Cited by 210Neural dynamics and brain functionTactile and Sensory InteractionsVisual perception and processing mechanisms

Sensory and decision-related activity propagate in a cortical feedback loop during touch perception

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Kwon, Sung Eun, Yang, Hongdian, Minamisawa, Genki, O'Connor, Daniel H·2016·Nature Neuroscience

Abstract

The brain transforms physical sensory stimuli into meaningful perceptions. In animals making choices about sensory stimuli, neuronal activity in successive cortical stages reflects a progression from sensation to decision. Feedforward and feedback pathways connecting cortical areas are critical for this transformation. However, the computational functions of these pathways are poorly understood because pathway-specific activity has rarely been monitored during a perceptual task. Using cellular-resolution, pathway-specific imaging, we measured neuronal activity across primary (S1) and secondary (S2) somatosensory cortices of mice performing a tactile detection task. S1 encoded the stimulus better than S2, while S2 activity more strongly reflected perceptual choice. S1 neurons projecting to S2 fed forward activity that predicted choice. Activity encoding touch and choice propagated in an S1-S2 loop along feedforward and feedback axons. Our results suggest that sensory inputs converge into a perceptual outcome as feedforward computations are reinforced in a feedback loop.

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  • wS1 neurons projecting to S2 increase their spike rate and predict choice.

    “In particular, wS1 neurons projecting to S2 were found to increase their spike rate, predicting the choice (20, 22).”

    From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [22]

    The Results section (‘Feedforward propagation of task-related activity’; page unavailable) reports larger responses on Hit than Miss trials in S1 neurons projecting to S2 and a stronger association with perceptual choice. It measured those responses with calcium imaging (ΔF/F0), however, rather than reporting an increase in spike rate. (LLM, conf=0.87)

    Experimental — accuracy not yet measured
  • The primary sensory cortex not only retains relatively weak and sparse choice-related activity but also, in this naturalistic behavioral task, directly participates in categorical coding of an all-or-none decision variable into which the majority of neural populations are recruited.

    “These observations indicate that the primary sensory cortex not only retains relatively weak and sparse choice-related activity, as it was shown previously (10, 11, 19–25), but also, in our naturalistic behavioral task, directly participates in a categorical coding of all-or-none DV into which the majority of neural populations are recruited.”

    From Neural correlates of perceptual decision-making in the primary somatosensory cortex (2026) · cites this paper as [22]

    Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

    Experimental — accuracy not yet measured
  • Neural activity in subpopulations of layer 2/3 wS1 neurons is correlated with behavioral choice.

    “More recent experiments (22–25) have shown neural activity in subpopulations of layer 2/3 of wS1 neurons is correlated with behavioral choice.”
  • Sensory S1 and S2 cortices have strongly lateralized ipsilateral outputs and are densely and reciprocally interconnected, forming a top-down feedback loop that exhibits choice-related activity.

    “In contrast, sensory S1 and S2 cortices have strongly lateralized ipsilateral outputs (43, 59) and are densely and reciprocally interconnected (60) forming a top–down feedback loop that exhibits choice-related activity (10, 11, 22–25).”

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Research works printed but not linked: 49

