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Robust neuronal dynamics in premotor cortex during motor planning
Open accessAbstract
Neural activity maintains representations that bridge past and future events, often over many seconds. Network models can produce persistent and ramping activity, but the positive feedback that is critical for these slow dynamics can cause sensitivity to perturbations. Here we use electrophysiology and optogenetic perturbations in the mouse premotor cortex to probe the robustness of persistent neural representations during motor planning. We show that preparatory activity is remarkably robust to large-scale unilateral silencing: detailed neural dynamics that drive specific future movements were quickly and selectively restored by the network. Selectivity did not recover after bilateral silencing of the premotor cortex. Perturbations to one hemisphere are thus corrected by information from the other hemisphere. Corpus callosum bisections demonstrated that premotor cortex hemispheres can maintain preparatory activity independently. Redundancy across selectively coupled modules, as we observed in the premotor cortex, is a hallmark of robust control systems. Network models incorporating these principles show robustness that is consistent with data.
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“Serial transformation of sensory inputs along bottom–up hierarchical pathways has been observed in rodents engaged in whisker-discrimination tasks (8, 9) with an increasingly stronger association with perceptual choice in S2 (10, 11) and premotor areas (12–14) rather than whisker-related wS1 (9).”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [13]
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“Therefore, this global regulation is unlikely to originate directly from frontal cortical premotor areas (12–14) since frontal cortices have a high degree of symmetry for both ipsilateral and contralateral projections (59).”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [13]
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“Hence, peak 4 is likely to reflect participation of the primary somatosensory cortex in motor preparatory activity, often observed in higher motor cortices (12–14).”
From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [13]
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Orbitofrontal cortex populations are differentially recruited to support actions
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Controlling brain dynamics: Landscape and transition path for working memory
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“…which is a major component of BGMT, or the ALM premotor cortex, through either optogenetic or muscimol inactivation selectively disrupts contralateral licking, while leaving ipsilateral licking unaffected (Li et al., 2015, Li et al., 2016, Chen et al., 2017, Guo et al., 2017, Svoboda and Li, 2017).”
BackgroundA novel device for real-time measurement and manipulation of licking behavior in head-fixed mice.
Williams, B., Speed, A., & Haider, B. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00500.2018 · Cited by 14
“We detected licks at both detectors and then used these signals to cause real-time laser illumination of the left ALM on a fraction of trials; ALM has been shown to be intimately involved in generating licking during perceptual tasks (Li et al. 2016).”
MethodRajan, R. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3003-17.2018 · Cited by 14
“These were classified as putative HVCRA-projecting neurons based on previous descriptions of such neurons (Hahnloser et al., 2002; Kozhevnikov and Fee, 2007; Long et al., 2010).”
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“…also make motor preparation robust to transient unilateral perturbations in cortical state, since both motor behavior and task-relevant neural population dynamics are rapidly restored after contralateral, but not bilateral, optogenetic silencing of premotor cortex in rodents (Li et al., 2016).”
Melodic Priming of Motor Sequence Performance: The Role of the Dorsal Premotor Cortex
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“Interestingly, this finding is compatible with recent evidence from animal literature indicating considerable robustness of neural representations that drive specific future movements after silencing PMC in one hemisphere (Li et al., 2016).”
ResultYan, H., Coughlin, C., Smolin, L., & Wang, J. (2024) · Advancement of science · doi:10.1002/advs.202405309 · Cited by 13
A multi-region recurrent circuit for evidence accumulation in rats
Gupta, D., Kopec, C. D., Bondy, A. G., Luo, T. Z., Elliott, V. A., & Brody, C. (2024) · bioRxiv · doi:10.1101/2024.07.08.602544 · Cited by 13
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InfluentialVisuo-vestibular heading perception: a model system to study multi-sensory decision making
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Emergence of preparatory dynamics in VIP interneurons during motor learning
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An Introduction to Emergence Dynamics in Complex Systems
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Brain-wide analysis reveals movement encoding structured across and within brain areas
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Self-citationAssessing Cross-Contamination in Spike-Sorted Electrophysiology Data
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“This anticipatory change in FC may reflect motor planning 2,50,51 and locomotion initiation 40,41,44,45 processes associated with upstream regions.”
