Disruption of the Dorsolateral Prefrontal Cortex Facilitates the Consolidation of Procedural Skills

In explicit sequence learning tasks, an improvement in performance (skill) typically occurs after sleep—leading to the recent literature on sleep-dependent motor consolidation. Consolidation can also be facilitated during wakefulness if declarative knowledge for the sequence is reduced through a secondary cognitive task. Accordingly, declarative and procedural consolidation processes appear to mutually interact. Here we used TMS to test the hypothesis that functions in the dorsolateral prefrontal cortex (DLPFC) that support declarative memory formation indirectly reduce the formation of procedural representations. We hypothesize that disrupting the DLPFC immediately after sequence learning would degrade the retention or the consolidation of the sequence within the declarative memory system and thus facilitate consolidation within procedural memory systems, evident as wakeful off-line skill improvement. Inhibitory theta-burst TMS was applied to the left DLPFC (n = 10), to the right DLPFC (n = 10), or to an occipital cortical control site (n = 10) immediately after training on the serial reaction time task (SRTT). All groups were retested after eight daytime hours without sleep. TMS of either left or right DLPFC lead to skill improvements on the SRTT. Increase in skill was greater following right DLPFC stimulation than left DLPFC stimulation; there was no improvement in skill for the control group. Across all participants, free recall of the sequence was inversely related to the improvements in performance on the SRTT. These results support the hypothesis of interference between declarative and procedural consolidation processes and are discussed in the framework of the interactions between memory systems.

[1]  Scott T. Grafton,et al.  Motor sequence learning with the nondominant left hand , 2002, Experimental Brain Research.

[2]  S. Keele,et al.  The cognitive and neural architecture of sequence representation. , 2003, Psychological review.

[3]  R. P. Maguire,et al.  Cerebral activation related to implicit sequence learning in a Double Serial Reaction Time task , 2006, Brain Research.

[4]  Emanuele Lo Gerfo,et al.  Cortical networks of procedural learning: Evidence from cerebellar damage , 2007, Neuropsychologia.

[5]  Á. Pascual-Leone,et al.  Safety of Theta Burst Transcranial Magnetic Stimulation: A Systematic Review of the Literature , 2011, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[6]  L. Cohen,et al.  Modulation of motor learning and memory formation by non-invasive cortical stimulation of the primary motor cortex , 2011, Neuropsychological rehabilitation.

[7]  C. Caltagirone,et al.  Interference of Left and Right Cerebellar rTMS with Procedural Learning , 2004, Journal of Cognitive Neuroscience.

[8]  John C Rothwell,et al.  The effect of short-duration bursts of high-frequency, low-intensity transcranial magnetic stimulation on the human motor cortex , 2004, Clinical Neurophysiology.

[9]  J. Gabrieli,et al.  Direct comparison of neural systems mediating conscious and unconscious skill learning. , 2002, Journal of neurophysiology.

[10]  廣瀬雄一,et al.  Neuroscience , 2019, Workplace Attachments.

[11]  C. Ranganath,et al.  The Dorsolateral Prefrontal Cortex Contributes to Successful Relational Memory Encoding , 2007, The Journal of Neuroscience.

[12]  Scott T. Grafton,et al.  Functional Mapping of Sequence Learning in Normal Humans , 1995, Journal of Cognitive Neuroscience.

[13]  M. Hallett,et al.  Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior , 2000, Clinical Neurophysiology.

[14]  J. Rothwell,et al.  Effects of theta burst stimulation protocols on phosphene threshold , 2006, Clinical Neurophysiology.

[15]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[16]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[17]  Alfredo Berardelli,et al.  Phasic voluntary movements reverse the aftereffects of subsequent theta-burst stimulation in humans. , 2008, Journal of neurophysiology.

[18]  R. Stickgold,et al.  Practice with Sleep Makes Perfect Sleep-Dependent Motor Skill Learning , 2002, Neuron.