  1. [1]de Lafuente V Romo R Neural correlate of subjective sensory experience gradually builds up across cortical areas Proc Natl Acad Sci U S A 2006 103 14266 14271 16924098 PMC1551903
  2. [3]Gilbert CD Li W Top-down influences on visual processing Nat Rev Neurosci 2013 14 350 363 23595013 PMC3864796
  3. [5]Cauller L Layer I of primary sensory neocortex: where top-down converges upon bottom-up Behav Brain Res 1995 71 163 170 8747184
  4. [6]Hopfield JJ Neural networks and physical systems with emergent collective computational abilities Proc Natl Acad Sci U S A 1982 79 2554 2558 6953413 PMC346238
  5. [7]Douglas RJ Koch C Mahowald M Martin KA Suarez HH Recurrent excitation in neocortical circuits Science 1995 269 981 985 7638624
  6. [8]Seung HS The Handbook of Brain Theory and Neural Networks 2003 MIT Press 94 97
  7. [9]Murphy BK Miller KD Balanced amplification: a new mechanism of selective amplification of neural activity patterns Neuron 2009 61 635 648 19249282 PMC2667957
  8. [10]Wang XJ Probabilistic decision making by slow reverberation in cortical circuits Neuron 2002 36 955 968 12467598
  9. [11]Douglas RJ Martin KA Opening the grey box Trends Neurosci 1991 14 286 293 1719675
  10. [12]Glickfeld LL Andermann ML Bonin V Reid RC Cortico-cortical projections in mouse visual cortex are functionally target specific Nat Neurosci 2013 16 219 226 23292681 PMC3808876
  11. [13]Petreanu L Activity in motor-sensory projections reveals distributed coding in somatosensation Nature 2012 489 299 303 22922646 PMC3443316
  12. [14]Chen JL Carta S Soldado-Magraner J Schneider BL Helmchen F Behaviour-dependent recruitment of long-range projection neurons in somatosensory cortex Nature 2013 499 336 340 23792559
  13. [15]Chen JL Pathway-specific reorganization of projection neurons in somatosensory cortex during learning Nat Neurosci 2015 26098757
  14. [16]Yamashita T Membrane potential dynamics of neocortical projection neurons driving target-specific signals Neuron 2013 80 1477 1490 24360548
  15. [17]Yamashita T Petersen C Target-specific membrane potential dynamics of neocortical projection neurons during goal-directed behavior Elife 2016 5 PMC4915810 27328320
  16. [18]Makino H Komiyama T Learning enhances the relative impact of top-down processing in the visual cortex Nat Neurosci 2015 18 1116 1122 26167904 PMC4523093
  17. [19]Suter BA Shepherd GM Reciprocal interareal connections to corticospinal neurons in mouse M1 and S2 J Neurosci 2015 35 2959 2974 25698734 PMC4331623
  18. [20]Carvell GE Simons DJ Thalamic and corticocortical connections of the second somatic sensory area of the mouse J Comp Neurol 1987 265 409 427 3693613
  19. [21]Carvell GE Simons DJ Somatotopic organization of the second somatosensory area (SII) in the cerebral cortex of the mouse Somatosens Res 1986 3 213 237 3749662
  20. [22]Kleinfeld D Delaney KR Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage-sensitive dyes J Comp Neurol 1996 375 89 108 8913895
  21. [23]Kwegyir-Afful EE Keller A Response properties of whisker-related neurons in rat second somatosensory cortex J Neurophysiol 2004 92 2083 2092 15163670 PMC2804247
  22. [24]Zuo Y Complementary contributions of spike timing and spike rate to perceptual decisions in rat S1 and S2 cortex Curr Biol 2015 25 357 363 25619766
  23. [25]Chen JL Voigt FF Javadzadeh M Krueppel R Helmchen F Long-range population dynamics of anatomically defined neocortical networks Elife 2016 5 PMC4929001 27218452
  24. [26]Chen TW Ultrasensitive fluorescent proteins for imaging neuronal activity Nature 2013 499 295 300 23868258 PMC3777791
  25. [27]Britten KH Newsome WT Shadlen MN Celebrini S Movshon JA A relationship between behavioral choice and the visual responses of neurons in macaque MT Vis Neurosci 1996 13 87 100 8730992
  26. [28]Parker AJ Newsome WT Sense and the single neuron: probing the physiology of perception Annu Rev Neurosci 1998 21 227 277 9530497
  27. [29]Nienborg H Cohen MR Cumming BG Decision-related activity in sensory neurons: correlations among neurons and with behavior Annu Rev Neurosci 2012 35 463 483 22483043
  28. [30]Shadlen MN Britten KH Newsome WT Movshon JA A computational analysis of the relationship between neuronal and behavioral responses to visual motion J Neurosci 1996 16 1486 1510 8778300 PMC6578557
  29. [32]Huber D Multiple dynamic representations in the motor cortex during sensorimotor learning Nature 2012 484 473 478 22538608 PMC4601999
  30. [33]Cohen MR Kohn A Measuring and interpreting neuronal correlations Nat Neurosci 2011 14 811 819 21709677 PMC3586814
  31. [34]Clancy KB Schnepel P Rao AT Feldman DE Structure of a single whisker representation in layer 2 of mouse somatosensory cortex J Neurosci 2015 35 3946 3958 25740523 PMC4348190
  32. [36]Cauller LJ Clancy B Connors BW Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I J Comp Neurol 1998 390 297 310 9453672
  33. [37]Mao T Long-range neuronal circuits underlying the interaction between sensory and motor cortex Neuron 2011 72 111 123 21982373 PMC5047281
  34. [40]Sachidhanandam S Sreenivasan V Kyriakatos A Kremer Y Petersen CC Membrane potential correlates of sensory perception in mouse barrel cortex Nat Neurosci 2013 16 1671 1677 24097038
  35. [43]Engel TA Chaisangmongkon W Freedman DJ Wang XJ Choice-correlated activity fluctuations underlie learning of neuronal category representation Nat Commun 2015 6 6454 25759251 PMC4382677
  36. [44]Sato TR Svoboda K The functional properties of barrel cortex neurons projecting to the primary motor cortex J Neurosci 2010 30 4256 4260 20335461 PMC6634518
  37. [45]El-Shamayleh Y Kumbhani RD Dhruv NT Movshon JA Visual response properties of V1 neurons projecting to V2 in macaque J Neurosci 2013 33 16594 16605 24133263 PMC3797376
  38. [46]Movshon JA Newsome WT Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys J Neurosci 1996 16 7733 7741 8922429 PMC6579106
  39. [47]Smolyanskaya A Haefner RM Lomber SG Born RT A Modality-Specific Feedforward Component of Choice-Related Activity in MT Neuron 2015 87 208 219 26139374 PMC4512164
  40. [48]Barth AL Poulet JF Experimental evidence for sparse firing in the neocortex Trends Neurosci 2012 35 345 355 22579264
  41. [49]Ramirez A Spatiotemporal receptive fields of barrel cortex revealed by reverse correlation of synaptic input Nat Neurosci 2014 17 866 875 24836076 PMC4203687
  42. [50]Peron SP Freeman J Iyer V Guo C Svoboda K A Cellular Resolution Map of Barrel Cortex Activity during Tactile Behavior Neuron 2015 86 783 799 25913859
  43. [51]Dana H Thy1-GCaMP6 transgenic mice for neuronal population imaging in vivo PLoS One 2014 9 e108697 25250714 PMC4177405
  44. [52]Hippenmeyer S A developmental switch in the response of DRG neurons to ETS transcription factor signaling PLoS Biol 2005 3 e159 15836427 PMC1084331
  45. [53]Madisen L A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing Nat Neurosci 2012 15 793 802 22446880 PMC3337962
  46. [54]O'Connor DH Neural coding during active somatosensation revealed using illusory touch Nat Neurosci 2013 16 958 965 23727820 PMC3695000
  47. [55]Pologruto TA Sabatini BL Svoboda K ScanImage: flexible software for operating laser scanning microscopes Biomed Eng Online 2003 2 13 12801419 PMC161784
  48. [56]O'Connor DH Peron SP Huber D Svoboda K Neural activity in barrel cortex underlying vibrissa-based object localization in mice Neuron 2010 67 1048 1061 20869600
  49. [57]Kerlin AM Andermann ML Berezovskii VK Reid RC Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex Neuron 2010 67 858 871 20826316 PMC3327881

