (gray bars ± SEM), participants immediately performed another task (random visually guided response vs motor skill learning), which had a differential effect on their later word recall (black bars ± SEM). Participants' word recall was maintained over wake after they made a series of random visually guided responses (0 ± 0.4 change in word recall; paired t test, t₍₉₎ < 0.001; p > 0.99), whereas there was a significant decrease in word recall after participants learned a motor skill (−1.6 ± 0.3 words; paired t test, t₍₉₎ = 5.237; p = 0.001). Thus, declarative consolidation can be blocked by motor skill learning.

Figure 6.

A, In experiment 2, declarative consolidation, as measured by a change in word recall between initial testing and later retesting, was differentially affected by the task performed immediately after initial word-list learning. Word recall was maintained after participants performance of a random series of visually guided movements (gray bar ± SEM). In contrast, declarative consolidation was blocked after participants learned a motor skill (black bar ± SEM). This disruption to declarative consolidation lead to a decrease in word recall over wake. B, The decline in word recall after motor skill learning was correlated with participants' acquired skill (r = 0.767; F = 11.42; p = 0.01). In contrast, there was no relationship between the declarative component of the SRTT (free recall of the 12-item sequence) and word recall. This implies that the declarative component of the SRTT did not influence word recall. Instead, there was a direct effect of motor skill learning on declarative consolidation.

Figure 7.

A, In experiment 2, word recall was maintained over a night of sleep despite participants having earlier learned a motor skill (0.1 ± 0.3 words; paired t test, t₍₉₎ = 0.361; p = 0.726; bars show mean ± SEM). B, Declarative consolidation, as measured by a change in word recall over wake or a night of sleep, was differentially effected by previous motor skill learning. Word recall fell over wake after motor skill learning, indicating a disruption of declarative consolidation (gray bar ± SEM). In contrast, word recall was maintained over a night of sleep (black bar ± SEM). This differential pattern cannot be attributed to a diurnal effect on word recall. There was no significant difference in initial recall between the groups (8:00 A.M. vs 8:00 P.M.). Furthermore, maintained recall could be expressed at 8:00 P.M., after an interval of wake, when participants made random visually guided responses immediately after initial word-list learning (dark gray bar ± SEM). Thus, motor skill learning has a differential capacity to block declarative consolidation over wake and a night of sleep.

Figure 8.

The biological infrastructure that may account for our observations. A, Memory systems may interact over wake because of direct or indirect connections. The indirect connections may arise from brain areas, such as the prefrontal cortex, controlling or receiving processing from otherwise distinct memory systems (Poldrack et al., 2001; Voermans et al., 2004). B, Alternatively, the processing of declarative and procedural memories may engage similar or at least partially overlapping neural circuits. Previous work has shown some overlap between the processing of declarative and procedural memories (Curran, 1997; Schendan et al., 2003; Walker et al., 2005). Such neuronal overlap could account for the behavioral interference between declarative and procedural processing over wake. In contrast, over sleep, memory systems cease to interact. C, Potentially, this is because of a decrease in the functional connectivity among brain areas (Massimini et al., 2005). This would allow declarative and procedural systems to operate as independent memory systems. D, Alternatively, a change in brain state from wake to sleep may open up independent pathways for both procedural and declarative consolidation. This would require, as has been shown in some previous studies that differential mechanisms support consolidation over wake and sleep (Cohen et al., 2005; Robertson et al., 2005; Robertson and Cohen, 2006). The neuronal circuits engaged over wake may have the property of allowing interactions between memory systems whereas a differential set of circuits, engaged over sleep, may support independent memory processing.