On the role of suppression in spatial attention: Evidence from negative bold in human subcortical and cortical structures

Journal of Neuroscience

Volumn 34, Issue 31, 2014, Pages 10347-10360

  Gouws, André D ^a   Alvarez, Ivan ^a   Watson, David M ^a   Uesaki, Maiko ^a   Rogers, Jessica ^a   Morland, Antony B ^a,b  

^a UNIVERSITY OF YORK   (United Kingdom)

^b UNIVERSITY OF HULL   (United Kingdom)

Author keywords

Contrast response; Lateral geniculate nucleus; Negative BOLD; Spatial attention; Suppression; Visual cortex

Indexed keywords

CONTRAST RESPONSE; LATERAL GENICULATE NUCLEUS; NEGATIVE BOLD; SPATIAL ATTENTION; SUPPRESSION; VISUAL CORTEX;

ADULT; ANALYSIS OF VARIANCE; ATTENTION; BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OXYGEN; PHOTIC STIMULATION; SPACE PERCEPTION; YOUNG ADULT;

EID: 84905014947     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0164-14.2014     Document Type: Article

References (63)

1. Allman JM, Kaas JH (1971) A representation of the visual field in the caudal third of the middle tempral gyrus of the owl monkey (Aotus trivirgatus). Brain Res 31: 85-105. CrossRef Medline.
2. Amano K, Wandell BA, Dumoulin SO (2009) Visual field maps, population receptive field sizes, and visual field coverage in the human MTβ complex. J Neurophysiol 102: 2704-2718. CrossRef Medline.
3. Andrews TJ, Halpern SD, Purves D (1997) Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J Neurosci 17: 2859-2868. Medline.
4. Anton-Erxleben K, Stephan VM, Treue S (2009) Attention reshapes centersurround receptive field structure in macaque cortical area MT. Cereb Cortex 19: 2466-2478. CrossRef Medline.
5. Baseler HA, Gouws A, Haak KV, Racey C, Crossland MD, Tufail A, Rubin GS, Cornelissen FW, Morland AB (2011) Large-scale remapping of visual cortex is absent in adult humans with macular degeneration. Nat Neurosci 14: 649-655. CrossRef Medline.
6. Behrens TE, Johansen-Berg H, WoolrichMW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, Thompson AJ, Brady JM, Matthews PM (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6: 750-757. CrossRef Medline.
7. BoyntonGM (2011) Spikes, BOLD, attention, and awareness: a comparison of electrophysiological and fMRI signals in V1. J Vis 11(5): 12. CrossRef Medline.
8. Buracas GT, Boynton GM (2007) The effect of spatial attention on contrast response functions in human visual cortex. J Neurosci 27: 93-97. CrossRef Medline.
9. CarrascoM (2011) Visual attention: the past 25 years. Vision Res 51: 1484-1525. CrossRef Medline.
10. Chalupa LM, Coyle RS, Lindsley DB (1976) Effect of pulvinar lesions on visual pattern discrimination in monkeys. J Neurophysiol 39: 354-369. Medline.
11. Cotton PL, Smith AT (2007) Contralateral visual hemifield representations in the human pulvinar nucleus. J Neurophysiol 98: 1600-1609. CrossRef Medline.
12. Desimone R, Wessinger M, Thomas L, Schneider W (1990) Attentional control of visual perception: cortical and subcortical mechanisms. Cold Spring Harb Symp Quant Biol 55: 963-971. CrossRef Medline.
13. Devlin JT, Sillery EL, Hall DA, Hobden P, Behrens TE, Nunes RG, Clare S, Matthews PM, Moore DR, Johansen-Berg H (2006) Reliable identification of the auditory thalamus using multi-modal structural analyses. Neuroimage 30: 1112-1120. CrossRef Medline.
14. Dumoulin SO, Bittar RG, Kabani NJ, Baker CL Jr, Le Goualher G, Bruce Pike G, Evans AC (2000) A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb Cortex 10: 454-463. CrossRef Medline.
15. Duncan J (2006) EPS Mid-Career Award 2004: brain mechanisms of attention. Q J Exp Psychol (Hove) 59: 2-27. CrossRef Medline.
16. Fujita N, Tanaka H, Takanashi M, Hirabuki N, Abe K, Yoshimura H, Nakamura H (2001) Lateral geniculate nucleus: anatomic and functional identification by use of MR imaging. AJNR Am J Neuroradiol 22: 1719-1726. Medline.