[19]  Karolina Janacsek,et al.  Predicting the future: from implicit learning to consolidation. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[20]  D. Willingham.  Systems of Memory in the Human Brain , 1997, Neuron.

[21]  Hillary D. Schwarb,et al.  Neural evidence of a role for spatial response selection in the learning of spatial sequences , 2009, Brain Research.

[22]  Steven W. Keele,et al.  Movement control in skilled motor performance. , 1968 .

[23]  R. Passingham,et al.  Active maintenance in prefrontal area 46 creates distractor-resistant memory , 2002, Nature Neuroscience.

[24]  John A. Detre,et al.  Using perfusion fMRI to measure continuous changes in neural activity with learning , 2006, Brain and Cognition.

[25]  Richard B. Ivry,et al.  Sleep-Dependent Consolidation of Contextual Learning , 2006, Current Biology.

[26]  Nitzan Censor,et al.  Using repetitive transcranial magnetic stimulation to study the underlying neural mechanisms of human motor learning and memory , 2010, The Journal of physiology.

[27]  K. Funke,et al.  Modulation of cortical inhibition by rTMS – findings obtained from animal models , 2011, The Journal of physiology.

[28]  Scott T. Grafton,et al.  Neural Substrates of Response-based Sequence Learning using fMRI , 2004, Journal of Cognitive Neuroscience.

[29]  U. Wagner,et al.  Patterns of Implicit Learning Below the Level of Conscious Knowledge , 2010 .

[30]  James B. Rowe,et al.  Working Memory for Location and Time: Activity in Prefrontal Area 46 Relates to Selection Rather than Maintenance in Memory , 2001, NeuroImage.

[31]  D J Povel,et al.  Structural factors in patterned finger tapping. , 1982, Acta psychologica.

[32]  E. Robertson.  The Serial Reaction Time Task: Implicit Motor Skill Learning? , 2007, The Journal of Neuroscience.

[33]  P. Goldman-Rakic,et al.  Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey , 1984, Neuroscience.

[34]  Katsuyuki Sakai,et al.  The prefrontal cortex and working memory: physiology and brain imaging , 2004, Current Opinion in Neurobiology.

[35]  Richard B. Ivry,et al.  Representational issues in motor learning: Phenomena and theory , 1996 .

[36]  D. Willingham,et al.  The Relation Between Implicit and Explicit Learning: Evidence for Parallel Development , 1999 .

[37]  P. Goldman-Rakic.  Cellular basis of working memory , 1995, Neuron.

[38]  M. Petrides.  Functional specialization within the dorsolateral frontal cortex for serial order memory , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[39]  J. Rothwell,et al.  Theta Burst Stimulation of the Human Motor Cortex , 2005, Neuron.

[40]  R. Seidler,et al.  Working memory capacity correlates with implicit serial reaction time task performance , 2011, Experimental Brain Research.

[41]  L R Squire,et al.  Dissociable properties of memory systems: differences in the flexibility of declarative and nondeclarative knowledge. , 1996, Behavioral neuroscience.

[42]  L. Squire,et al.  Learning about categories in the absence of memory. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[43]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[44]  C. Umilta,et al.  The use of transcranial magnetic stimulation in cognitive neuroscience: A new synthesis of methodological issues , 2011, Neuroscience & Biobehavioral Reviews.

[45]  Daniel B. Willingham,et al.  A Neuropsychological Theory of Motor Skill Learning , 2004 .

[46]  Edwin M Robertson,et al.  Inducing motor skill improvements with a declarative task , 2007, Nature Neuroscience.

[47]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[48]  Scott T. Grafton,et al.  Attention and stimulus characteristics determine the locus of motor-sequence encoding. A PET study. , 1997, Brain : a journal of neurology.

[49]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[50]  M. D’Esposito,et al.  The neural basis of the central executive system of working memory , 1995, Nature.

[51]  Edwin M Robertson,et al.  Off-Line Processing: Reciprocal Interactions between Declarative and Procedural Memories , 2007, The Journal of Neuroscience.