The Resting Human Brain and Motor Learning

“Each EPI volume was motion-corrected using MCFLIRT [3], high-pass filtered (0.01HZ cutoff), masked to eliminate non-brain voxels, spatially-smoothed using a 5mm FWHM filter, demeaned on a voxel-by-voxel basis, whitened, and projected into a 48-dimensional subspace using PICA.”

“The role of this resting state activity, evident as low-frequency fluctuations of BOLD (see[1]forreview,[2‐4])orelectrical[ 5 ,6]signals,isunclear.”

“The role of this resting state activity, evident as low-frequency fluctuations of BOLD (see[1]forreview,[2‐4])orelectrical[5, 6 ]signals,isunclear.”

“We identified six previously reported RSNs (see Figures 2A–2E and 2H of [4]).”

“The change in strength of the two RSN components identified by PICA across participants within the test group (Figure 2, main paper) was not linearly correlated with behavioral measures of learning, but this does not imply there is no relationship.”

“Non-brain structures were removed from the high-resolution structural image using BET [5] and the transformation matrix used for the affine registration of this image to the ICBM152 brain [2] was applied to the PICA output from each session.”

“The role of this resting state activity, evident as low-frequency fluctuations of BOLD (see [1] for review, [2– 4]) or electrical [5, 6] signals, is unclear.”

“of change in resting state activity [7, 8 ]. The gradual increase in the visuo-motor perturbation”

“The role of this resting state activity, evident as low-frequency fluctuations of BOLD (see [1] for review, [2– 4]) or electrical [5, 6] signals, is unclear.”

“Previous imaging reports suggest widespread cerebellar activation during active performance of motor learning tasks [10, 12, 17], but as far as we are aware, no others have searched for cerebellar resting state components after a period of motor learning.”

“In fact, there is a striking overlap between the areas identified with PICA in this experiment and areas involved in motor learning (see [29] for review) and areas that represent consolidated motor skills (see [30] for review).”

“could lead to memory consolidation, which takes place over several hours (or overnight) after exposure to learning [28].”

“The networks affected by visuomotor adaptation, including the fronto-parietal (Figure 2) and cerebellar circuits (Figure 3), are known to be active during visuomotor adaptation [14, 15, 18–21] and are necessary for the long-term retention of motor skills [16, 17, 22].”

“This is an important distinction from an earlier report of offline persistence of memory-related activity [27].”

“Activity within the resting brain may reflect the on-going ‘‘offline’’ processing of information gained from earlier learning [8, 27, 31].”

“The visuomotor task [23] (see Supplemental Experimental Procedures) interleaved between the two rest sessions required the participants to use their nonpreferred left hand to move an MR-compatible joystick.”

“An alternative perspective is that the resting brain actively and selectively processes previous experiences [8].”

“Moreover, consolidation processes would be expected to modulate the strength of cortico-cortical interactions [36], and thus be evident as the increase in strength of spatio-temporal patterns identified by PICA analysis.”

“, 2007), learning (Albert et al., 2009; Bassett et al., 2011; Lewis et al., 2009; Tambini et al., 2010), and large state transitions such as sleep (Horovitz et al.”

“For instance, functional connectivity is modulated by cognitive (47) and emotional state (48), arousal, and sleep (26), whereas structural connectivity is grossly unaffected by such factors.”

“Overall, these studies suggest that functional connectivity in fronto-parietal networks supports consolidation after fast (Albert et al., 2009) and slow learning (Taubert et al.”

“The frontoparietal control network, composed of rostrolateral prefrontal cortex (RLPFC), middle frontal gyrus (MFG), anterior insula/frontal operculum (aIfO), dorsal anterior cingulate cortex (dACC), precuneus (PCu), and anterior inferior parietal lobule (aIPL), is anatomically interposed between the default and dorsa…”

“A greater level of basal activity in motor networks, as well as greater coactivation between different networks, may be related to increased use and coordination between these systems, as suggested by recent studies of motor learning and functional connectivity (Albert et al., 2009; Xiong et al., 2009).”

