Humans' ability to adapt and learn relies on reflecting on past performance. These experiences form latent representations called internal states that induce movement variability that improves how we interact with our environment. Our study uncovered temporal dynamics and neural substrates of two states from ten subjects implanted with intracranial depth electrodes while they performed a goal-directed motor task with physical perturbations. We identified two internal states using state-space models: one tracking past errors and the other past perturbations. These states influenced reaction times and speed errors, revealing how subjects strategize from trial history. Using local field potentials from over 100 brain regions, we found large-scale brain networks such as the dorsal attention and default mode network modulate visuospatial attention based on recent performance and environmental feedback. Notably, these networks were more prominent in higher-performing subjects, emphasizing their role in improving motor performance by regulating movement variability through internal states.
Disciplines :
Engineering, computing & technology: Multidisciplinary, general & others
Author, co-author :
Breault, Macauley Smith ; Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Cambridge, MA, USA. breault@mit.edu ; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA. breault@mit.edu
Sacré, Pierre ; Université de Liège - ULiège > Département d'électricité, électronique et informatique (Institut Montefiore) > Robotique intelligente
Fitzgerald, Zachary B; Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
Gale, John T; DIXI Neurolab, Inc., Oxford, MI, USA
Cullen, Kathleen E ; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
González-Martínez, Jorge A; Department of Neurological Surgery, University of Pittsburgh, Pittsburgh, PA, USA
Sarma, Sridevi V; Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, USA
Language :
English
Title :
Internal states as a source of subject-dependent movement variability are represented by large-scale brain networks.
Faisal, A. A., Selen, L. P. J. & Wolpert, D. M. Noise in the nervous system. Nat. Rev. Neurosci. 9, 292–303 (2008).
McIntosh, A. R., Kovacevic, N. & Itier, R. J. Increased brain signal variability accompanies lower behavioral variability in development. PLoS Comput.Biol. 4, e1000106 (2008).
Wolpert, D. M., Diedrichsen, J. & Flanagan, J. R. Principles of sensorimotor learning. Nature Rev. Neurosci. 12, 739–751 (2011).
Garrett, D. D. et al. Moment-to-moment brain signal variability: a next frontier in human brain mapping? Neurosci. Biobehav. Rev. 37, 610–624 (2013).
Dhawale, A. K., Smith, M. A. & Ölveczky, B. P. The role of variability in motor learning. Annu. Rev. Neurosci. 40, 479–498 (2017).
Ölveczky, B. P., Andalman, A. S. & Fee, M. S. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol. 3, e153 (2005).
Wu, H. G., Miyamoto, Y. R., Castro, L. N. G., Ölveczky, B. P. & Smith, M. A. Temporal structure of motor variability is dynamically regulated and predicts motor learning ability. Nat. Neurosci. 17, 312–321 (2014).
Mir, P. et al. Motivation and movement: the effect of monetary incentive on performance speed. Exp. Brain Res. 209, 551–559 (2011).
Galaro, J. K., Celnik, P. & Chib, V. S. Motor cortex excitability reflects the subjective value of reward and mediates its effects on incentive-motivated performance. J. Neurosci. 39, 1236–1248 (2019).
Kiani, R. & Shadlen, M. N. Representation of confidence associated with a decision by neurons in the parietal cortex. Science 324, 759–764 (2009).
Zylberberg, A., Fetsch, C. R. & Shadlen, M. N. The influence of evidence volatility on choice, reaction time and confidence in a perceptual decision. eLife 5, e17688 (2016).
Schmidt, L. et al. Get aroused and be stronger: emotional facilitation of physical effort in the human brain. J. Neurosci. 29, 9450–9457 (2009).
Lawrence, G. P., Khan, M. A. & Hardy, L. The effect of state anxiety on the online and offline control of fast target-directed movements. Psychol. Res. 77, 422–433 (2012).
Blakemore, R. L. & Vuilleumier, P. An emotional call to action: integrating affective neuroscience in models of motor control. Emotion Rev. 9, 299–309 (2016).
Braun, A., Urai, A. E. & Donner, T. H. Adaptive history biases result from confidence-weighted accumulation of past choices. J. Neurosci. 38, 2418–2429 (2018).
Maclnnes, W. J., Hunt, A. R., Clarke, A. D. F. & Dodd, M. D. A generative model of cognitive state from task and eye movements. Cogn. Comput. 10, 703–717 (2018).
Calhoun, A. J., Pillow, J. W. & Murthy, M. Unsupervised identification of the internal states that shape natural behavior. Nat. Neurosci. 22, 2040–2049 (2019).
Ashwood, Z. C. et al. Mice alternate between discrete strategies during perceptual decision-making. Nat. Neurosci. 25, 201–212 (2022).