17. Gandhi SP, Heeger DJ, Boynton GM (1999) Spatial attention affects brain activity in human primary visual cortex. Proc Natl Acad Sci U S A 96: 3314-3319. CrossRef Medline.
18. Goense J, Merkle H, Logothetis NK (2012) High-resolution fMRI reveals laminar differences in neurovascular coupling between positive and negative BOLD responses. Neuron 76: 629-639. CrossRef Medline.
19. Gouws A, Woods W, Millman R, Morland A, Green G (2009) DataViewer3D: an open-source, cross-platform multi-modal neuroimaging data visualization tool. Front Neuroinform 3: 9. CrossRef Medline.
20. Gutierrez C, Cola MG, Seltzer B, Cusick C (2000) Neurochemical and connectional organization of the dorsal pulvinar complex in monkeys. J Comp Neurol 419: 61-86. CrossRef Medline.
21. Hupé JM, Bordier C, DojatM (2012) A BOLD signature of eyeblinks in the visual cortex. Neuroimage 61: 149-161. CrossRef Medline.
22. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17: 825-841. CrossRef Medline.
23. Kastner S, Pinsk MA, De Weerd P, Desimone R, Ungerleider LG (1999) Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22: 751-761. CrossRef Medline.
24. Kastner S, O'Connor DH, Fukui MM, Fehd HM, Herwig U, Pinsk MA (2004) Functional imaging of the human lateral geniculate nucleus and pulvinar. J Neurophysiol 91: 438-448. Medline.
25. Katyal S, Ress D (2014) Endogenous attention signals evoked by threshold contrast detection in human superior colliculus. J Neurosci 34: 892-900. CrossRef Medline.
26. Katyal S, Zughni S, Greene C, Ress D (2010) Topography of covert visual attention in human superior colliculus. J Neurophysiol 104: 3074-3083. CrossRef Medline.
27. Krauzlis RJ, Lovejoy LP, Zénon A (2013) Superior colliculus and visual spatial attention. Annu Rev Neurosci 36: 165-182. CrossRef Medline.
28. Li X, Lu ZL, Tjan BS, Dosher BA, Chu W (2008) Blood oxygenation leveldependent contrast response functions identify mechanisms of covert attention in early visual areas. Proc Natl Acad Sci U S A 105: 6202-6207. CrossRef Medline.
29. Limbrick-Oldfield EH, Brooks JC, Wise RJ, Padormo F, Hajnal JV, Beckmann CF, Ungless MA (2012) Identification and characterisation of midbrain nuclei using optimised functional magnetic resonance imaging. Neuroimage 59: 1230-1238. CrossRef Medline.
30. Lovejoy LP, Krauzlis RJ (2010) Inactivation of primate superior colliculus impairs covert selection of signals for perceptual judgments. Nat Neurosci 13: 261-266. CrossRef Medline.
31. Luck SJ, Chelazzi L, Hillyard SA, Desimone R (1997) Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J Neurophysiol 77: 24-42. Medline.
32. Martínez A, Anllo-Vento L, Sereno MI, Frank LR, Buxton RB, Dubowitz DJ, Wong EC, Hinrichs H, Heinze HJ, Hillyard SA (1999) Involvement of striate and extrastriate visual cortical areas in spatial attention. Nat Neurosci 2: 364-369. CrossRef Medline.
33. McAlonan K, Cavanaugh J, Wurtz RH (2008) Guarding the gateway to cortex with attention in visual thalamus. Nature 456: 391-394. CrossRef Medline.
34. Mehta AD, Ulbert I, Schroeder CE (2000a) Intermodal selective attention in monkeys. II: physiological mechanisms of modulation. Cereb Cortex 10: 359-370. CrossRef Medline.
35. Mehta AD, Ulbert I, Schroeder CE (2000b) Intermodal selective attention in monkeys. I: distribution and timing of effects across visual areas. Cereb Cortex 10: 343-358. CrossRef Medline.
36. Motter BC (1993) Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J Neurophysiol 70: 909-919. Medline.
37. Mullinger KJ, Mayhew SD, Bagshaw AP, Bowtell R, Francis ST (2014) Evidence that the negative BOLD response is neuronal in origin: a simultaneous EEG-BOLD-CBF study in humans. Neuroimage 94: 263-274. CrossRef Medline.
38. Murray SO (2008) The effects of spatial attention in early human visual cortex are stimulus independent. J Vis 8(10): 2. 1-11. CrossRef Medline.
39. Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211: 1792-1804. CrossRef Medline.
