Cited by 190Visual perception and processing mechanismsVisual Attention and Saliency DetectionNeural and Behavioral Psychology Studies

Attentional Enhancement via Selection and Pooling of Early Sensory Responses in Human Visual Cortex

Open access
Pestilli, Franco, Carrasco, Marisa, Heeger, David J., Gardner, Justin L.·2011·Neuron

Abstract

The computational processes by which attention improves behavioral performance were characterized by measuring visual cortical activity with functional magnetic resonance imaging as humans performed a contrast-discrimination task with focal and distributed attention. Focal attention yielded robust improvements in behavioral performance accompanied by increases in cortical responses. Quantitative analysis revealed that if performance were limited only by the sensitivity of the measured sensory signals, the improvements in behavioral performance would have corresponded to an unrealistically large reduction in response variability. Instead, behavioral performance was well characterized by a pooling and selection process for which the largest sensory responses, those most strongly modulated by attention, dominated the perceptual decision. This characterization predicts that high-contrast distracters that evoke large responses should negatively impact behavioral performance. We tested and confirmed this prediction. We conclude that attention enhanced behavioral performance predominantly by enabling efficient selection of the behaviorally relevant sensory signals.

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 · 10.1016/j.neuron.2011.09.025

Cites

5 of 5 references verified0 citation errors · 0 not checkable

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?

  • In detection and coarse discrimination tasks, Lau, Rahnev, and colleagues report that subjects overestimate their confidence in the periphery and for unattended stimuli.

    “In detection and coarse discrimination tasks, Lau, Rahnev, and colleagues report that subjects overestimate their confidence in the periphery and for unattended stimuli.”

    From Comparing Bayesian and non-Bayesian accounts of human confidence reports (2018) · cites this paper as [61]

    The Results section on psychophysical contrast-discrimination functions reports lower thresholds with focal than distributed cues, but does not report confidence judgments. Searches for Lau, Rahnev, peripheral confidence, and confidence overestimation found no passage addressing the attributed finding. Page numbers were not available in our copy. (LLM, conf=0.77)