Gründemann, J. et al. Amygdala ensembles encode behavioral states. Science 364, eaav8736 (2019).
Sacré, P. et al. Risk-taking bias in human decision-making is encoded via a right–left brain push–pull system. Proc. Natl Acad. Sci. USA 116, 1404–1413 (2019).
Hwang, E. J., Dahlen, J. E., Mukundan, M. & Komiyama, T. History-based action selection bias in posterior parietal cortex. Nat. Commun. 8, 1–14 (2017).
Cowley, B. R. et al. Slow drift of neural activity as a signature of impulsivity in macaque visual and prefrontal cortex. Neuron 108, 551–567 (2020).
Wolpert, D. M. & Landy, M. S. Motor control is decision-making. Curr. Opinion Neurobiol. 22, 996–1003 (2012).
Churchland, M. M., Afshar, A. & Shenoy, K. V. A central source of movement variability. Neuron 52, 1085–1096 (2006).
van Beers, R. J., Haggard, P. & Wolpert, D. M. The role of execution noise in movement variability. J. Neurophysiol. 91, 1050–1063 (2004).
Renart, A. & Machens, C. K. Variability in neural activity and behavior. Curr Opinion Neurobiol. 25, 211–220 (2014).
Tourangeau, R. & Rasinski, K. A. Cognitive processes underlying context effects in attitude measurement. Psychol. Bullet 103, 299 (1988).
Critchley, H. D., Elliott, R., Mathias, C. J. & Dolan, R. J. Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study. J. Neurosci. 20, 3033–3040 (2000).
Lane, R. D. et al. Neural correlates of heart rate variability during emotion. NeuroImage 44, 213–222 (2009).
Thayer, J. F., Åhs, F., Fredrikson, M., Sollers III, J. J. & Wager, T. D. A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci. Biobehav. Rev. 36, 747–756 (2012).
Podvalny, E., King, L. E. He, B. J. Spectral signature and behavioral consequence of spontaneous shifts of pupil-linked arousal in human. eLife https://doi.org/10.7554/eLife.68265 (2021).
Schwarz, N. & Oyserman, D. Asking questions about behavior: cognition, communication, and questionnaire construction. Am. J. Eval. 22, 127–160 (2001).
Kanwal, J. K. et al. Internal state: dynamic, interconnected communication loops distributed across body, brain, and time. Integr. Compar. Biol. 61, 867–886 (2021).
Lurie, D. J. et al. Questions and controversies in the study of time-varying functional connectivity in resting fmri. Netw. Neurosci. 4, 30–69 (2020).
Logothetis, N. K. What we can do and what we cannot do with fMRI. Nature 453, 869–878 (2008).
Maris, E. & Oostenveld, R. Nonparametric statistical testing of EEG- and MEG-data. J. Neurosci. Methods 164, 177–190 (2007).
Friston, K. J. Functional and effective connectivity in neuroimaging: a synthesis. Human Brain Mapp. 2, 56–78 (1994).
Harris, C. M. & Wolpert, D. M. Signal-dependent noise determines motor planning. Nature 394, 780–784 (1998).
Todorov, E. & Jordan, M. I. Optimal feedback control as a theory of motor coordination. Nat. Neurosci. 5, 1226–1235 (2002).
Fine, M. S. & Thoroughman, K. A. Trial-by-trial transformation of error into sensorimotor adaptation changes with environmental dynamics. J. Neurophysiol. 98, 1392–1404 (2007).
Fine, M. S. & Thoroughman, K. A. Motor adaptation to single force pulses: sensitive to direction but insensitive to within-movement pulse placement and magnitude. J. Neurophysiol. 96, 710–720 (2006).
Corbetta, M. & Shulman, G. L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).
Shulman, G. L. et al. Interaction of stimulus-driven reorienting and expectation in ventral and dorsal frontoparietal and basal ganglia-cortical networks. J. Neurosci. 29, 4392–4407 (2009).
Heitz, R. P. The speed-accuracy tradeoff: history, physiology, methodology, and behavior. Front. Neurosci. 8, 150 (2014).
Steinhauser, M. & Yeung, N. Error awareness as evidence accumulation: effects of speed-accuracy trade-off on error signaling. Front. Human Neurosci. 6, 240 (2012).
Van Veen, V., Krug, M. K. & Carter, C. S. The neural and computational basis of controlled speed-accuracy tradeoff during task performance. J. Cogn. Neurosci. 20, 1952–1965 (2008).
Agam, Y. et al. Network dynamics underlying speed-accuracy trade-offs in response to errors. PLoS One 8, e73692 (2013).
Eryurek, K. et al. Default mode and dorsal attention network involvement in visually guided motor sequence learning. Cortex 146, 89–105 (2022).
