CoChat
Sign Up
Cited by 6Neural and Behavioral Psychology StudiesVisual perception and processing mechanismsNeural dynamics and brain function

Transient neuronal suppression for exploitation of new sensory evidence

Open access
Shinn, Maxwell, Lee, Daeyeol, Murray, John D., Seo, Hyojung·2022·Nature Communications
DOI 10.1038/s41467-021-27697-4PMC PMC8748884

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

In noisy but stationary environments, decisions should be based on the temporal integration of sequentially sampled evidence. This strategy has been supported by many behavioral studies and is qualitatively consistent with neural activity in multiple brain areas. By contrast, decision-making in the face of non-stationary sensory evidence remains poorly understood. Here, we trained monkeys to identify and respond via saccade to the dominant color of a dynamically refreshed bicolor patch that becomes informative after a variable delay. Animals’ behavioral responses were briefly suppressed after evidence changes, and many neurons in the frontal eye field displayed a corresponding dip in activity at this time, similar to that frequently observed after stimulus onset but sensitive to stimulus strength. Generalized drift-diffusion models revealed consistency of behavior and neural activity with brief suppression of motor output, but not with pausing or resetting of evidence accumulation. These results suggest that momentary arrest of motor preparation is important for dynamic perceptual decision making.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41467-021-27697-4

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Emergence of synchronous modulation, dimensionality collapse, and strong suppression locked to sensory stimulation are known neural correlates of top-down regulated attention and decision-making processes.

    “Emergence of synchronous modulation (33, 34), dimensionality collapse (46), and strong suppression locked to sensory stimulation (47, 48) are known neural correlates of top–down regulated attention (35) and decision-making processes (3–5).”

    From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [48]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

No citation lists for this paper

No citation lists for this paper yet — checked again daily.