    Experimental — accuracy not yet measured

Self-check

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

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

Cites

Flagged first, then by citations

Research works printed but not linked: 53

  1. Albrecht DG Hamilton DB Striate cortex of monkey and cat: contrast response function J Neurophysiol 1982 48 217 237 7119846
  2. Boudreau CE Williford TH Maunsell JH Effects of task difficulty and target likelihood in area V4 of macaque monkeys J Neurophysiol 2006 96 2377 2387 16855106
  3. Boynton GM Engel SA Glover GH Heeger DJ Linear systems analysis of functional magnetic resonance imaging in human V1 J Neurosci 1996 16 4207 4221 8753882 PMC6579007
  4. Braun J Visual search among items of different salience: removal of visual attention mimics a lesion in extrastriate area V4 J Neurosci 1994 14 554 567 8301354 PMC6576816
  5. Buracas GT Boynton GM The effect of spatial attention on contrast response functions in human visual cortex J Neurosci 2007 27 93 97 17202476 PMC6672290
  6. Carrasco M Penpeci-Talgar C Eckstein M Spatial covert attention increases contrast sensitivity across the CSF: support for signal enhancement Vision Res 2000 40 1203 1215 10788636 PMC3825514
  7. Chen Y Geisler WS Seidemann E Optimal decoding of correlated neural population responses in the primate visual cortex Nat Neurosci 2006 9 1412 1420 17057706 PMC1851689
  8. Cohen MR Maunsell JH Attention improves performance primarily by reducing interneuronal correlations Nat Neurosci 2009 12 1594 1600 19915566 PMC2820564
  9. Cook EP Maunsell JH Attentional modulation of behavioral performance and neuronal responses in middle temporal and ventral intraparietal areas of macaque monkey J Neurosci 2002 22 1994 2004 11880530 PMC6758868
  10. Desimone R Duncan J Neural mechanisms of selective visual attention Annu Rev Neurosci 1995 18 193 222 7605061
  11. Douglas RJ Martin KA Mapping the matrix: the ways of neocortex Neuron 2007 56 226 238 17964242
  12. Eckstein MP Thomas JP Palmer J Shimozaki SS A signal detection model predicts the effects of set size on visual search accuracy for feature, conjunction, triple conjunction, and disjunction displays Percept Psychophys 2000 62 425 451 10909235
  13. Foley JM Schwarz W Spatial attention: effect of position uncertainty and number of distractor patterns on the threshold-versus-contrast function for contrast discrimination Journal of the Optical Society of America 1998 15 11 Section A
  14. Gardner JL Sun P Waggoner RA Ueno K Tanaka K Cheng K Contrast adaptation and representation in human early visual cortex Neuron 2005 47 607 620 16102542 PMC1475737
  15. Geisler WS Albrecht DG Visual cortex neurons in monkeys and cats: detection, discrimination, and identification Vis Neurosci 1997 14 897 919 9364727
  16. Gorea A Sagi D Disentangling signal from noise in visual contrast discrimination Nat Neurosci 2001 4 1146 1150 11687818
  17. Heeger DJ Normalization of cell responses in cat striate cortex Vis Neurosci 1992 9 181 197 1504027
  18. Heeger DJ Huk AC Geisler WS Albrecht DG Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? Nat Neurosci 2000 3 631 633 10862687
  19. Heeger DJ Ress D What does fMRI tell us about neuronal activity? Nat Rev Neurosci 2002 3 142 151 11836522
  20. Herrmann K Montaser-Kouhsari L Carrasco M Heeger DJ When size matters: attention affects performance by contrast or response gain Nat Neurosci 2010 13 1554 1559 21057509 PMC3058765
  21. Jonides J Yantis S Uniqueness of abrupt visual onset in capturing attention Percept Psychophys 1988 43 346 354 3362663
  22. Koch C Ullman S Shifts in selective visual attention: towards the underlying neural circuitry Hum Neurobiol 1985 4 219 227 3836989
  23. Kouh M Poggio T A canonical neural circuit for cortical nonlinear operations Neural Comput 2008 20 1427 1451 18254695
  24. Lee DK Itti L Koch C Braun J Attention activates winner-take-all competition among visual filters Nat Neurosci 1999 2 375 381 10204546
  25. Lee J Maunsell JH The effect of attention on neuronal responses to high and low contrast stimuli J Neurophysiol 2010 104 960 971 20538780 PMC2934943
  26. Legge GE Foley JM Contrast masking in human vision J Opt Soc Am 1980 70 1458 1471 7463185
  27. Li X Lu ZL Tjan BS Dosher BA Chu W Blood oxygenation level-dependent contrast response functions identify mechanisms of covert attention in early visual areas Proc Natl Acad Sci U S A 2008 105 6202 6207 18413602 PMC2329700
  28. Liu T Pestilli F Carrasco M Transient attention enhances perceptual performance and FMRI response in human visual cortex Neuron 2005 45 469 477 15694332 PMC3825510
  29. Logothetis NK Wandell BA Interpreting the BOLD signal Annu Rev Physiol 2004 66 735 769 14977420
  30. Lu ZL Dosher BA External noise distinguishes attention mechanisms Vision Res 1998 38 1183 1198 9666987
  31. Luck SJ Vogel EK The capacity of visual working memory for features and conjunctions Nature 1997 390 279 281 9384378
  32. Martinez-Trujillo J Treue S Attentional modulation strength in cortical area MT depends on stimulus contrast Neuron 2002 35 365 370 12160753
  33. Mitchell JF Sundberg KA Reynolds JH Spatial attention decorrelates intrinsic activity fluctuations in macaque area V4 Neuron 2009 63 879 888 19778515 PMC2765230
  34. Morrone MC Denti V Spinelli D Color and luminance contrasts attract independent attention Curr Biol 2002 12 1134 1137 12121622
  35. Mukamel R Gelbard H Arieli A Hasson U Fried I Malach R Coupling between neuronal firing, field potentials, and FMRI in human auditory cortex Science 2005 309 951 954 16081741
  36. Murray SO The effects of spatial attention in early human visual cortex are stimulus independent J Vis 2008 8 2 1 11 19146344
  37. Nachmias J Sansbury RV Letter: Grating contrast: discrimination may be better than detection Vision Res 1974 14 1039 1042 4432385
  38. Palmer J Moore CM Using a filtering task to measure the spatial extent of selective attention Vision Res 2009 49 1045 1064 18405935 PMC2767212
  39. Palmer J Verghese P Pavel M The psychophysics of visual search Vision Res 2000 40 1227 1268 10788638
  40. Pestilli F Ling S Carrasco M A population-coding model of attention’s influence on contrast response: Estimating neural effects from psychophysical data Vision Res 2009 49 1144 1153 18926845 PMC2743869
  41. Pooresmaeili A Poort J Thiele A Roelfsema PR Separable codes for attention and luminance contrast in the primary visual cortex J Neurosci 2010 30 12701 12711 20861375 PMC6633579
  42. Reynolds JH Heeger DJ The normalization model of attention Neuron 2009 61 168 185 19186161 PMC2752446
  43. Reynolds JH Pasternak T Desimone R Attention increases sensitivity of V4 neurons Neuron 2000 26 703 714 10896165
  44. Sapir A d’Avossa G McAvoy M Shulman GL Corbetta M Brain signals for spatial attention predict performance in a motion discrimination task Proc Natl Acad Sci U S A 2005 102 17810 17815 16306268 PMC1308888
  45. Schiller PH Lee K The role of the primate extrastriate area V4 in vision Science 1991 251 1251 1253 2006413
  46. Sergent C Ruff CC Barbot A Driver J Rees G Top-Down Modulation of Human Early Visual Cortex after Stimulus Offset Supports Successful Postcued Report J Cogn Neurosci 2010 20715902
  47. Shmuel A Augath M Oeltermann A Logothetis NK Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 Nat Neurosci 2006 9 569 577 16547508
  48. Sirotin YB Das A Anticipatory haemodynamic signals in sensory cortex not predicted by local neuronal activity Nature 2009 457 475 479 19158795 PMC2705195
  49. Softky WR Koch C The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs The Journal of neuroscience: the official journal of the Society for Neuroscience 1993 13 334 350 8423479 PMC6576320
  50. Thiele A Pooresmaeili A Delicato LS Herrero JL Roelfsema PR Additive effects of attention and stimulus contrast in primary visual cortex Cereb Cortex 2009 19 2970 2981 19372142 PMC2774399
  51. Vogel EK McCollough AW Machizawa MG Neural measures reveal individual differences in controlling access to working memory Nature 2005 438 500 503 16306992
  52. Yigit-Elliott S Palmer J Moore CM Distinguishing blocking from attenuation in visual selective attention Psychol Sci 2011 22 771 780 21551339 PMC7106067
  53. Zenger-Landolt B Heeger DJ Response suppression in v1 agrees with psychophysics of surround masking J Neurosci 2003 23 6884 6893 12890783 PMC2275204

Cited by

Sorted by citations

Authors
Pestilli, F., Carrasco, M., Heeger, D. J., & Gardner, J. L.
Affiliations
  • RIKEN Center for Brain Science (JP)
  • New York University (US)
Corresponding author
  • Pestilli, Franco
  • Gardner, Justin L.
Venue
Neuron
Publisher
Elsevier BV
Published
2011-12
Volume
72
Issue
5
Pages
832-846
ISSN
0896-6273 (ISSN-L)
OpenAlex
W1967985907
Cited by
190
References
5
Citations by year
2026: 4 · 2025: 12 · 2024: 8 · 2023: 9 · 2022: 12 · 2021: 14 · 2020: 12 · 2019: 13 · 2018: 12 · 2017: 13 · 2016: 15 · 2015: 16 · 2014: 18 · 2013: 12 · 2012: 17
FWCI
7.80
Type
journal article
Language
en
Open access
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • Israel National Road Safety Authority
  • National Institutes of Health (R01-EY016200, R01-EY019693, R01-MH069880)
  • RIKEN Brain Science Institute
  • National Institute of Mental Health (T32-EY1393309, T32-MH05174)
  • National Eye Institute (F32-EY016260)
  • Italian Academy for Advanced Studies in America, Columbia University
  • Burroughs Wellcome Fund
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Visual Attention and Saliency Detection
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
visual attention, focal attention, distributed attention, contrast discrimination, early visual cortex, response variability, perceptual decision making, distractors, behavioral performance
MeSH terms
Adult, Attention, Brain Mapping, Choice Behavior, Cues, Discrimination, Psychological, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Male, Neuropsychological Tests, Oxygen, Photic Stimulation, Psychophysics, Reaction Time, Visual Cortex, Models, Statistical, Contrast Sensitivity

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