Sleep is required for improving reaction times after training on a procedural visuo-motor task

Sleep has been found to enhance consolidation of many different forms of memory. However in most procedural tasks, a sleep-independent, fast learning component interacts with slow, sleep-dependent improvements. Here, we show that in humans a visuo-motor saccade learning task shows no improvements during training, but only during a delayed recall testing after a period of sleep. Subjects were trained in a prosaccade task (saccade to a visual target). Performance was tested in the prosaccade and the antisaccade task (saccade to opposite direction of the target) before training, after a night of sleep or sleep deprivation, after a night of recovery sleep, and finally in a follow-up test 4 weeks later. We found no immediate improvement in saccadic reaction time (SRT) during training, but a delayed reduction in SRT, indicating a slow-learning process. This reduction occurred only after a period of sleep, i.e. after the first night in the sleep group and after recovery sleep in the sleep deprivation group. This improvement was stable during the 4-week follow-up. Saccadic training can thus induce covert changes in the saccade generation pathway. During the following sleep period, these changes in turn bring about overt performance improvements, presuming a learning effect based on synaptic tagging.

[1]  W. Heide,et al.  Combined deficits of saccades and visuo-spatial orientation after cortical lesions , 1998, Experimental Brain Research.

[2]  Robert Stickgold,et al.  Cerebral Cortex doi:10.1093/cercor/bhi043 The Functional Anatomy of Sleep-dependent Visual Skill Learning , 2005 .

[3]  R. Boch,et al.  Express-saccades of the monkey: Effect of daily training on probability of occurrence and reaction time , 2004, Experimental Brain Research.

[4]  Manuel Schabus,et al.  Sleep transforms the cerebral trace of declarative memories , 2007, Proceedings of the National Academy of Sciences.

[5]  Andreas Sprenger,et al.  Differential effects of sleep deprivation on saccadic eye movements. , 2005, Sleep.

[6]  J. Hobson,et al.  Visual Discrimination Task Improvement: A Multi-Step Process Occurring During Sleep , 2000, Journal of Cognitive Neuroscience.

[7]  J. Born,et al.  Sleep inspires insight , 2004, Nature.

[8]  J. Born,et al.  Sleep after learning aids memory recall. , 2006, Learning & memory.

[9]  A. Rechtschaffen,et al.  A manual of standardized terminology, technique and scoring system for sleep stages of human subjects , 1968 .

[10]  P. Maquet,et al.  Neural correlates of perceptual learning: A functional MRI study of visual texture discrimination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[11]  A. Radant,et al.  Human oculomotor function: Reliability and diurnal variation , 1995, Biological Psychiatry.

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

[13]  Liat Kishon-Rabin,et al.  A latent consolidation phase in auditory identification learning: time in the awake state is sufficient. , 2005, Learning & memory.

[14]  A. Karni,et al.  Daytime sleep condenses the time course of motor memory consolidation , 2007, Nature Neuroscience.

[15]  B. Fischer,et al.  The role of fixation and visual attention in the occurrence of express saccades in man , 2004, European archives of psychiatry and neurological sciences.

[16]  Leslie G. Ungerleider,et al.  Experience-dependent changes in cerebellar contributions to motor sequence learning , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[17]  W. Singer,et al.  Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex , 1992, Brain Research.

[18]  R. Morris,et al.  Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas , 2006, The European journal of neuroscience.

[19]  D P Munoz,et al.  Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. , 1996, Journal of neurophysiology.

[20]  R. Krauzlis.  The Control of Voluntary Eye Movements: New Perspectives , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[21]  Justin C. Hulbert,et al.  Interfering with Theories of Sleep and Memory: Sleep, Declarative Memory, and Associative Interference , 2006, Current Biology.

[22]  C. Pierrot-Deseilligny,et al.  Eye movement control by the cerebral cortex , 2004, Current opinion in neurology.

[23]  J. Born,et al.  Early sleep triggers memory for early visual discrimination skills , 2000, Nature Neuroscience.

[24]  C. Law,et al.  Sleep-Dependent Plasticity Requires Cortical Activity , 2005, The Journal of Neuroscience.

[25]  J. Hobson,et al.  Visual discrimination learning requires sleep after training , 2000, Nature Neuroscience.

[26]  Tamar Flash,et al.  Multiple shifts in the representation of a motor sequence during the acquisition of skilled performance , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Jan Born,et al.  Implicit Learning–Explicit Knowing: A Role for Sleep in Memory System Interaction , 2006, Journal of Cognitive Neuroscience.

[28]  J. Born,et al.  Sleep forms memory for finger skills , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Matthew P Walker,et al.  A refined model of sleep and the time course of memory formation. , 2005, The Behavioral and brain sciences.

[30]  Leslie G. Ungerleider,et al.  The acquisition of skilled motor performance: fast and slow experience-driven changes in primary motor cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[31]  J. Dorrian,et al.  The dynamics of neurobehavioural recovery following sleep loss , 2007, Journal of sleep research.

[32]  R. Stickgold,et al.  Sleep and the time course of motor skill learning. , 2003, Learning & memory.