Covert shifts of spatial attention in the macaque monkey

Journal of Neuroscience

Volumn 35, Issue 20, 2015, Pages 7695-7714

  Caspari, Natalie ^a   Janssens, Thomas ^a   Mantini, Dante ^a,b,c   Vandenberghe, Rik ^a,d   Vanduffel, Wim ^a,e,f  

^a KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

^b ETH ZURICH   (Switzerland)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^e HARVARD MEDICAL SCHOOL   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

FMRI; Human; Monkey; Shifting; Spatial attention; Superior parietal lobe

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; ATTENTION; BEHAVIOR; DIRECTIONAL SELECTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; INTRAPARIETAL SULCUS; MALE; NERVE CELL NETWORK; NONHUMAN; PERCEPTIVE THRESHOLD; PRIORITY JOURNAL; RESPONSE TIME; RHESUS MONKEY; SENSORY STIMULATION; SUPERIOR PARIETAL LOBULE; SUPERIOR TEMPORAL SULCUS; TASK PERFORMANCE; ANIMAL; CONNECTOME; DEPTH PERCEPTION; PARIETAL LOBE; PHYSIOLOGY; VISUAL CORTEX;

ANIMALS; ATTENTION; CONNECTOME; FEMALE; MACACA MULATTA; MALE; PARIETAL LOBE; SPACE PERCEPTION; VISUAL CORTEX;

EID: 84929691934     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4383-14.2015     Document Type: Article

References (79)