“Importantly, functional connectivity is related to motor skill learning (Albert et al., 2009; Song, Gotts, Dayan, & Cohen, 2015) and to higher levels of motor skill (Di, Zhu, Jin, Wang, Ye, Zhou et al.”

“(50), who demonstrated increased functional connectivity in the motor system only when subjects learn a novel task, but not when they repeat a familiar task with the same intensity.”

“, 2007), and that they are affected by the performance of a prior task (Albert et al., 2009; Barnes et al., 2009; Lewis et al., 2009; Tambini et al., 2010) and induced changes in mood state (Harrison et al.”

“Furthermore, Albert et al. (2009) found that connectivity in the default network, as well as in the cerebellum, is specifically enhanced during rest after a task requiring motor learning, demonstrating a relationship between learning and changes in resting connectivity, similar to changes seen in…”

“Few studies have analyzed badminton players’ ability to cope with the neural [141] and biomechanical constraints of gripping and swinging a badminton racket [142].”

“Indeed, the temporal coherence of some components has been shown to be modulated by performing an active task immediately prior to resting-state study: this evidence suggests that the recent experience as well as consolidated abilities can leave ‘a memory trace’ and that, more generally, spontaneous fluctuations may b…”

“Shaping of envelope ICMs by history of coupling during preceding tasks has been shown in several studies involving sensorimotor learning (Albert et al., 2009; Lewis et al., 2009) or memory encoding (Tambini et al., 2010).”

“We are using functional imaging to understand the co-activation of cerebral and cerebellar areas [129] and more recently to explore how their connectivity changes as a consequence of learning [130].”

“This may be related to variable mental states of participants across scans which induce variations in RSFC [19,20,21,22,23,24,25].”

“state fcMRI before and after tasks can circumvent this confound, an approach that has been used to document modulation of resting state functional connectivity by learning tasks (Albert et al., 2009; Lewis et al., 2009; Tambini et al., 2010).”

“Previous studies of training-related changes in intrinsic connectivity have demonstrated that, in general, brain networks recruited during training show robust changes in intrinsic connectivity (Albert et al., 2009; Lewis et al., 2009).”

“However, reconfigurations can be directly induced by changing the behavioural task or behavioural context [14–39].”

“Modulations in RSFC were found after learning (Albert et al., 2009; Lewis et al., 2009; Xiong et al., 2009), in relation to specific task demands (Barnes et al.”

“This belief is based on a growing literature in normal subjects (Albert et al., 2009; Hampson et al., 2006; Lewis et al., 2009; Tambini et al., 2010; van den Heuvel et al., 2009) showing that in healthy subjects behavioral parameters and learning are significantly correlated with patterns of resting functional connect…”

“Also suggestive of validity have been reports of changes in the functional connectome following learning in healthy volunteers (Albert et al., 2009; Lewis et al., 2009; Ma et al., 2011; Taubert et al., 2011).”

“Another study showed that active learning was involved in enhancement of connectivity in resting state networks reflective of task-relevant regions in the learned task, while connectivity was not affected by mere rote performance of the same learned task (Albert et al., 2009).”

“Human imaging studies of healthy subjects have demonstrated increased functional connectivity between the lateral cerebellum and the frontoparietal network soon after sensorimotor learning (Albert et al., 2009) and after a period of learning the serial reaction time task (Sami et al.”

“Similarly, Albert et al. 56 demonstrated increased functional connectivity in the motor system only when subjects learnt a novel task, but not when they repeated a familiar task with the same intensity, and Stevens et al. 57 observed increased correlations between the inferior frontal gyrus and…”

“For instance, learning a visuomotor tracking task enhanced IFC between frontal and parietal brain regions during subsequent resting wakefulness (Albert et al., 2009).”

“J Neurol Neurosurg Psychiatry 68(2):157–161.”

“Brain areas involved in force-field learning have been studied previously by Shadmehr and Holcomb (1997) using positron emission tomography and under resting-state conditions by Albert et al. (2009).”

“Using this approach, recent studies have demonstrated a modulation of resting-state components by motor learning and memory consolidation (Albert et al., 2009a,b).”

