Skip to main content
NCBI home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1998 Aug 29;353(1373):1307–1317. doi: 10.1098/rstb.1998.0285

Converging levels of analysis in the cognitive neuroscience of visual attention.

J Duncan 1
PMCID: PMC1692330  PMID: 9770224

Abstract

Experiments using behavioural, lesion, functional imaging and single neuron methods are considered in the context of a neuropsychological model of visual attention. According to this model, inputs compete for representation in multiple visually responsive brain systems, sensory and motor, cortical and subcortical. Competition is biased by advance priming of neurons responsive to current behavioural targets. Across systems competition is integrated such that the same, selected object tends to become dominant throughout. The behavioural studies reviewed concern divided attention within and between modalities. They implicate within-modality competition as one main restriction on concurrent stimulus identification. In contrast to the conventional association of lateral attentional focus with parietal lobe function, the lesion studies show attentional bias to be a widespread consequence of unilateral cortical damage. Although the clinical syndrome of unilateral neglect may indeed be associated with parietal lesions, this probably reflects an assortment of further deficits accompanying a simple attentional imbalance. The functional imaging studies show joint involvement of lateral prefrontal and occipital cortex in lateral attentional focus and competition. The single unit studies suggest how competition in several regions of extrastriate cortex is biased by advance priming of neurons responsive to current behavioural targets. Together, the concepts of competition, priming and integration allow a unified theoretical approach to findings from behavioural to single neuron levels.

Full Text

The Full Text of this article is available as a PDF (298.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Broadbent D. E., Broadbent M. H. From detection to identification: response to multiple targets in rapid serial visual presentation. Percept Psychophys. 1987 Aug;42(2):105–113. doi: 10.3758/bf03210498. [DOI] [PubMed] [Google Scholar]
  2. Bundesen C. A theory of visual attention. Psychol Rev. 1990 Oct;97(4):523–547. doi: 10.1037/0033-295x.97.4.523. [DOI] [PubMed] [Google Scholar]
  3. Bushnell M. C., Goldberg M. E., Robinson D. L. Behavioral enhancement of visual responses in monkey cerebral cortex. I. Modulation in posterior parietal cortex related to selective visual attention. J Neurophysiol. 1981 Oct;46(4):755–772. doi: 10.1152/jn.1981.46.4.755. [DOI] [PubMed] [Google Scholar]
  4. Butter C. M., Rapcsak S., Watson R. T., Heilman K. M. Changes in sensory inattention, directional motor neglect and "release" of the fixation reflex following a unilateral frontal lesion: a case report. Neuropsychologia. 1988;26(4):533–545. doi: 10.1016/0028-3932(88)90110-8. [DOI] [PubMed] [Google Scholar]
  5. Chelazzi L., Miller E. K., Duncan J., Desimone R. A neural basis for visual search in inferior temporal cortex. Nature. 1993 May 27;363(6427):345–347. doi: 10.1038/363345a0. [DOI] [PubMed] [Google Scholar]
  6. Corbetta M., Miezin F. M., Shulman G. L., Petersen S. E. A PET study of visuospatial attention. J Neurosci. 1993 Mar;13(3):1202–1226. doi: 10.1523/JNEUROSCI.13-03-01202.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Desimone R., Duncan J. Neural mechanisms of selective visual attention. Annu Rev Neurosci. 1995;18:193–222. doi: 10.1146/annurev.ne.18.030195.001205. [DOI] [PubMed] [Google Scholar]
  8. Duncan J. Coordination of what and where in visual attention. Perception. 1993;22(11):1261–1270. doi: 10.1068/p221261. [DOI] [PubMed] [Google Scholar]