Fuster, J. M. & Alexander, G. E. Neuron activity related to short-term memory. Science 173, 652–654 (1971).
Lachaux, J.-P., Axmacher, N., Mormann, F., Halgren, E. & Crone, N. E. High-frequency neural activity and human cognition: past, present and possible future of intracranial eeg research. Prog. Neurobiol. 98, 279–301 (2012).
Constantinidis, C. et al. Persistent spiking activity underlies working memory. J. Neurosci. 38, 7020–7028 (2018).
Gnadt, J. W. & Andersen, R. A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp. Brain Res. 70, 216–220 (1988).
Fiehler, K. et al. Working memory maintenance of grasp-target information in the human posterior parietal cortex. NeuroImage 54, 2401–2411 (2011).
Majerus, S., Péters, F., Bouffier, M., Cowan, N. & Phillips, C. The dorsal attention network reflects both encoding load and top–down control during working memory. J. Cogn. Neurosci. 30, 144–159 (2018).
Bledowski, C., Rahm, B. & Rowe, J. B. What “works” in working memory? separate systems for selection and updating of critical information. J. Neurosci. 29, 13735–13741 (2009).
Seidler, R. D., Bo, J. & Anguera, J. A. Neurocognitive contributions to motor skill learning: the role of working memory. J. Motor Behav. 44, 445–453 (2012).
Masse, N. Y., Rosen, M. C. & Freedman, D. J. Reevaluating the role of persistent neural activity in short-term memory. Trends Cogn. Sci. 24, 242–258 (2020).
Robertson, I. H., Manly, T., Andrade, J., Baddeley, B. T. & Yiend, J. ’oops!’: performance correlates of everyday attentional failures in traumatic brain injured and normal subjects. Neuropsychologia 35, 747–758 (1997).
Pessoa, L., Gutierrez, E., Bandettini, P. A. & Ungerleider, L. G. Neural correlates of visual working memory: fmri amplitude predicts task performance. Neuron 35, 975–987 (2002).
Padilla, M. L., Wood, R. A., Hale, L. A. & Knight, R. T. Lapses in a prefrontal-extrastriate preparatory attention network predict mistakes. J. Cogn. Neurosci. 18, 1477–1487 (2006).
Fortenbaugh, F. C., Rothlein, D., McGlinchey, R., DeGutis, J. & Esterman, M. Tracking behavioral and neural fluctuations during sustained attention: a robust replication and extension. NeuroImage 171, 148–164 (2018).
Kucyi, A. et al. Electrophysiological dynamics of antagonistic brain networks reflect attentional fluctuations. Nat. Commun. 11, 1–14 (2020).
Esterman, M., Noonan, S. K., Rosenberg, M. & DeGutis, J. In the zone or zoning out? tracking behavioral and neural fluctuations during sustained attention. Cerebr. Cortex 23, 2712–2723 (2013).
McVay, J. C. & Kane, M. J. Drifting from slow to “d’oh!”: Working memory capacity and mind wandering predict extreme reaction times and executive control errors. J. Exp. Psychol. Learn. Memory Cogn. 38, 525 (2012).
Adam, K. C., Mance, I., Fukuda, K. & Vogel, E. K. The contribution of attentional lapses to individual differences in visual working memory capacity. J. Cogn. Neurosci. 27, 1601–1616 (2015).
DeBettencourt, M. T., Keene, P. A., Awh, E. & Vogel, E. K. Real-time triggering reveals concurrent lapses of attention and working memory. Nat. Human Behav. 3, 808–816 (2019).
Machner, B. et al. Resting-state functional connectivity in the dorsal attention network relates to behavioral performance in spatial attention tasks and may show task-related adaptation. Front. Human Neurosci. 15, 757128 (2022).
Roberts, S. D. et al. Investigation of baseline attention, executive control, and performance variability in female varsity athletes. Brain Imaging Behav. 16, 1635–1645 (2022).
Burgess, G. C. et al. Attentional control activation relates to working memory in attention-deficit/hyperactivity disorder. Biol. Psychiat. 67, 632–640 (2010).
Salmi, J. et al. Out of focus–Brain attention control deficits in adult ADHD. Brain Res. 1692, 12–22 (2018).
Brandman, T., Malach, R. & Simony, E. The surprising role of the default mode network in naturalistic perception. Commun. Biol. 4, 1–9 (2021).
Kerr, M. S. D. et al. The role of associative cortices and hippocampus during movement perturbations. Front. Neural Circ. 11, 26 (2017).
Dohmatob, E., Dumas, G. & Bzdok, D. Dark control: The default mode network as a reinforcement learning agent. Human Brain Mapp. 41, 3318–3341 (2020).
