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.”

“For example, after a short (11 min) motor training session, subjects showed strengthened connections in the FPN compared with a control group (Albert et al., 2009).”

“Another study investigated the effects of motor learning on resting state activity (Albert et al., 2009).”

“For example, motor learning modulates fronto-parietal resting state networks (Albert et al., 2009) and the performance on a language task affects resting state networks in regions associated with language (Waites et al., 2005).”

“Such effects have been shown for numerous cognitive domains, including motor learning (Albert et al. 2009), visual perception (Lewis et al.”

“Albert et al. (2009) and Lewis et al. (2009) related the post-taskmodulation in the resting-state functional connectivity to the recent learning experiences.”

“Several measures of connectivity in resting state have been proposed to predict motor learning (Albert et al., 2009; Wu et al., 2014), task performance (Lee et al., 2011; Zhou et al., 2012) or personality traits (Langer et al., 2012; Putman, 2011).”

“…metrics can generate reproducible results when examining the modulation of resting state activity by diseases (Salvador et al. 2007; Zang et al. 2007; Lai et al. 2010; Wang et al. 2010) or by the subjects’ experiences (Albert et al. 2009; Barnes et al. 2009; Wang et al. 2009; Tambini et al. 2010).”

“It has been suggested that the pattern of resting-state FC can be altered by extensive training and recent experiences (Albert et al., 2009; Jolles et al., 2013; Lewis et al., 2009).”

“, 2009], are subtly modulated by recent or ongoing experience in functionally relevant networks [Albert et al., 2009; Gordon et al., 2014; Grigg and Grady, 2010; Hasson et al., 2009; Lewis et al., 2009; Stevens et al., 2010; Tambini et al., 2010; Tung et al., 2013; Waites et al., 2005], predict individual differences…”

“…of anatomical (T1-weighted) MR images can be used to assess local changes in GM structure in the living human brain by comparing tissueclassified whole brain GM maps either in cross-sectional or longitudinal studies (Ashburner and Friston 2000; Ashburner and Friston 2005; Draganski and May 2008).”

“Resting-state networks also change actively, reflecting dynamic functional networks activated by recent cognitive (Albert, Robertson, & Miall, 2009; Hasson, Nusbaum, & Small, 2009; Tambini, Ketz, & Davachi, 2010; Waites, Stanislavsky, Abbott, & Jackson, 2005) and emotional states (van Marle,…”

“Furthermore, these modulations in the oscillatory activity of cortico-motor networks persist long after motor skill practice and continue to evolve during the consolidation of motor memory (Albert et al., 2009; Sami et al., 2014).”

“…resting state activity following the practice of a skill is influenced in specific ways related to functional activity in the practice of the skill, contributing to the consolidation of procedural memory (Miall and Robertson, 2006; Albert et al., 2009; Taubert et al., 2011; Vahdat et al., 2011).”

“, task performance can induce changes in functional connectivity strength [Albert et al., 2009; Hasson et al., 2009; Lewis et al., 2009; Waites et al., 2005].”

“[2] Albert NB, Robertson EM, Miall RC (2009).”

“Such interpretation is consistent with previous work, which has shown that motor learning influences resting-state network activity (e.g., Albert et al., 2009, Vahdat et al., 2011), and that the functional dynamics observed during a resting state period can also impact subsequent motor learning…”

“Furthermore, learning can transiently modify the strength of intrinsic activity correlations measured during subsequent rest periods (14).”

“Functional connectivity changes have been observed in the context of numerous training paradigms including visuomotor adaptation [88,89], Braille training in sighted individuals [90] visual perception practice [91], playing the Space Fortress videogame [92], and acquisition of episodic memory [93], among others [94].”

“Training duration varied from 11 minutes [15] to several weeks or months [20].”

“Albert et al. noted that independent-component-analysis (ICA) based connection strength (from 11-minute fcMRI data) increased following an 11-minute left-hand joystick target tracking task, which was attributed to neural plasticity associated with motor learning (Albert et al., 2009).”

“Several studies demonstrated that persistent training could induce the strengthening of functional connectivity which refers to its improved functions, such as motor [Albert et al., 2009], visual [Lewis et al.”

“neuroplastic changes in premotor and motor areas and the connection between them (Nelles et al., 2001; Sun et al., 2007; Albert et al., 2009; Taubert et al., 2011; Wiestler and Diedrichsen, 2013; Horn et al., 2016).”

“Given the evidence for activity-dependent plasticity of parietal-frontal circuits (Albert et al., 2009) and relationships between frontal network strengths and social activity levels (Bickart et al.”