  9. Duncan J., Humphreys G., Ward R. Competitive brain activity in visual attention. Curr Opin Neurobiol. 1997 Apr;7(2):255–261. doi: 10.1016/s0959-4388(97)80014-1. [DOI] [PubMed] [Google Scholar]
  10. Duncan J., Martens S., Ward R. Restricted attentional capacity within but not between sensory modalities. Nature. 1997 Jun 19;387(6635):808–810. doi: 10.1038/42947. [DOI] [PubMed] [Google Scholar]
  11. Duncan J., Nimmo-Smith I. Objects and attributes in divided attention: surface and boundary systems. Percept Psychophys. 1996 Oct;58(7):1076–1084. doi: 10.3758/bf03206834. [DOI] [PubMed] [Google Scholar]
  12. Duncan J. Perceptual selection based on alphanumeric class: evidence from partial reports. Percept Psychophys. 1983 Jun;33(6):533–547. doi: 10.3758/bf03202935. [DOI] [PubMed] [Google Scholar]
  13. Duncan J. Selective attention and the organization of visual information. J Exp Psychol Gen. 1984 Dec;113(4):501–517. doi: 10.1037//0096-3445.113.4.501. [DOI] [PubMed] [Google Scholar]
  14. Duncan J. Similarity between concurrent visual discriminations: dimensions and objects. Percept Psychophys. 1993 Oct;54(4):425–430. doi: 10.3758/bf03211764. [DOI] [PubMed] [Google Scholar]
  15. Duncan J. The locus of interference in the perception of simultaneous stimuli. Psychol Rev. 1980 May;87(3):272–300. [PubMed] [Google Scholar]
  16. Duncan J., Ward R., Shapiro K. Direct measurement of attentional dwell time in human vision. Nature. 1994 May 26;369(6478):313–315. doi: 10.1038/369313a0. [DOI] [PubMed] [Google Scholar]
  17. Funahashi S., Bruce C. J., Goldman-Rakic P. S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol. 1989 Feb;61(2):331–349. doi: 10.1152/jn.1989.61.2.331. [DOI] [PubMed] [Google Scholar]
  18. Fuster J. M., Bauer R. H., Jervey J. P. Functional interactions between inferotemporal and prefrontal cortex in a cognitive task. Brain Res. 1985 Mar 25;330(2):299–307. doi: 10.1016/0006-8993(85)90689-4. [DOI] [PubMed] [Google Scholar]
  19. Gado M., Hanaway J., Frank R. Functional anatomy of the cerebral cortex by computed tomography. J Comput Assist Tomogr. 1979 Feb;3(1):1–19. doi: 10.1097/00004728-197902000-00001. [DOI] [PubMed] [Google Scholar]
  20. Gnadt J. W., Andersen R. A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp Brain Res. 1988;70(1):216–220. doi: 10.1007/BF00271862. [DOI] [PubMed] [Google Scholar]
  21. Goldman-Rakic P. S. Topography of cognition: parallel distributed networks in primate association cortex. Annu Rev Neurosci. 1988;11:137–156. doi: 10.1146/annurev.ne.11.030188.001033. [DOI] [PubMed] [Google Scholar]
  22. Gottlieb J. P., Kusunoki M., Goldberg M. E. The representation of visual salience in monkey parietal cortex. Nature. 1998 Jan 29;391(6666):481–484. doi: 10.1038/35135. [DOI] [PubMed] [Google Scholar]
  23. Guariglia C., Antonucci G. Personal and extrapersonal space: a case of neglect dissociation. Neuropsychologia. 1992 Nov;30(11):1001–1009. doi: 10.1016/0028-3932(92)90051-m. [DOI] [PubMed] [Google Scholar]
  24. Heilman K. M., Valenstein E. Frontal lobe neglect in man. Neurology. 1972 Jun;22(6):660–664. doi: 10.1212/wnl.22.6.660. [DOI] [PubMed] [Google Scholar]
  25. Heinze H. J., Mangun G. R., Burchert W., Hinrichs H., Scholz M., Münte T. F., Gös A., Scherg M., Johannes S., Hundeshagen H. Combined spatial and temporal imaging of brain activity during visual selective attention in humans. Nature. 1994 Dec 8;372(6506):543–546. doi: 10.1038/372543a0. [DOI] [PubMed] [Google Scholar]
  26. Husain M., Shapiro K., Martin J., Kennard C. Abnormal temporal dynamics of visual attention in spatial neglect patients. Nature. 1997 Jan 9;385(6612):154–156. doi: 10.1038/385154a0. [DOI] [PubMed] [Google Scholar]
  27. Karnath H. O. Deficits of attention in acute and recovered visual hemi-neglect. Neuropsychologia. 1988;26(1):27–43. doi: 10.1016/0028-3932(88)90028-0. [DOI] [PubMed] [Google Scholar]
