The Journal of Neuroscience, October 5, 2005 • 25(40):9067–9068 • 9067

Journal Club

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Motor Consolidation, Night and Day

Valeria Della-Maggiore Neuropsychology/Cognitive Neuroscience Unit, Montreal Neurological Institute, Montreal, Quebec, Canada H3A 2B4 Review of Robertson et al. (http://www.jneurosci.org/cgi/content/full/25/27/6372)

In neuroscience, the term consolidation mechanism, performance would be simi- Stickgold, 2004). However, neither study traditionally refers to the processes larly affected by disrupting M1 function was originally designed to address off-line through which newly acquired, labile regardless of the time of interference. learning during the daytime. By using the stabilize. However, in addition They applied repetitive pulses of trans- implicit version of the SRTT, Robertson et to being preserved, performance can be cranial magnetic stimulation (rTMS) al. (2005) showed that memory enhance- enhanced in the absence of practice (i.e., over M1 immediately after practice ment can also occur during the day and “off-line”). Improvements in perfor- either at 8 A.M. or at 8 P.M. and reas- can be prevented by interfering with M1 mance beyond practice have been re- sessed performance after a 12 h interval function within a narrow time interval. ported for learning sequences of finger [Robertson et al. (2005), their Fig. 1 In addition, the results of this study of- movements either explicitly (when sub- (http://www.jneurosci.org/cgi/content/ fer significant insight into the role of the jects are aware of the sequence) or implic- full/25/27/6372/FIG1)]. The results re- primary in learn- itly (when subjects are unaware of the se- vealed a distinct impairment of off-line ing. Increased M1 activity has been con- quence). However, whereas increases in learning when rTMS was applied at 8 sistently reported during the acquisition performance for sequences learned ex- A.M., but not at 8 P.M. [Robertson et al. of motor sequences in the SRTT (Grafton plicitly develop exclusively overnight (2005), their Fig. 2 (http://www.jneurosci. et al., 1995). Yet the fact that learning of- (Walker et al., 2002), off-line learning for org/cgi/content/full/25/27/6372/FIG2)]. ten transfers to other effectors questions sequences learned implicitly also occurs This effect was location and time specific. whether M1 contributes directly to the during the day (Robertson et al., 2004). Interestingly, the application of rTMS at 10 formation of motor memories or simply These findings offer the intriguing possi- A.M. did not impair performance, suggest- reflects from higher-order corti- bility that consolidation of memories ac- ing that the contribution of M1 to off-line ces that encode the skill at a more abstract quired explicitly may be sleep dependent, learning was restricted to a narrow time level (Grafton et al., 1998). The inhibitory whereas consolidation of memories ac- window of Ͻ2 h [Robertson et al. (2005), effect of rTMS opens up the possibility quired implicitly may just depend on their Fig. 3 (http://www.jneurosci.org/ that M1 is directly involved in motor time. cgi/content/full/25/27/6372/FIG3)]. , and is consistent In their Journal of Neuroscience article, The study by Robertson et al. (2005) with the notion of parallel levels of repre- Robertson et al. (http://www.jneurosci. has some important implications for the sentation within the nervous system. org/cgi/content/full/25/27/6372) address understanding of memory consolidation. The study has some caveats worth not- this possibility experimentally by interfer- Primarily, it replicates previous findings ing, however. Based on their findings, the ing with neural activity of the primary demonstrating that off-line learning of authors conclude that different mecha- motor cortex (M1) after implicit learning implicitly acquired skills occurs both dur- nisms involving M1 may engage during on the serial reaction-time task (SRTT). ing the day and during the night, support- the day and overnight. They propose two The authors reasoned that, if off-line ing the hypothesis that memory consoli- possible explanations for the behavioral learning was supported by a unique dation is modulated by awareness. dissociation induced by TMS, both de- Furthermore, it suggests that the consoli- pendent on sleep. However, overnight Received Aug. 5, 2005; revised Aug. 18, 2005; accepted Aug. 26, 2005. dation of implicitly acquired skills may be changes in memory consolidation do not Correspondence should be addressed to Valeria Della-Maggiore, influenced by the time of day at which the necessarily reflect sleep-related consolida- Neuropsychology/Cognitive Neuroscience Unit, Montreal Neurological skill was learned. This finding contradicts tion. Neither the effect of sleep depriva- Institute, Montreal, Quebec, Canada H3A 2B4. E-mail: valeria@ bic.mni.mcgill.ca. a recent hypothesis stating that memories tion nor the effect of sleep induction dur- DOI:10.1523/JNEUROSCI.3296-05.2005 are stabilized during the day and en- ing the daytime was evaluated here. Copyright©2005SocietyforNeuroscience 0270-6474/05/259067-02$15.00/0 hanced during the night (Walker and Moreover, the possibility that improve- 9068 • J. Neurosci., October 5, 2005 • 25(40):9067–9068 Della-Maggiore • Journal Club ments in performance may have occurred circadian modulation of synaptic trans- the motor cortex in off-line learning and while subjects were still awake (on average mission cannot be completely excluded. will stimulate additional research in the 3 h before bedtime) was not examined. In addition, one might question fields of motor learning and memory Thus, the idea that the differential effect of whether the similarity in the level of per- consolidation. rTMS on performance is based on sleep, formance observed at test (8 A.M.) and rather than time of day, may require addi- retest (12 h later) supports the proposal References Grafton S, Hazeltine E, Ivry R (1995) Functional tional study. that consolidation of off-line learning (memory enhancement) is mechanisti- anatomy of in normal The authors dismiss a circadian . J Cogn Neurosci 7:497–510. rhythm in cortical excitability as a source cally different from that associated with Grafton ST, Hazeltine E, Ivry RB (1998) Ab- for the behavioral dissociation. This inter- skill acquisition (memory stabilization). stract and effector-specific representations of The magnitude of the inhibitory effect of motor sequences identified with PET. J Neu- pretation rests on the lack of a statistically rTMS on motor cortical excitability de- rosci 18:9420–9428. significant difference in the resting motor pends on the parameters of choice. Thus, Robertson EM, Pascual-Leone A, Press DZ threshold as assessed exclusively before longer exposure times and/or suprath- (2004) Awareness modifies the skill-learning benefits of sleep. Curr Biol 14:208–212. practice. Although the motor threshold is reshold stimulation could potentially in- a reliable measure of cortical excitability, Robertson EM, Press DZ, Pascual-Leone A fluence memory retention through retro- (2005) Off-line learning and the primary mo- it likely reflects axonal excitability rather active interference, which would be tor cortex. J Neurosci 25:6372–6378. than synaptic transmission, which can be inconsistent with the authors’ proposal. Walker MP, Stickgold R (2004) Sleep-dependent assessed using other measures (e.g., in- This paper raises the intriguing possi- learning and memory consolidation. put–output motor-evoked potential bility that consolidation of procedural 44:121–133. curve, intracortical inhibition/facilita- Walker MP, Brakefield T, Morgan A, Hobson JA, motor skills acquired implicitly may be Stickgold R (2002) Practice with sleep makes tion). Given that the effect of rTMS on influenced by the time of acquisition. The perfect: sleep-dependent motor skill learning. cortical excitability was not examined, a results offer support for an active role of Neuron 35:205–211.