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BackgroundMethodInhibitory control of synaptic signals preceding locomotion in mouse frontal cortex
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ResultTakagi, Y., Hunt, L. T., Woolrich, M. W., Behrens, T. E. J., & Klein-Flügge, M. C. (2021) · eLife · doi:10.7554/elife.60988 · Cited by 20
“…Morcos and Harvey, 2016; Raposo et al., 2014), the critical stages of movement preparation and reaching in premotor and motor cortices (Churchland et al., 2012; Kaufman et al., 2014; Li et al., 2016), and the mechanisms underlying working memory in prefrontal cortex (PFC) (Murray et al., 2017).”
BackgroundInfluentialApproximate any nonlinear system with spiking artificial neural networks: no training required
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Sensing the Environment With Whiskers
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Attention Decorrelates Sensory and Motor Signals in the Mouse Visual CortexPreprint
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“Previous work suggests that this may hold in certain cases, in response to changes in stimulus statistics [42,43], or optogonetic perturbations [44].”
BackgroundCorrigendum: Robust neuronal dynamics in premotor cortex during motor planning
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Self-citationDurá-Bernal, S., Neymotin, S. A., Suter, B. A., Shepherd, G. M., & Lytton, W. W. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/201707 · Cited by 11
“Overall firing rates ranged up to 20 Hz for excitatory populations, with 40 Hz for inhibitory populations, consistent with the in vivo recordings from multiple cortical areas in rat and mouse [23, 35, 50, 13].”
BackgroundBrain–computer interfaces as a causal probe for scientific inquiry
Motiwala, A., Soldado-Magraner, J., Batista, A. P., Smith, M. A., & Yu, B. M. (2025) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2025.06.017 · Cited by 7
“Forexample,prefrontal[118], premotor [119], and motor [98] circuits have been shown to exhibit robustness to large-scale, non-natural activity perturbations, potentially through mechanisms that involve neural population-level properties [118], inter-hemispheric communication [119], or maintaining…”
Disentangling the Roles of Distinct Cell Classes with Cell-Type Dynamical Systems
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BackgroundStable choice coding in rat frontal orienting fields across model-predicted changes of mind
Boyd-Meredith, J. T., Piet, A. T., Dennis, E. J., Hady, A. E., & Brody, C. D. (2022) · Nature Communications · doi:10.1038/s41467-022-30736-3 · Cited by 16
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A midbrain - thalamus - cortex circuit reorganizes cortical dynamics to initiate planned movement
Inagaki, H. K., Chen, S.-S., Ridder, M., Sah, P., Li, N., Yang, Z., Hasanbegović, H., Gao, Z.-Y., Gerfen, C., & Svoboda, K. (2020) · bioRxiv · doi:10.1101/2020.12.16.423127 · Cited by 10
“Consistent with previous studies, this direction contains almost all movement direction-selective activity before the Go cue and allows decoding of lick direction one second before movement (Figures 1E and S1I) (Li et al., 2016; Inagaki et al., 2019).”
BackgroundResultInfluentialSelf-citationSpatiotemporal limits of optogenetic manipulations in cortical circuitsPreprint
Li, N., Chen, S., Guo, Z. V., Chen, H., Huo, Y., Inagaki, H., Davis, C., Hansel, D., Guo, C., & Svoboda, K. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/642215 · Cited by 11
“Activity in a brain region can be robust to perturbation of a strongly connected brain region (Li et al., 2016), yet perturbation of other connected brain regions can have a dramatic effect (Guo et al.”
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“…captured stimulus-evoked activity in the first 600 ms of the trial; the choice dimension separated left and right trials during the delay period (600 ms before the go cue); and the response dimension distinguished left and right licks 350 ms after the go cue (Li et al. 2016; Chen et al. 2024) (Fig.”
InfluentialSelf-citationMulti-region coordination of evidence accumulation and decision commitment in the brainPreprint
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Stimulation of caudal inferior and middle frontal gyri disrupts planning during spoken interaction
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“This prominence is attributed to its crucial role in motion planning and movement control, especially concerning the hands and eyes [30], [31], [32].”
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“Such a distributed computation creates some degree of robustness against local perturbations (Li et al. 2016).”