“…Cheeran et al., 2010; Eisenegger et al., 2008). fMRI enables to gain insight into intrinsic functional connectivity while the brain is at rest (Albert et al., 2009; Fox and Raichle, 2007; Tambini et al., 2010; Vahdat et al., 2011), evaluating the effects of interference with existing memories…”

“For instance, using probabilistic independent component analysis of rsFC data, Albert et al. (2009) found a frontoparietal and a cerebellar component that increased in strength after motor espan Changes in Brain and slo, Pb. 1094 Blindern, 0317 0 01.”

“Such intrinsic connectivity increases are found in humans for simple motor learning (Albert et al., 2009) and for learning to navigate in a virtual environment (Woolley et al., 2015).”

“Studies have shown that the post-task resting-state network might be shaped by the performance during a prior task or through training 44,45,49 .”

“2009) or recent behavior or experience (Waites et al. 2005; Albert et al. 2009; Hasson et al. 2009; Lewis et al. 2009; Grigg and Grady 2010; Stevens et al. 2010; Tambini et al. 2010).”

“The findings reported here reaffirm the behavioral significance of endogenous brain activity following hemiparetic stroke and invite the possibility that behavior-based therapies can promote dynamic changes in resting-state connectivity.(4,50)”

“A recent fMRI study reported that motor learning by 11-min visuomotor training can modulate subsequent activity within resting-state networks (Albert et al., 2009).”

“This choicewas based on prior findings that resting state activity in task-relevant networks is modified by learning (Albert et al., 2009; Vahdat et al., 2011) and correlates with subsequent recognition memory (Deuker et al., 2013; Stevens et al., 2010; Tambini et al., 2010).”

“Also, the FPN has been shown to reorganize after longterm motor skill training (Jancke et al. 2009; Di et al. 2012; Taubert et al. 2011; Albert et al. 2009).”

“[11] in that within-network learning effects would mainly consist of increased resting state functional connectivity that were related to highly specific synaptic mechanisms stimulated by the learning task.”

“Using resting-state connectivity in healthy subjects, studies have shown functional changes in fronto-parietal-cerebellar networks (Albert et al., 2009; Sami and Miall, 2013) as well as motor cortex-cerebellar networks (Vahdat et al.”

“Notably, initial adult studies exploring training effects on mature, established resting-state connectivity patterns suggest that resting-state connectivity may continue to undergo refinement through different, short-term Hebbian-like mechanisms in maturity (Albert et al., 2009; Lewis et al., 2009; Tambini et al., 201…”

“Further, the associations between regions within the motor network are modifiable, with long-term motor learning increasing the strength of primary and supplementarymotor connectivity (Albert et al., 2009; Xiong et al., 2009; Ma et al., 2011; Taubert et al., 2011).”

“Over short time scales, resting state patterns are altered for up to 20 minutes following task performance (Barnes et al., 2009), being modulated by cognitive processes as diverse as short term memory (Gerraty et al., 2014) and visual-motor learning (Albert et al., 2009).”

“Using resting-state functional connectivity (RSFC), recent memory consolidation studies also suggested that the functional connectivity between brain areas played an important role in memory consolidation (fronto-parietal network, hippocampal-lateral occipital network) (Albert et al., 2009; Tambini et al., 2010).”

“Given that relatively subtle effects like learning can influence rfMRI data [97, 98], there certainly must be more to learn about stroke recovery from rfMRI.”

“Motor, perceptual, and phonological learning as well as memory tasks specifically modulate FC during (Sun et al., 2007) and after the tasks (Albert et al., 2009; Sami et al., 2014; Tambini et al., 2010; Veroude et al., 2010).”

“, 2009) or a motor learning task (Albert et al., 2009), influences the resting-state network's activity.”

“It is thought that the strength of functional connectivity reflects the strength of synchronization of neuronal activities that was shown to correlate with motor performance in healthy subjects (Sun et al., 2007; Albert et al., 2009) and after successful motor rehabilitation after stroke (Abutalebi et al.”

“The retinotopic localizer took place after the resting-state scans to avoid a possible effect of the retinotopic localizer on the resting-state scans [Albert et al., 2009; Hasson et al., 2009; Waites et al., 2005].”

“Consistent with this idea several studies have reported modifications of resting FC patterns after learning (Albert et al. 2009; Lewis et al. 2009; Tambini et al. 2010; Harmelech and Malach 2013).”

“Other studies reported that motor [17] and perceptual learning [18,19] can lead to longlasting changes in functional connectivity and a modulation of region specific plasticity.”

“In the subsequent analysis, connectivity strength and network strength were measured as in previous studies [7,8].”

“But there have also been reports of immediate variations in the coherence of ICNs associated with task performance of humans (Fox et al., 2007; Seeley et al., 2007; Albert et al., 2009; Lewis et al., 2009).”

“Based on our previous ICA results (Albert et al., 2009) and on a recent meta-analysis of the motor learning literature (Hardwick et al.”

“…patterns during post-training sleep (Peigneux et al., 2003, 2004; Huber et al., 2004; Walker and Stickgold, 2006; Rauchs et al., 2008; Diekelmann and Born, 2010) and wakefulness (Peigneux et al., 2006; Albert et al., 2009; Lewis et al., 2009; Tambini et al., 2010; Wang et al., 2012).”

“Other fMRI studies showed that the strength of spontaneous connectivity increases within the fronto-parietal and cerebellar networks immediately after a visuo-motor adaptation task [Albert et al., 2009].”

“, 2013) or motor skill (Albert et al., 2009; Taubert et al., 2011; Zhang et al., 2014) are associated with larger increases in intrinsic connectivity within and between sensory, motor and higher-order RSNs after learning.”

“They found that the leg Fugl-Meyer score—a clinical scale of function—and the extent of motor cortex that was recruited during movements of the ipsilateral foot (assessed with functionalMRI) provided the best predictors of subsequent treatment gains (Burke et al., 2014).”

“, 2004), and learning (Waites et al., 2005; Albert et al., 2009; Lewis et al., 2009; Stevens et al., 2010; Tambini et al., 2010).”

“Similar to earlier findings of state-related modulations of resting state connectivity (Albert et al., 2009; Hasson et al., 2009; Stevens et al., 2010; Tambini et al., 2010), we observed that fusiform connectivity was increased in light sleep compared to wake after learning.”

“Given that cognitive task performance can influence subsequent measures of rsFC (Albert et al, 2009), it is unknown to what extent group differences and abstinence effects on rsFC were due to residual effects of reactivity during the reward task.”

“Thus, t-values exceeding a threshold of p 0.01 (uncorrected) where spatially clustered based on neighboring electrodes.”

“We measured spontaneous patterns of activity within the resting brain before and after learning a new sensorimotor skill or sensorimotor performance, and showed that two circuits within the resting brain were specifically affected by sensorimotor learning.(7,8) One included the frontal and parietal cortices, the other…”

“The strength of the network including the frontal and parietal areas could be modulated by cognitive control and decision making process such as motor learning (Albert et al., 2009).”

“…cathodal electrode on the controlateral side of the parietal lobe, and not on the prefrontal cortex, not to affect the mechanisms that might relate to learning (Iuculano and Cohen Kadosh, 2013), and feedback/reward, which was provided during the learning phase (Duncan, 2001; Albert et al., 2009).”

“Motor learning increased functional connectivity within a frontoparietal resting-state network when compared to the same motor task without learning [Albert et al., 2009].”

“, 2012] associated with learning [Albert et al., 2009; Lewis et al., 2009; Vincent, 2009] and cognition [Grigg and Grady, 2010; Hasson et al.”

“Moreover, learning and behavioral intervention produce measurable changes in FC in relevant cortical circuits and resting correlation is altered by learning and adaptation (Albert et al. 2009; Lewis et al. 2009; Tambini et al. 2010; SampaioBaptista et al. 2015; Newbold 2020).”

“Remarkably, the functional coupling between these two nodes is highly flexible, shifting as a function of experiences ranging from motor training (Albert et al., 2009; Dayan et al., 2011; Taubert et al., 2011; Hamzei et al., 2012; Philip et al., 2016) to brain injuries (Nelles et al.”

“Recently, a few fMRI studies investigating the impact of motor skill learning on resting-state networks have found changes in fronto-parietal and cerebellar networks following visuo-motor tracking [13] and dynamic balancing training [14], changes in the motor network following motor sequence learning [15] and changes…”

“In line with the animal literature, human functional neuroimaging studies have found that learning experiences can modulate resting-state brain connectivity (Albert et al., 2009; Deuker et al., 2013; Groen et al., 2011; Hasson et al., 2009; Urner et al., 2013; Wang et al., 2012; Zou et al., 2013), and that the HPC act…”

“A recent study conducted by Albert et al. (2009) showed that motor learning modulated resting state networks in a positive manner, and another study performed by Lewis et al. (2009) demonstrated that visual perceptual learning modified the interaction and organization between functional networks.”

“This is in line with a large body of evidence suggesting that neural events leading to motor memory consolidation begin with practice but continue after training (Albert et al. 2009; see Dayan and Cohen 2011 for a recent review in motor skill learning).”

“…individual differences in the consolidation of learned information, such that individuals with superior performance on a preceding learning task display the greatest changes in rsFC from a pre-to postlearning resting scan (e.g., Albert et al., 2009; Vahdat et al., 2011; Wegman and Jan-zen, 2011).”

“Learning and subsequently consolidating a motor skill memory leads to activity changes within brain areas that include the hippocampus, which have traditionally been considered part of the declarative memory system [28,36–38].”