Zhang, H. et al. Motor imagery learning modulates functional connectivity of multiple brain systems in resting state. PLoS One 9, e85489 (2014).
Albouy, G. et al. Neural correlates of performance variability during motor sequence acquisition. NeuroImage 60, 324–331 (2012).
Sali, A. W., Courtney, S. M. & Yantis, S. Spontaneous fluctuations in the flexible control of covert attention. J. Neurosci. 36, 445–454 (2016).
Hinds, O. et al. Roles of default-mode network and supplementary motor area in human vigilance performance: evidence from real-time fmri. J. Neurophysiol. 109, 1250–1258 (2013).
Hsu, H. M., Yao, Z.-F., Hwang, K. & Hsieh, S. Between-module functional connectivity of the salient ventral attention network and dorsal attention network is associated with motor inhibition. PLoS One 15, e0242985 (2020).
Diedrichsen, J., Hashambhoy, Y., Rane, T. & Shadmehr, R. Neural correlates of reach errors. J. Neurosci. 25, 9919–9931 (2005).
Cléry-Melin, M.-L. et al. Why don’t you try harder? An investigation of effort production in major depression. PLoS One 6, e23178 (2011).
Burris, K. et al. Sensorimotor abilities predict on-field performance in professional baseball. Sci. Rep. 8, 1–9 (2018).
González-Martínez, J. et al. Technique, results, and complications related to robot-assisted stereoelectroencephalography. Neurosurgery 78, 169–180 (2015).
Johnson, M. A. et al. Performing behavioral tasks in subjects with intracranial electrodes. J. Vis. Exp. 92, 51947 (2014).
Breault, M. S., Sacré, P., González-Martínez, J., Gale, J. T. Sarma, S. V. An exploratory data analysis method for identifying brain regions and frequencies of interest from large-scale neural recordings. J. Comput. Neurosci. https://doi.org/10.1007/s10827-018-0705-9 (2018).
Breault, M. S. et al. Non-motor brain regions in non-dominant hemisphere dominate in decoding movement speed. Front. Neurosci. 13, 715 (2019).
Asaad, W. F. & Eskandar, E. N. A flexible software tool for temporally-precise behavioral control in Matlab. J. Neurosci. Methods 174, 245–258 (2008).
Afshar, A. et al. Single-trial neural correlates of arm movement preparation. Neuron 71, 555–564 (2011).
Crammond, D. J. & Kalaska, J. F. Prior information in motor and premotor cortex: Activity during the delay period and effect on pre-movement activity. J. Neurophysiol. 84, 986–1005 (2000).
Cluff, T. & Scott, S. H. Apparent and actual trajectory control depend on the behavioral context in upper limb motor tasks. J. Neurosci. 35, 12465–12476 (2015).
Oostenveld, R., Fries, P., Maris, E. Schoffelen, J. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput. Intell. Neurosci. https://doi.org/10.1155/2011/156869 (2011).
Stolk, A. et al. Integrated analysis of anatomical and electrophysiological human intracranial data. Nat. Prot. 13, 1699–1723 (2018).
Destrieux, C., Fischl, B., Dale, A. & Halgren, E. Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage 53, 1–15 (2010).
Yeo, B. et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106, 1125–1165 (2011).
Fischl, B. Freesurfer. Neuroimage 62, 774–781 (2012).
Hamilton, L. S., Chang, D. L., Lee, M. B. & Chang, E. F. Semi-automated anatomical labeling and inter-subject warping of high-density intracranial recording electrodes in electrocorticography. Front. Neuroinform. 11, 62 (2017).
Prerau, M. J., Brown, R. E., Bianchi, M. T., Ellenbogen, J. M. & Purdon, P. L. Sleep neurophysiological dynamics through the lens of multitaper spectral analysis. Physiology 32, 60–92 (2017).
Sani, O. G. et al. Mood variations decoded from multi-site intracranial human brain activity. Nat. Biotechnol. 36, 954–961 (2018).
Crone, N. E., Sinai, A. & Korzeniewska, A. High-frequency gamma oscillations and human brain mapping with electrocorticography. Progr. Brain Res. 159, 275–295 (2006).
Bastos, A. M. & Schoffelen, J.-M. A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front. Syst. Neurosci. 9, 175 (2016).
Fisher, R. A. Frequency distribution of the values of the correlation coefficient in samples from an indefinitely large population. Biometrika 10, 507–521 (1915).
Silver, N. C. & Dunlap, W. P. Averaging correlation coefficients: should Fisher’s z transformation be used? J. Appl. Psychol. 72, 146 (1987).
Breault, M. S. et al. Internal States as a Source of Subject-Dependent Movement Variability are Represented by Iarge-Scale Brain Networks. (Johns Hopkins Research Data Repository, 2023).