References 65 · Cited by 6

Research works printed but not linked: 58

  1. [2]Gold JI Shadlen MN The neural basis of decision making Annu. Rev. Neurosci. 2007 30 535 574 17600525
  2. [3]Hanes DP Schall JD Neural control of voluntary movement initiation Science 1996 274 427 430 8832893
  3. [4]Zoltowski DM Latimer KW Yates JL Huk AC Pillow JW Discrete stepping and nonlinear ramping dynamics underlie spiking responses of LIP neurons during decision-making Neuron 2019 102 1249 1258.e10 31130330
  4. [5]Glaze CM Kable JW Gold JI Normative evidence accumulation in unpredictable environments eLife 2015 4 e08825 PMC4584511 26322383
  5. [6]Wyart V de Gardelle V Scholl J Summerfield C Rhythmic fluctuations in evidence accumulation during decision making in the human brain Neuron 2012 76 847 858 23177968 PMC3975574
  6. [7]Thura D Cisek P Deliberation and commitment in the premotor and primary motor cortex during dynamic decision making Neuron 2014 81 6 1401 1416 24656257
  7. [8]van Maanen L Fontanesi L Hawkins GE Forstmann BU Striatal activation reflects urgency in perceptual decision making NeuroImage 2016 139 294 303 27355435
  8. [9]Derosiere G Thura D Cisek P Duque J Motor cortex disruption delays motor processes but not deliberation about action choices J. Neurophysiol. 2019 122 4 1566 1577 31411932 PMC6843092
  9. [10]Khalighinejad N A basal forebrain-cingulate circuit in macaques decides it is time to act Neuron 2020 105 370 384.e8 31813653 PMC6975166
  10. [11]Sato T Schall J Pre-excitatory pause in frontal eye field responses Exp. Brain Res. 2001 139 53 58 11482843
  11. [14]Ding L Gold JI Neural correlates of perceptual decision making before, during, and after decision commitment in monkey frontal eye field Cereb. Cortex 2011 22 1052 1067 21765183 PMC3328342
  12. [16]Teichert T Grinband J Ferrera V The importance of decision onset J. Neurophysiol. 2016 115 643 661 26609111 PMC4752305
  13. [17]Reingold EM Stampe DM Saccadic inhibition in voluntary and reflexive saccades J. Cogn. Neurosci. 2002 14 371 388 11970798
  14. [18]Akerfelt Annika Visual-tactile saccadic inhibition Exp. Brain Res. 2005 169 554 563 16328301
  15. [20]Logan GD Yamaguchi M Schall JD Palmeri TJ Inhibitory control in mind and brain 2.0: Blocked-input models of saccadic countermanding Psychological Rev. 2015 122 115 147 PMC4556000 25706403
  16. [21]Salinas, E. & Stanford, T. R. Saccadic inhibition interrupts ongoing oculomotor activity to enable the rapid deployment of alternate movement plans. Sci. Rep.8, 14163 (2018). PMC6155112 30242249
  17. [22]Purcell BA Neurally constrained modeling of perceptual decision making Psychological Rev. 2010 117 1113 1143 PMC2979343 20822291
  18. [23]Bompas A Sumner P Saccadic inhibition reveals the timing of automatic and voluntary signals in the human brain J. Neurosci. 2011 31 12501 12512 21880912 PMC6703251
  19. [24]Bompas A Sumner P Saccadic inhibition and the remote distractor effect: One mechanism or two? J. Vis. 2015 15 15 26024462
  20. [25]Wessel JR Aron AR Unexpected events induce motor slowing via a brain mechanism for action-stopping with global suppressive effects J. Neurosci. 2013 33 18481 18491 24259571 PMC3834054
  21. [27]Duque J Greenhouse I Labruna L Ivry RB Physiological markers of motor inhibition during human behavior Trends Neurosci. 2017 40 219 236 28341235 PMC5389740
  22. [28]Shinn M Ehrlich DB Lee D Murray JD Seo H Confluence of Timing and Reward Biases in Perceptual Decision-Making Dynamics J. Neurosci. 2020 40 7326 7342 32839233 PMC7534922
  23. [29]Shinn, M., Lam, N. H. & Murray, J. D. A flexible framework for simulating and fitting generalized drift-diffusion models. eLife9, e56938 (2020). PMC7462609 32749218
  24. [30]Thura D Beauregard-Racine J Fradet C-W Cisek P Decision making by urgency gating: theory and experimental support J. Neurophysiol. 2012 108 11 2912 2930 22993260
  25. [31]Reingold, E. M. & Stampe, D. M. Saccadic Inhibition and Gaze Contingent Research Paradigms. in Reading as a Perceptual Process 119–145 (Elsevier, 2000). 10.1016/b978-008043642-5/50008-5. · DOI
  26. [32]Salinas, E. et al. Voluntary and involuntary contributions to perceptually guided saccadic choices resolved with millisecond precision. eLife8, e46359 (2019). PMC6645714 31225794
  27. [33]Engbert R Kliegl R Microsaccades uncover the orientation of covert attention Vis. Res. 2003 43 1035 1045 12676246
  28. [34]Hafed ZM Ignashchenkova A On the Dissociation between Microsaccade Rate and Direction after Peripheral Cues: Microsaccadic Inhibition Revisited J. Neurosci. 2013 33 16220 16235 24107954 PMC6618351
  29. [35]Buonocore A Alteration of the microsaccadic velocity-amplitude main sequence relationship after visual transients: implications for models of saccade control J. Neurophysiol. 2017 117 1894 1910 28202573 PMC5411461
  30. [36]Wessel, J. R. et al. Surprise disrupts cognition via a fronto-basal ganglia suppressive mechanism. Nat. Commun.7, 11195 (2016). PMC4837448 27088156
  31. [37]White AL Rolfs M Oculomotor inhibition covaries with conscious detection J. Neurophysiol. 2016 116 3 1507 1521 27385794 PMC5040379
  32. [38]Corbetta M Shulman GL Control of goal-directed and stimulus-driven attention in the brain Nat. Rev. Neurosci. 2002 3 201 215 11994752
  33. [39]Peel TR Hafed ZM Dash S Lomber SG Corneil BD A causal role for the cortical frontal eye fields in microsaccade deployment PLOS Biol. 2016 14 e1002531 27509130 PMC4980061
  34. [40]Jun, E. J. et al. Causal role for the primate superior colliculus in the computation of evidence for perceptual decisions. Nat. Neurosci.24, 1121–1131 (2021). PMC8338902 34183869
  35. [41]Huk, A. C. & Meister, M. L. R. Neural correlates and neural computations in posterior parietal cortex during perceptual decision-making. Front. Integr. Neurosci.6, 86 (2012). PMC3467999 23087623
  36. [42]Burman DD Bruce CJ Suppression of task-related saccades by electrical stimulation in the primate\textquotesingles frontal eye field J. Neurophysiol. 1997 77 2252 2267 9163356
  37. [43]Izawa Y Suzuki H Shinoda Y Suppression of visually and memory-guided saccades induced by electrical stimulation of the monkey frontal eye field. II. Suppression of Bilateral Saccades J. Neurophysiol. 2004 92 4 2261 2273 15381745
  38. [44]Tehovnik EJ Slocum WM Schiller PH Behavioural conditions affecting saccadic eye movements elicited electrically from the frontal lobes of primates Eur. J. Neurosci. 1999 11 2431 2443 10383633
  39. [45]Opris I Ferrera VP Barborica A On the gap effect for saccades evoked by electrical microstimulation of frontal eye fields in monkeys Exp. Brain Res. 2001 138 1 7 11374075
  40. [46]Izawa Y Suzuki H Shinoda Y Response properties of fixation neurons and their location in the frontal eye field in the monkey J. Neurophysiol. 2009 102 2410 2422 19675294
  41. [47]Sommer MA Wurtz RH Composition and topographic organization of signals sent from the frontal eye field to the superior colliculus J. Neurophysiol. 2000 83 1979 2001 10758109
  42. [48]Isoda M Hikosaka O Role for subthalamic nucleus neurons in switching from automatic to controlled eye movement J. Neurosci. 2008 28 7209 7218 18614691 PMC2667154
  43. [49]Pasquereau, B. & Turner, R. S. A selective role for ventromedial subthalamic nucleus in inhibitory control. eLife6, e31627 (2017). PMC5730370 29199955
  44. [50]Falkner AL Krishna BS Goldberg ME Surround suppression sharpens the priority map in the lateral intraparietal area J. Neurosci. 2010 30 12787 12797 20861383 PMC2967305
  45. [51]Bollimunta A Ditterich J Local computation of decision-relevant net sensory evidence in parietal cortex Cereb. Cortex 2011 22 903 917 21709177
  46. [52]Ratcliff R Cherian A Segraves M A comparison of macaque behavior and superior colliculus neuronal activity to predictions from models of two-choice decisions J. Neurophysiol. 2003 90 1392 1407 12761282
  47. [53]Li X Kim B Basso MA Transient pauses in delay-period activity of superior colliculus neurons J. Neurophysiol. 2006 95 2252 2264 16394072
  48. [54]Nowak LG Munk MHJ Girard P Bullier J Visual latencies in areas V1 and V2 of the macaque monkey Vis. Neurosci. 1995 12 371 384 7786857
  49. [55]Aosaki T Kimura M Graybiel AM Temporal and spatial characteristics of tonically active neurons of the primate’s striatum J. Neurophysiol. 1995 73 1234 1252 7608768
  50. [56]Ford KA Everling S Neural activity in primate caudate nucleus associated with pro- and antisaccades J. Neurophysiol. 2009 102 2334 2341 19692516
  51. [57]Schulz JM Reynolds JNJ Pause and rebound: sensory control of cholinergic signaling in the striatum Trends Neurosci. 2013 36 41 50 23073210
  52. [58]Brown JW Hanes DP Schall JD Stuphorn V Relation of frontal eye field activity to saccade initiation during a countermanding task Exp. Brain Res. 2008 190 135 151 18604527 PMC2748998
  53. [59]Buonocore A McIntosh RD Saccadic inhibition underlies the remote distractor effect Exp. Brain Res. 2008 191 117 122 18784920
  54. [60]Edelman JA Xu KZ Inhibition of voluntary saccadic eye movement commands by abrupt visual onsets J. Neurophysiol. 2009 101 1222 1234 19019977 PMC2666419
  55. [61]Sokolov EN Higher nervous functions: the orienting reflex Annu. Rev. Physiol. 1963 25 545 580 13977960
  56. [62]Courchesne E Hillyard SA Galambos R Stimulus novelty, task relevance and the visual evoked potential in man Electroencephalogr. Clin. Neurophysiol. 1975 39 131 143 50210
  57. [63]Bisley JW The neural basis of visual attention J. Physiol. 2010 589 49 57 20807786 PMC3039259
  58. [64]Churchland MM Shenoy KV Delay of movement caused by disruption of cortical preparatory activity J. Neurophysiol. 2007 97 348 359 17005608

Authors
Shinn, M., Lee, D., Murray, J. D., & Seo, H.
Affiliations
  • Yale University (US)
  • Johns Hopkins University (US)
Corresponding author
  • Murray, John D.
  • Seo, Hyojung
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2022-01-10
Volume
13
Issue
1
Pages
23-23
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/s41467-021-27697-4
PMC
PMC8748884
OpenAlex
W4225777536
Cited by
6
References
65
Citations by year
2026: 3 · 2023: 3
FWCI
0.39
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Gruber Foundation
  • Gruber Foundation Science Fellowship
  • U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (R01 MH108629)
  • U.S. Department of Health & Human Services | National Institutes of Health (R01 MH112746)
  • National Science Foundation (2015276)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
frontal eye field, saccades, drift-diffusion model, evidence accumulation, motor preparation, color discrimination, variable delay
MeSH terms
Animals, Brain, Decision Making, Frontal Lobe, Macaca mulatta, Male, Neurons, Photic Stimulation, Saccades

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review