Cited by

Sorted by citations

Authors
Kwon, S. E., Yang, H., Minamisawa, G., & O'Connor, D. H.
Affiliations
Johns Hopkins University (US)
Venue
Nature Neuroscience
Published
2016-07-20
Volume
19
Issue
9
Pages
1243-1249
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
OpenAlex
W2481900801
Cited by
210
References
62
Citations by year
2026: 21 · 2025: 18 · 2024: 21 · 2023: 17 · 2022: 19 · 2021: 27 · 2020: 22 · 2019: 20 · 2018: 27 · 2017: 15 · 2016: 3
FWCI
13.79
Type
journal article
Language
en
Open access
Locations
  • Nature Neuroscience (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • Johns Hopkins University
  • National Institutes of Health
  • Science of Learning Institute, Johns Hopkins University
  • Japan Society for the Promotion of Science
  • National Institute of Neurological Disorders and Stroke (R01NS089652, P30NS050274)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Keywords
tactile perception, somatosensory cortex, primary somatosensory cortex, secondary somatosensory cortex, feedforward pathways, feedback pathways, perceptual decision making, tactile detection, sensory coding
MeSH terms
Action Potentials, Animals, Choice Behavior, Female, Male, Mice, Inbred C57BL, Mice, Transgenic, Neurons, Somatosensory Cortex, Touch, Models, Animal, Touch Perception

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