1. Arsenault JT, Nelissen K, Jarraya B, Vanduffel W (2013) Dopaminergic reward signals selectively decrease fMRI activity in primate visual cortex. Neuron 77:1174-1186.CrossRef Medline
2. Battaglia-Mayer A, Ferraina S, Genovesio A, Marconi B, Squatrito S, Molinari M, Lacquaniti F, Caminiti R (2001) Eye-hand coordination during reaching: II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections. Cereb Cortex 11:528-544.CrossRef Medline
3. Bisley JW, Goldberg ME (2003a) Neuronal activity in the lateral intraparietal area and spatial attention. Science 299:81-86.CrossRef Medline
4. Bisley JW, Goldberg ME (2003b) The role of the parietal cortex in the neural processing of saccadic eye movements. Adv Neurol 93:141-157. Medline
5. Buschman TJ, Miller EK (2009) Serial, covert shifts of attention during visual search are reflected by the frontal eye fields and correlated with population oscillations. Neuron 63:386-396.CrossRef Medline
6. Capotosto P, Tosoni A, Spadone S, Sestieri C, Perrucci MG, Romani GL, Della Penna S, Corbetta M (2013) Anatomical segregation of visual selection mechanisms in human parietal cortex. J Neurosci 33:6225-6229.CrossRef Medline
7. Chiu YC, Yantis S (2009) A domain-independent source of cognitive control for task sets: shifting spatial attention and switching categorization rules. J Neurosci 29:3930-3938.CrossRef Medline
8. Ciavarro M, Ambrosini E, Tosoni A, Committeri G, Fattori P, Galletti C (2013) rTMS of medial parieto-occipital cortex interferes with attentional reorienting during attention and reaching tasks. J Cogn Neurosci 25:1453-1462.CrossRef Medline
9. Cohen YE, Andersen RA (2002) A common reference frame for movement plans in the posterior parietal cortex. Nat Rev Neurosci 3:553-562.CrossRef Medline
10. Corbetta M, Kincade JM, Ollinger JM, McAvoy MP, Shulman GL (2000) Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci 3:292-297.CrossRef Medline
11. Cui X, Stetson C, Montague PR, Eagleman DM (2009) Ready.go: amplitude of the FMRI signal encodes expectation of cue arrival time 1. PLoS Biol 7:e1000167.CrossRef Medline
12. Denys K, Vanduffel W, Fize D, Nelissen K, Sawamura H, Georgieva S, Vogels R, Van Essen D, Orban GA (2004) Visual activation in prefrontal cortex is stronger in monkeys than in humans. J Cogn Neurosci 16:1505-1516.CrossRef Medline
13. Ekstrom LB, Roelfsema PR, Arsenault JT, Bonmassar G, Vanduffel W (2008) Bottom-up dependent gating of frontal signals in early visual cortex. Science 321:414-417.CrossRef Medline
14. Ekstrom LB, Roelfsema PR, Arsenault JT, Kolster H, Vanduffel W (2009) Modulation of the contrast response function by electrical microstimulation of the macaque frontal eye field. J Neurosci 29:10683-10694.CrossRef Medline
15. Engbert R, Kliegl R (2003) Microsaccades uncover the orientation of covert attention. Vision Res 43:1035-1045.CrossRef Medline
16. Esterman M, Chiu YC, Tamber-Rosenau BJ, Yantis S (2009) Decoding cognitive control in human parietal cortex. Proc Natl Acad Sci U S A 106: 17974-17979.CrossRef Medline
17. Fattori P, Breveglieri R, Amoroso K, Galletti C (2004) Evidence for both reaching and grasping activity in the medial parieto-occipital cortex of the macaque 47. Eur J Neurosci 20:2457-2466.CrossRef Medline
18. Fattori P, Kutz DF, Breveglieri R, Marzocchi N, Galletti C (2005) Spatial tuning of reaching activity in the medial parieto-occipital cortex (area V6A) of macaque monkey 42. Eur J Neurosci 22:956-972.CrossRef Medline
19. Friston KJ (2011) Functional and effective connectivity: a review. Brain Connect 1:13-36.CrossRef Medline
20. Friston KJ, Stephan KE, Lund TE, Morcom A, Kiebel S (2005) Mixed-effects and fMRI studies. Neuroimage 24:244-252.CrossRef Medline
21. Galletti C, Fattori P, Battaglini PP, Shipp S, Zeki S (1996) Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur J Neurosci 8:30-52.CrossRef Medline
22. Galletti C, Fattori P, Kutz DF, Gamberini M (1999) Brain location and visual topography of cortical area V6A in the macaque monkey 59. Eur J Neurosci 11:575-582.CrossRef Medline
23. Galletti C, Gamberini M, Kutz DF, Fattori P, Luppino G, Matelli M (2001) The cortical connections of area V6: an occipito-parietal network processing visual information 56. Eur J Neurosci 13:1572-1588.CrossRef Medline
24. Galletti C, Breveglieri R, Lappe M, Bosco A, Ciavarro M, Fattori P (2010) Covert shift of attention modulates the ongoing neural activity in a reaching area of the macaque dorsomedial visual stream. PLoS One 5:e15078.CrossRef Medline
25. Gamberini M, Passarelli L, Fattori P, Zucchelli M, Bakola S, Luppino G, Galletti C (2009) Cortical connections of the visuomotor parietooccipital area V6Ad of the macaque monkey. J Comp Neurol 513:622-642.CrossRef Medline
26. Gerbella M, Borra E, Tonelli S, Rozzi S, Luppino G (2013) Connectional heterogeneity of the ventral part of the macaque area 46. Cereb Cortex 23:967-987.CrossRef Medline
27. Gottlieb J, Goldberg ME (1999) Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task. Nat Neurosci 2:906-912.CrossRef Medline
28. Grefkes C, Fink GR (2005) The functional organization of the intraparietal sulcus in humans and monkeys. J Anat 207:3-17.CrossRef Medline
29. Janssens T, Keil B, Farivar R, McNab JA, Polimeni JR, Gerits A, Arsenault JT, Wald LL, Vanduffel W (2012) An implanted 8-channel array coil for high-resolution macaque MRI at 3T. Neuroimage 62:1529-1536.CrossRef Medline
30. Janssens T, Zhu Q, Popivanov ID, Vanduffel W (2014) Probabilistic and single-subject retinotopic maps reveal the topographic organization of face patches in the macaque cortex. J Neurosci 34:10156-10167.CrossRef Medline
31. Johnson PB, Ferraina S, Bianchi L, Caminiti R (1996) Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. Cereb Cortex 6:102-119.CrossRef Medline
32. Kagan I, Iyer A, Lindner A, Andersen RA (2010) Space representation for eye movements is more contralateral in monkeys than in humans. Proc Natl Acad Sci U S A 107:7933-7938.CrossRef Medline
33. Kaping D, Vinck M, Hutchison RM, Everling S, Womelsdorf T (2011) Specific contributions of ventromedial, anterior cingulate, and lateral prefrontal cortex for attentional selection and stimulus valuation. PLoS Biol 9:e1001224.CrossRef Medline
34. Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315-341.CrossRef Medline
35. Kelley TA, Serences JT, Giesbrecht B, Yantis S (2008) Cortical mechanisms for shifting and holding visuospatial attention. Cereb Cortex 18:114-125.CrossRef Medline
36. Kolster H, Mandeville JB, Arsenault JT, Ekstrom LB, Wald LL, Vanduffel W (2009) Visual field map clusters in macaque extrastriate visual cortex. J Neurosci 29:7031-7039.CrossRef Medline
37. Kutz DF, Fattori P, Gamberini M, Breveglieri R, Galletti C (2003) Early-and late-responding cells to saccadic eye movements in the cortical area V6A of macaque monkey 51. Exp Brain Res 149:83-95. Medline
38. Kuwabara M, Mansouri FA, Buckley MJ, Tanaka K (2014) Cognitive control functions of anterior cingulate cortex in macaque monkeys performing a Wisconsin Card Sorting Test analog. J Neurosci 34:7531-7547.CrossRef Medline
39. Latto R, Cowey A (1971) Visual field defects after frontal eye-field lesions in monkeys. Brain Res 30:1-24.CrossRef Medline
40. Laubrock J, Engbert R, Kliegl R (2005) Microsaccade dynamics during covert attention. Vision Res 45:721-730.CrossRef Medline
41. Leite FP, Tsao D, Vanduffel W, Fize D, Sasaki Y, Wald LL, Dale AM, Kwong KK, Orban GA, Rosen BR, Tootell RB, Mandeville JB (2002) Repeated fMRI using iron oxide contrast agent in awake, behaving macaques at 3 Tesla. Neuroimage 16:283-294.CrossRef Medline
42. Lewis JW, Van EssenDC (2000a) Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J Comp Neurol 428:112-137.CrossRef Medline
43. Lewis JW, Van Essen DC (2000b) Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. J Comp Neurol 428:79-111.CrossRef Medline
44. Li CS, Mazzoni P, Andersen RA (1999) Effect of reversible inactivation of macaque lateral intraparietal area on visual and memory saccades. J Neurophysiol 81:1827-1838. Medline
45. Liu T, Slotnick SD, Serences JT, Yantis S (2003) Cortical mechanisms of feature-based attentional control. Cereb Cortex 13:1334-1343.CrossRef Medline
46. Madore B, Glover GH, Pelc NJ (1999) Unaliasing by Fourier-encoding the overlaps using the temporal dimension (UNFOLD), applied to cardiac imaging and fMRI. Magn Reson Med 42:813-828.CrossRef Medline
47. Mandeville JB, Marota JJ (1999) Vascular filters of functional MRI: spatial localization using BOLD and CBV contrast. Magn Reson Med 42:591-598.CrossRef Medline
48. Margulies DS, Vincent JL, Kelly C, Lohmann G, Uddin LQ, Biswal BB, Villringer A, Castellanos FX, Milham MP, Petrides M (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci U S A 106:20069-20074.CrossRef Medline
49. McLaren DG, Kosmatka KJ, Oakes TR, Kroenke CD, Kohama SG, Matochik JA, Ingram DK, Johnson SC (2009) A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage 45:52-59.CrossRef Medline
50. Molenberghs P, Mesulam MM, Peeters R, Vandenberghe RR (2007) Remapping attentional priorities: differential contribution of superior parietal lobule and intraparietal sulcus. Cereb Cortex 17:2703-2712.CrossRef Medline
51. Molenberghs P, Gillebert CR, Peeters R, Vandenberghe R (2008) Convergence between lesion-symptom mapping and functional magnetic resonance imaging of spatially selective attention in the intact brain. J Neurosci 28:3359-3373.CrossRef Medline
52. Nakahara K, Hayashi T, Konishi S, Miyashita Y (2002) Functional MRI of macaque monkeys performing a cognitive set-shifting task. Science 295: 1532-1536.CrossRef Medline
53. Nelissen K, Luppino G, Vanduffel W, Rizzolatti G, Orban GA (2005) Observing others: multiple action representation in the frontal lobe. Science 310:332-336.CrossRef Medline
54. Nelissen K, Borra E, Gerbella M, Rozzi S, Luppino G, Vanduffel W, Rizzolatti G, Orban GA (2011) Action observation circuits in the macaque monkey cortex. J Neurosci 31:3743-3756.CrossRef Medline
55. Passarelli L, Rosa MG, Gamberini M, Bakola S, Burman KJ, Fattori P, Galletti C (2011) Cortical connections of area V6Av in the macaque: a visualinput node to the eye/hand coordination system 17. J Neurosci 31:1790-1801.CrossRef Medline
56. Patel GH, Shulman GL, Baker JT, Akbudak E, Snyder AZ, Snyder LH, Corbetta M (2010) Topographic organization of macaque area LIP. Proc Natl Acad Sci U S A 107:4728-4733.CrossRef Medline
57. Paxinos G, Huang XF, Petrides M, Toga A (2008) The Rhesus monkey brain: in stereotaxic coordinates. London: Elsevier.
58. Premereur E, Janssen P, Vanduffel W (2015) Effector specificity in macaque frontal and parietal cortex. J Neurosci 35:3446-3459.CrossRef Medline
59. Pruessmann KP, Weiger M, Scheidegger MB, Boesiger P (1999) SENSE: sensitivity encoding for fast MRI. Magn Reson Med 42:952-962.CrossRef Medline
60. Serences JT, Schwarzbach J, Courtney SM, Golay X, Yantis S (2004) Control of object-based attention in human cortex. Cereb Cortex 14:1346-1357.CrossRef Medline
61. Shomstein S, Yantis S (2004) Control of attention shifts between vision and audition in human cortex. J Neurosci 24:10702-10706.CrossRef Medline
62. Shulman GL, Astafiev SV, Franke D, Pope DL, Snyder AZ, McAvoy MP, Corbetta M (2009) Interaction of stimulus-driven reorienting and expectation in ventral and dorsal frontoparietal and basal ganglia-cortical networks. J Neurosci 29:4392-4407.CrossRef Medline
63. Simon O, Mangin JF, Cohen L, Le Bihan D, Dehaene S (2002) Topographical layout of hand, eye, calculation, and language-related areas in the human parietal lobe. Neuron 33:475-487.CrossRef Medline
64. Thompson KG, Bichot NP, Schall JD (1997) Dissociation of visual discrimination from saccade programming in macaque frontal eye field. J Neurophysiol 77:1046-1050. Medline
65. Tosoni A, Shulman GL, Pope AL, McAvoy MP, Corbetta M (2013) Distinct representations for shifts of spatial attention and changes of reward contingencies in the human brain. Cortex 49:1733-1749.CrossRef Medline
66. Van Essen DC (2004) Surface-based approaches to spatial localization and registration in primate cerebral cortex. Neuroimage 23 [Suppl 1]:S97-S107.
67. Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, Anderson CH (2001) An integrated software suite for surface-based analyses of cerebral cortex. J Am Medical Inform Assoc 8:443-459.CrossRef Medline
68. Vandenberghe R, Gillebert CR (2009) Parcellation of parietal cortex: convergence between lesion-symptom mapping and mapping of the intact functioning brain. Behav Brain Res 199:171-182.CrossRef Medline
69. Vandenberghe R, Gitelman DR, Parrish TB, Mesulam MM (2001) Functional specificity of superior parietal mediation of spatial shifting. Neuroimage 14:661-673.CrossRef Medline
70. Vandenberghe R, Molenberghs P, Gillebert CR (2012) Spatial attention deficits in humans: the critical role of superior compared to inferior parietal lesions. Neuropsychologia 50:1092-1103.CrossRef Medline
71. Vanduffel W, Fize D, Mandeville JB, Nelissen K, Van Hecke P, Rosen BR, Tootell RB, Orban GA (2001) Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron 32:565-577.CrossRef Medline
72. Vanduffel W, Zhu Q, Orban GA (2014) Monkey cortex through fMRI glasses. Neuron 83:533-550.CrossRef Medline
73. Wardak C, Olivier E, Duhamel JR (2002) Saccadic target selection deficits after lateral intraparietal area inactivation in monkeys. J Neurosci 22: 9877-9884. Medline
74. Wardak C, Olivier E, Duhamel JR (2004) A deficit in covert attention after parietal cortex inactivation in the monkey. Neuron 42:501-508.CrossRef Medline
75. Wardak C, Ibos G, Duhamel JR, Olivier E (2006) Contribution of the monkey frontal eye field to covert visual attention. J Neurosci 26:4228-4235.CrossRef Medline
76. Wardak C, Olivier E, Duhamel JR (2011) The relationship between spatial attention and saccades in the frontoparietal network of the monkey. Eur J Neurosci 33:1973-1981.CrossRef Medline
77. Xiao Q, Barborica A, Ferrera VP (2007) Modulation of visual responses in macaque frontal eye field during covert tracking of invisible targets. Cereb Cortex 17:918-928.CrossRef Medline
78. Yantis S, Schwarzbach J, Serences JT, Carlson RL, Steinmetz MA, Pekar JJ, Courtney SM (2002) Transient neural activity in human parietal cortex during spatial attention shifts. Nat Neurosci 5:995-1002.CrossRef Medline
79. Zhao F, Wang P, Hendrich K, Ugurbil K, Kim SG (2006) Cortical layerdependent BOLD and CBV responses measured by spin-echo and gradient-echo fMRI: insights into hemodynamic regulation. Neuroimage 30:1149-1160.CrossRef Medline