  28. Kwon S. E., Heilman K. M. Ipsilateral neglect in a patient following a unilateral frontal lesion. Neurology. 1991 Dec;41(12):2001–2004. doi: 10.1212/wnl.41.12.2001. [DOI] [PubMed] [Google Scholar]
  29. Lappin J. S. Attention in the identification of stimuli in complex visual displays. J Exp Psychol. 1967 Nov;75(3):321–328. doi: 10.1037/h0025044. [DOI] [PubMed] [Google Scholar]
  30. Luck S. J., Chelazzi L., Hillyard S. A., Desimone R. Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J Neurophysiol. 1997 Jan;77(1):24–42. doi: 10.1152/jn.1997.77.1.24. [DOI] [PubMed] [Google Scholar]
  31. Merikle P. M. Selection from visual persistence by perceptual groups and category membership. J Exp Psychol Gen. 1980 Sep;109(3):279–295. doi: 10.1037//0096-3445.109.3.279. [DOI] [PubMed] [Google Scholar]
  32. Mesulam M. M. A cortical network for directed attention and unilateral neglect. Ann Neurol. 1981 Oct;10(4):309–325. doi: 10.1002/ana.410100402. [DOI] [PubMed] [Google Scholar]
  33. Mesulam M. M. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol. 1990 Nov;28(5):597–613. doi: 10.1002/ana.410280502. [DOI] [PubMed] [Google Scholar]
  34. Mijović-Prelec D., Shin L. M., Chabris C. F., Kosslyn S. M. When does "no" really mean "yes"? A case study in unilateral visual neglect. Neuropsychologia. 1994 Feb;32(2):151–158. doi: 10.1016/0028-3932(94)90002-7. [DOI] [PubMed] [Google Scholar]
  35. Miller E. K., Erickson C. A., Desimone R. Neural mechanisms of visual working memory in prefrontal cortex of the macaque. J Neurosci. 1996 Aug 15;16(16):5154–5167. doi: 10.1523/JNEUROSCI.16-16-05154.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Milner A. D., Harvey M. Distortion of size perception in visuospatial neglect. Curr Biol. 1995 Jan 1;5(1):85–89. doi: 10.1016/s0960-9822(95)00020-0. [DOI] [PubMed] [Google Scholar]
  37. Miyashita Y., Chang H. S. Neuronal correlate of pictorial short-term memory in the primate temporal cortex. Nature. 1988 Jan 7;331(6151):68–70. doi: 10.1038/331068a0. [DOI] [PubMed] [Google Scholar]
  38. Moran J., Desimone R. Selective attention gates visual processing in the extrastriate cortex. Science. 1985 Aug 23;229(4715):782–784. doi: 10.1126/science.4023713. [DOI] [PubMed] [Google Scholar]
  39. Motter B. C. Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J Neurophysiol. 1993 Sep;70(3):909–919. doi: 10.1152/jn.1993.70.3.909. [DOI] [PubMed] [Google Scholar]
  40. Motter B. C. Neural correlates of attentive selection for color or luminance in extrastriate area V4. J Neurosci. 1994 Apr;14(4):2178–2189. doi: 10.1523/JNEUROSCI.14-04-02178.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Niki H., Watanabe M. Prefrontal unit activity and delayed response: relation to cue location versus direction of response. Brain Res. 1976 Mar 19;105(1):79–88. doi: 10.1016/0006-8993(76)90924-0. [DOI] [PubMed] [Google Scholar]
  42. Nobre A. C., Sebestyen G. N., Gitelman D. R., Mesulam M. M., Frackowiak R. S., Frith C. D. Functional localization of the system for visuospatial attention using positron emission tomography. Brain. 1997 Mar;120(Pt 3):515–533. doi: 10.1093/brain/120.3.515. [DOI] [PubMed] [Google Scholar]
  43. Ostry D., Moray N., Marks G. Attention, practice, and semantic targets. J Exp Psychol Hum Percept Perform. 1976 Aug;2(3):326–336. doi: 10.1037//0096-1523.2.3.326. [DOI] [PubMed] [Google Scholar]
  44. Pashler H. Dual-task interference in simple tasks: data and theory. Psychol Bull. 1994 Sep;116(2):220–244. doi: 10.1037/0033-2909.116.2.220. [DOI] [PubMed] [Google Scholar]
  45. Paus T., Kalina M., Patocková L., Angerová Y., Cerný R., Mecir P., Bauer J., Krabec P. Medial vs lateral frontal lobe lesions and differential impairment of central-gaze fixation maintenance in man. Brain. 1991 Oct;114(Pt 5):2051–2067. doi: 10.1093/brain/114.5.2051. [DOI] [PubMed] [Google Scholar]