“…2006) and anodal transcranial direct current stimulation (tDCS) applied to M1 (Stagg et al., 2009, 2011a) have previously been shown to decrease M1 GABA levels and to increase motor resting functional connectivity (Albert et al., 2009; Sehm et al., 2012; Amadi et al., 2014; Stagg et al., 2014).”

“Similar modulations have also been observed immediately following task performance (Albert et al., 2009; Stevens et al., 2010; Waites et al., 2005).”

“Using the traditional analysis method of correlation between networks on the time scale of entire resting-state functional imaging runs [Albert et al., 2009; Kelly et al., 2008; Tambini et al., 2010; Wang et al., 2010] a significant relationship was shown between faster reaction times and anticorrelation between the d…”

“Indeed, RSFC in awake humans has been extensively used to reveal neural circuit function in both normal (Albert et al., 2009; Horovitz et al., 2009) and pathological conditions (Anand et al.”

“, 2006), increases RSN functional connectivity (Albert et al., 2009).”

“Moreover, training-related changes of functional 529 connectivity have been observed during resting-state (Albert et al., 2009;Lewis et al., 530 2009;Jolles et al., 2011), suggesting that changes of interregional interactions are not 531 necessarily specific to task conditions.”

“This view is supported by developmental [33] and learning studies [34,35].”

“We argue that restingstate connectivity might not only be influenced by a pre- ceding task [e.g., Albert et al., 2009; Barnes et al., 2009] but can also be modified by (implicit or explicit) preparatory processes in anticipation of a task.”

“…that LF-BOLD fluctuations during rest are modulated by previous tasks within networks engaged during task performance (Waites et al. 2005; Albert et al. 2009; Hasson et al. 2009; Lewis et al. 2009); some providing support for the suggestion that resting-state activity may be involved in…”

“Our whole-brain analysis found no interactions between group and task (silent reading, phonological lexical decision, and rest) on connectivity of the left FFG.”

“Recent studies have also delineated significant influences of various pathological conditions on RSFC (Greicius et al., 2007), indicating vital neurobiological and psychopathological relevance (Kennedy et al., 2006; Albert et al., 2009).”

“In order to control for potential differences in RSN functional connectivity affected by prior task performance (Albert et al., 2009), separately from the cognitive and clinical withdrawal symptoms of interest, accuracy scores in the most difficult condition of the information processing taskwere similarly included as…”

“1368 Current Biology 25, 1368–1374, May 18, 2015 a2015 Elsevier L ‘‘resting-state’’ BOLD correlation structure reflects learning [7], conscious states [8], brain maturity [9], cognitive control, and intelligence [10], as well as neuropsychiatric diseases [2, 11–13].”

“, 2006) and is also sensitive to individual variations that are linked to behavioral performance (Albert et al., 2009; Boly et al., 2007; Hampson et al., 2006; Thompson et al., 2012; Waites et al., 2005; Weissman et al., 2006).”

“Functional magnetic resonance imaging (fMRI) studies show that learning a task changes this wakeful resting state activity in task-relevant networks (Albert et al. 2009), and that these changes predict better recognition of the learned material later that same day (Tambini et al.”

“The networks engaged after the visuomotor learning task (Albert et al., 2009) appear to be members of previously identified”

“Albert et al. (2009) observed increased functional connectivity strength in the fronto-parietal topdown control ICN and a cerebellar ICN after few minutes of motor learning.”

“Resting state data have been used to investigate both clinical (see Fox and Greicius, 2010; Greicius, 2008 for review) and non-clinical (e.g., Albert et al., 2009b; Biswal et al., 1995; Hampson et al., 2002; Jiang et al., 2004; Xiong et al., 1999, among many other studies) populations.”

“ORIGINAL RESEARCH published: 30 March 2015 doi: 10.3389/fnhum.2015.00160 Frontiers in Human Neuroscience | www.frontiersin.org 1 March 2015 | Volume 9 | Article 160 Edited by: Daniel S. Margulies, Max Planck Institute for Human Cognitive and Brain Sciences, Germany Reviewed by: Marco Taubert, Max-Planck-Institute for…”

“Even in adults, learning experiences (e.g., motor learning) can alter RSFC patterns (Albert et al. 2009; Xiong et al. 2009).”