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“Using this framework, most studies have analyzed how distinct information features about stimuli [92,93] or motor actions [94,95] were encoded into lower-dimensional population activity subspaces, i.e. firing-rate subspaces that were of lower rank than the number of recorded neurons.”
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Xu, D., Chen, Y., Delgado, Á., Hughes, N. C., Zhang, L., Dong, M., & O'Connor, D. H. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/783050 · Cited by 9
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“Perturbations to the delay period neural activities cause changes in the animal’s subsequent report of the remembered stimulus representation (Li et al., 2016; Wimmer et al., 2014).”
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“This was also reflected in the angular separation of activity axes (modes) [86] for movement and visual responses: in layer 3, the angle between activity axes was larger when the network did not learn and this followed from most units being unresponsive to movement inputs, thereby increasing the dissimilarity between…”
BackgroundCompetitive state of movements during planning predicts sequence performance
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“To test this, we designed an analysis which uses the top selective neurons of each familiar corridor to create a coding direction axis [30] (Figure 2g,h).”
MethodAn adaptive behavioral control motif mediated by cortical axo-axonic inhibition
Jung, K., Chang, M., Steinecke, A., Burke, B., Choi, Y., Oisi, Y., Fitzpatrick, D., Taniguchi, H., & Kwon, H. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01380-x · Cited by 18
Redundant representations are required to disambiguate simultaneously presented complex stimuli
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“However, our work shows that redundancy between the stimulus representations present in different brain regions is necessary to disambiguating multiple stimuli—other potentialy benefits of redundancy across and within brain regions are robustness to noise [50], damage, and interference [55].”
tension: A Python package for FORCE learning
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“Other nodes of the network could change their activity in responses to the inactivation, compensating for its effects (Li et al. 2016).”
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“Preparatory signals in pre- and primary motor cortex are thought to converge on an ideal population state, or initial condition, such that internal circuit dynamics will guide appropriate patterns of activity for the upcoming movement [24,26,27,74].”
BackgroundSubthreshold basis for reward-predictive persistent activity in mouse prefrontal cortex
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BackgroundFrom mouse to man—a bridge too far?
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“One formulation of this idea is movement-potent vs movement-null dimensions of population activity (Druckmann and Chklovskii, 2012; Kaufman et al., 2014; Li et al., 2016; Shenoy et al., 2013).”
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Dynamic consensus-building between neocortical areas via long-range connectionsPreprint
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Active learning of neural population dynamics using two-photon holographic optogenetics
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“…enabled neuroscientists to generate and test a multitude of hypotheses about how specific neural populations support the neural computations that underlie, for example, motor control [2–4], motor timing [5, 6], decision making [7–10], working memory [11], social behavior [12], and learning [13–16].”
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“The DRN is a major source of 5-HTergic neurons (Huang et al. 2019 ), with the 5-HT system critically regulating mood, stress responses, and drug reward processing (Liu et al. 2014 ; Li et al. 2016b).”
Specialized structure of neural population codes in parietal cortex outputs
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“In contrast, contralateral PPC projections carried less information about the task, implying that cross-hemisphere interactions serve a role other than computing specific task quantities and may instead help maintain activity patterns 56 .”
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Metadata
- Authors
- Li, N., Daie, K., Svoboda, K., & Druckmann, S.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Svoboda, Karel
- Druckmann, Shaul
- Venue
- Nature
- Published
- 2016-04-13
- Volume
- 532
- Issue
- 7600
- Pages
- 459-464
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5081260
- OpenAlex
- W2336155947
- Cited by
- 492
- References
- 53
- Citations by year
- 2026: 39 · 2025: 52 · 2024: 55 · 2023: 56 · 2022: 51 · 2021: 59 · 2020: 50 · 2019: 41 · 2018: 39 · 2017: 37 · 2016: 13
- FWCI
- 27.58
- Type
- journal article
- Language
- en
- Update notices
- erratum (2016-06-29)
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- premotor cortex, motor planning, preparatory activity, network robustness, interhemispheric connectivity, network redundancy, working memory, optogenetic perturbation, mouse cortex, network models
- MeSH terms
- Animals, Brain Mapping, Corpus Callosum, Female, Light, Male, Memory, Short-Term, Models, Neurological, Motor Cortex, Movement, Neurons, Mice, Executive Function, Optogenetics
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