40. O'Connor DH, Fukui MM, Pinsk MA, Kastner S (2002) Attention modulates responses in the human lateral geniculate nucleus. Nat Neurosci 5: 1203-1209. CrossRef Medline.
41. Posner MI (1980) Orienting of attention. QJ Exp Psychol 32: 3-25. CrossRef Medline.
42. Purushothaman G, Marion R, Li K, Casagrande VA (2012) Gating and control of primary visual cortex by pulvinar. Nat Neurosci 15: 905-912. CrossRef Medline.
43. Rafal RD, Posner MI (1987) Deficits in human visual spatial attention following thalamic lesions. Proc Natl Acad Sci U S A 84: 7349-7353. CrossRef Medline.
44. Ress D, Backus BT, Heeger DJ (2000) Activity in primary visual cortex predicts performance in a visual detection task. Nat Neurosci 3: 940-945. CrossRef Medline.
45. Reynolds JH, Heeger DJ (2009) The normalization model of attention. Neuron 61: 168-185. CrossRef Medline.
46. Robinson DL, Petersen SE (1992) The pulvinar and visual salience. Trends Neurosci 15: 127-132. CrossRef Medline.
47. Saalmann YB, Kastner S (2009) Gain control in the visual thalamus during perception and cognition. Curr Opin Neurobiol 19: 408-414. CrossRef Medline.
48. Schneider KA (2011) Subcortical mechanisms of feature-based attention. J Neurosci 31: 8643-8653. CrossRef Medline.
49. Schneider KA, Kastner S (2009) Effects of sustained spatial attention in the human lateral geniculate nucleus and superior colliculus. J Neurosci 29: 1784-1795. CrossRef Medline.
50. Shipp S (2003) The functional logic of cortico-pulvinar connections. Philos Trans R Soc Lond B Biol Sci 358: 1605-1624. CrossRef Medline.
51. Shmuel A, Yacoub E, Pfeuffer J, Van de Moortele PF, Adriany G, Hu X, Ugurbil K (2002) Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 36: 1195-1210. CrossRef Medline.
52. Slotnick SD, Schwarzbach J, Yantis S (2003) Attentional inhibition of visual processing in human striate and extrastriate cortex. Neuroimage 19: 1602-1611. CrossRef Medline.
53. Smith AT, Singh KD, Greenlee MW (2000) Attentional suppression of activity in the human visual cortex. Neuroreport 11: 271-277. CrossRef Medline.
54. Smith AT, Williams AL, Singh KD (2004) Negative BOLD in the visual cortex: evidence against blood stealing. Hum Brain Mapp 21: 213-220. CrossRef Medline.
55. Snow JC, Allen HA, Rafal RD, HumphreysGW (2009) Impaired attentional selection following lesions to human pulvinar: evidence for homology between human and monkey. Proc Natl Acad Sci U S A 106: 4054-4059. CrossRef Medline.
56. Somers DC, Dale AM, Seiffert AE, Tootell RB (1999) Functional MRI reveals spatially specific attentional modulation in human primary visual cortex. Proc Natl Acad Sci U S A 96: 1663-1668. CrossRef Medline.
57. Tootell RB, Mendola JD, Hadjikhani NK, Liu AK, Dale AM (1998a) The representation of the ipsilateral visual field in human cerebral cortex. Proc Natl Acad Sci U S A 95: 818-824. CrossRef Medline.
58. Tootell RB, Hadjikhani N, Hall EK, Marrett S, Vanduffel W, Vaughan JT, Dale AM (1998b) The retinotopy of visual spatial attention. Neuron 21: 1409-1422. CrossRef Medline.
59. Treue S, Martinez-Trujillo JC (2007) Attending to features inside and outside the spotlight of attention. Neuron 55: 174-176. CrossRef Medline.
60. Vanduffel W, Tootell RB, Orban GA (2000) Attention-dependent suppression of metabolic activity in the early stages of the macaque visual system. Cereb Cortex 10: 109-126. CrossRef Medline.
61. Wade AR, Rowland J (2010) Early suppressive mechanisms and the negative blood oxygenation level-dependent response in human visual cortex. J Neurosci 30: 5008-5019. CrossRef Medline.
62. Wall MB, Walker R, Smith AT (2009) Functional imaging of the human superior colliculus: an optimised approach. Neuroimage 47: 1620-1627. CrossRef Medline.
63. Zeki SM (1969) The secondary visual areas of the monkey. Brain Res 13: 197-226. CrossRef Medline.