“, 2007), indicating its vital neurobiological and psychopathological relevance (Albert et al., 2009; Kennedy et al., 2006).”

“The study of these networks represents a fertile area of research given their ability to experience neuroplastic changes, for example in relation to learning (Albert et al., 2009; Mantini et al., 2009).”

“In one of the earliest studies to examine training-related plasticity in iFC, Albert et al. (2009) had participants perform a short (11 min) task in which they had to adapt their visuomotor movements to an altered cursorjoystick relationship that required progressively increasing compensation.”

“We argue that this finding may reflect different consequences of training phases between short-term training in Albert et al. (2009) and long-term athletic training in the present study.”

“…et al. (2011) found that motor training reinforces resting-state functional connectivity within both a motor and a somatosensory network, while Albert et al. (2009) reported modulations in resting-state functional connectivity in the wake of new complex motor learning, but not after simple,…”

“Since cognitive task performance can impact subsequent measures of RSN function (Albert et al., 2009), it is possible that group RSN differences may have been a consequence of group differences in reactivity to smoking-related cues.”

“While plastic changes are easily assessed using rs-fMRI techniques (Albert et al., 2009), it is well known that plastic interventions, such as those produced by cognitive or behavioral demands, are able to impact both WM (Engvig et al., 2012) and GM (Engvig et al., 2010) structure assessed with MRI…”

“In addition, the plasticity of specific neural circuitries induced by neurobiological behaviors such as learning and memory has been repeatedly revealed by rsfMRI (Albert et al., 2009; Foster and Wilson, 2006; Horovitz et al., 2009).”

“For example, Albert et al. (2009) and Hasson et al. (2009) demonstrated that resting-state DMN connectivity could be modulated by previous experiences, and Tambini et al. (2010) further demonstrated that modulated resting-state hippocampal-cortical connectivity after an encoding task can predict…”

“Furthermore, several studies have demonstrated that acute changes in resting-state FC reflect experiencedependent plasticity following experimental manipulations of learning and memory [26–28].”

“The behavioral relevance of endogenous DMN activity remains elusive, despite an emerging literature correlating resting fMRI fluctuations with memory performance [4, 5]—particularly in DMN regions [6–8].”

“This hypothesis is supported by previous evidence for activity-dependent plasticity of functional connectivity within frontoparietal (Albert et al., 2009) and lower-level visual (Baldassarre et al., 2012) networks, in response to motor and perceptual learning, respectively, and for associations…”

“Support for this idea is provided by a study done on human participants in which blood oxygen level dependent (BOLD) signals were measured during rest periods in between bouts of motor training [81].”

“For instance, 11 min of motor training increased the strength of the fronto-parietal and the cerebellum resting state networks (RSNs) (Albert et al., 2009).”

“But the fact that resting state FC can be modified over relatively short time periods by performing a task has suggested that resting state interactions between brain regions also reflect the frequency and past history of coactivation (Albert et al., 2009; Hasson et al., 2009; Lewis et al., 2009; Tambini et al., 2010).”

“Also, consolidation following motor training that required continuous updating of the parameters for manually tracking a moving object, a form of VP training, was associated with increased synchrony among brain regions in a fronto-parietal brain network (Albert et al., 2009).”

“The subjects were required to perform the stop-signal task after RS-fMRI data acquisition for the consideration that RS-fMRI signals could possibly be modulated by preceding events (Albert et al., 2009; Tambini et al., 2010; Yan et al., 2009).”

“Actually, as mentioned above, some studies have shown changes in frontal θ power after WM training (Jaušovec and Jaušovec, 2012) or training that uses a complex video game (Anguera et al., 2013), suggesting that these EEG biomarkers can be useful for tracking the progress of cognitive training.”

“Notably, the direction of change in restingstate connectivity was not consistent across these studies, with connectivity after task performance becoming more positive [Albert et al., 2009; Duff et al., 2008; Grigg and Grady, 2010; Tambini et al., 2010; Vahdat et al., 2011; Waites et al., 2005], more negative [Lewis et…”