  46. Phaf R. H., Van der Heijden A. H., Hudson P. T. SLAM: a connectionist model for attention in visual selection tasks. Cogn Psychol. 1990 Jul;22(3):273–341. doi: 10.1016/0010-0285(90)90006-p. [DOI] [PubMed] [Google Scholar]
  47. Posner M. I., Walker J. A., Friedrich F. J., Rafal R. D. Effects of parietal injury on covert orienting of attention. J Neurosci. 1984 Jul;4(7):1863–1874. doi: 10.1523/JNEUROSCI.04-07-01863.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Raymond J. E., Shapiro K. L., Arnell K. M. Temporary suppression of visual processing in an RSVP task: an attentional blink? . J Exp Psychol Hum Percept Perform. 1992 Aug;18(3):849–860. doi: 10.1037//0096-1523.18.3.849. [DOI] [PubMed] [Google Scholar]
  49. Robertson I. H., North N. T. One hand is better than two: motor extinction of left hand advantage in unilateral neglect. Neuropsychologia. 1994 Jan;32(1):1–11. doi: 10.1016/0028-3932(94)90064-7. [DOI] [PubMed] [Google Scholar]
  50. Robertson I. Anomalies in the laterality of omissions in unilateral left visual neglect: implications for an attentional theory of neglect. Neuropsychologia. 1989;27(2):157–165. doi: 10.1016/0028-3932(89)90168-1. [DOI] [PubMed] [Google Scholar]
  51. Shibuya H. Efficiency of visual selection in duplex and conjunction conditions in partial report. Percept Psychophys. 1993 Dec;54(6):716–732. doi: 10.3758/bf03211797. [DOI] [PubMed] [Google Scholar]
  52. Treisman A. M., Gelade G. A feature-integration theory of attention. Cogn Psychol. 1980 Jan;12(1):97–136. doi: 10.1016/0010-0285(80)90005-5. [DOI] [PubMed] [Google Scholar]
  53. Treisman A., Kahneman D., Burkell J. Perceptual objects and the cost of filtering. Percept Psychophys. 1983 Jun;33(6):527–532. doi: 10.3758/bf03202934. [DOI] [PubMed] [Google Scholar]
  54. Treue S., Maunsell J. H. Attentional modulation of visual motion processing in cortical areas MT and MST. Nature. 1996 Aug 8;382(6591):539–541. doi: 10.1038/382539a0. [DOI] [PubMed] [Google Scholar]
  55. Vallar G., Rusconi M. L., Bignamini L., Geminiani G., Perani D. Anatomical correlates of visual and tactile extinction in humans: a clinical CT scan study. J Neurol Neurosurg Psychiatry. 1994 Apr;57(4):464–470. doi: 10.1136/jnnp.57.4.464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Vandenberghe R., Duncan J., Dupont P., Ward R., Poline J. B., Bormans G., Michiels J., Mortelmans L., Orban G. A. Attention to one or two features in left or right visual field: a positron emission tomography study. J Neurosci. 1997 May 15;17(10):3739–3750. doi: 10.1523/JNEUROSCI.17-10-03739.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Vandenberghe R., Dupont P., De Bruyn B., Bormans G., Michiels J., Mortelmans L., Orban G. A. The influence of stimulus location on the brain activation pattern in detection and orientation discrimination. A PET study of visual attention. Brain. 1996 Aug;119(Pt 4):1263–1276. doi: 10.1093/brain/119.4.1263. [DOI] [PubMed] [Google Scholar]
  58. Vecera S. P., Farah M. J. Does visual attention select objects or locations? J Exp Psychol Gen. 1994 Jun;123(2):146–160. doi: 10.1037//0096-3445.123.2.146. [DOI] [PubMed] [Google Scholar]
  59. Walley R. E., Weiden T. D. Lateral inhibition and cognitive masking: a neuropsychological theory of attention. Psychol Rev. 1973 Jul;80(4):284–302. doi: 10.1037/h0035007. [DOI] [PubMed] [Google Scholar]
  60. Zeki S. M. Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. J Physiol. 1978 Apr;277:273–290. doi: 10.1113/jphysiol.1978.sp012272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. di Pellegrino G., Wise S. P. Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate. J Neurosci. 1993 Mar;13(3):1227–1243. doi: 10.1523/JNEUROSCI.13-03-01227.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES