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Neural Basis of Saccadic Decision Making in the Human Cortex

  • Samson Freyermuth
  • Jean-Philippe Lachaux
  • Philippe Kahane
  • Alain Berthoz

Abstract

We summarize a few of the brain imaging studies on cortical control of ocular saccades (including the main eye fields: PEF, FEF, SEF, CEF, pre-SEF, PFEF) and describes recent new findings obtained with intracranial recordings of brain activity in epileptic patients (Stereotaxic EEG). We shall particularly focus on the problem of decision making in saccadic control by describing experiments during which subjects had to decide to make an horizontal saccade to a particular direction in space. Oculomotor execution and decision can be studied only by integrating dynamic component. The SEEG signals clearly reveal the multidimensionality of the ensemble neuronal responses, which consist of event-related potentials (ERPs), induced synchronizations and desynchronizations in distinct frequency bands. Our short study show a specific activation in the high frequencies (very high gamma band: 110–140 Hz) of the PFEF in an oculomotor task when the decision is needed.

Keywords

Prefrontal Cortex Transcranial Magnetic Stimulation Antisaccade Task Saccade Generation Saccade Goal 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Amador N, Schlag-Rey M, Schlag J (2004) Primate antisaccade: II. Supplementary eye field neuronal activity predicts correct performance. J Neurophysiol 91:1672–1689PubMedCrossRefGoogle Scholar
  2. Andersson F, Joliot M, Perchey G, Petit L (2006) Eye position-dependent activity in the primary visual area as revealed by fMRI. Hum Brain Mapping (early view)Google Scholar
  3. Aspell JE, Tanskanen T, Hurlbert AC (2005) Neuromagnetic correlates of visual motion coherence. Eur J Neurosci 22:2937–2945PubMedCrossRefGoogle Scholar
  4. Astafiev SV, Shulman GL, Stanley CM, Snyder AZ, Van Essen DC, Corbetta M (2003) Functional organization of human intraparietal and frontal cortex for attending, looking, and pointing. J Neurosci 23(2):591–596Google Scholar
  5. Beauchamp MS, Petit L, Ellmore TM, Ingeholm J, Haxby JV (2001) A parametric fMRI study of overt and covert shifts of visuospatial attention. NeuroImage 14:310–321PubMedCrossRefGoogle Scholar
  6. Berman RA, Colby CL, Genovese CR (1999) Cortical networks subserving pursuit and saccadic eye movements in humans: an fMRI study. Hum Brain Mapping 8:209–225CrossRefGoogle Scholar
  7. Berthoz A (2003) La décision. Jacob, ParisGoogle Scholar
  8. Blanke O, Seeck M (2003) Direction of saccadic and smooth eye movements induced by electrical stimulation of the human frontal eye field: effect of orbital position. Exp Brain Res 150:174–183PubMedGoogle Scholar
  9. Bodis-Wollner I, Von Gizyckia H, Amassiana V, Avitablea M, Maria Z, Hallettb M, Bucherc SF, Hussaina Z, Lallia S, Cracco R (2002) The dynamic effect of saccades in the visual cortex: evidence from fMRI, sTMS and EEG studies. Int Congr Ser 1232:843–851CrossRefGoogle Scholar
  10. Brown MR, Goltz HC, Vilis T, Ford KA, Everling S (2006) Inhibition and generation of saccades: rapid event-related fMRI of prosaccades, antisaccades, and nogo trials. NeuroImage 33:644–659PubMedCrossRefGoogle Scholar
  11. Connolly JD, Goodale MA, Menon RS, Munoz DP (2002) Human fMRI evidence for the neural correlates of preparatory set. Nat Neurosci 5:1345–1352PubMedCrossRefGoogle Scholar
  12. Constantinidis C, Williams GV, Goldman-Rakic PS (2002) A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat Neurosci 5:175–180PubMedCrossRefGoogle Scholar
  13. Corbetta M (1998a) Frontoparietal cortical networks for directing attention and the eye to visual locations: identical, independent, or overlapping systems. Proc Natl Acad Sci U S A 95:831–838PubMedCrossRefGoogle Scholar
  14. Corbetta M, Akbudak E, Conturo TE, Snyder AZ, Ollinger JM, Drury HA, Linenweber MR, Petersen SE, Raichle ME, Van Essen DC, Shulman GL (1998b) A common network of functional areas for attention and eye movements. Neuron 21:761–773PubMedCrossRefGoogle Scholar
  15. Corbetta M, Kincade JM, Shulman GL (2002) Neural systems for visual orienting and their relationships to spatial working memory. J Cognit Neurosci 14:508–523CrossRefGoogle Scholar
  16. Cornelissen FW, Kimmig H, Schira M, Rutschmann RM, Maguire RP, Broerse A, Den Boer JA, Greenlee MW (2002) Event-related fMRI responses in the human frontal eye fields in a randomized pro-and antisaccade task. Exp Brain Res 145:270–274PubMedCrossRefGoogle Scholar
  17. Coull JT, Frith CD, Büchel C, Nobre AC (2000) Orienting attention in time: behavioural and neuroanatomical distinction between exogenous and endogenous shifts. Neuropsychologia 38:808–819PubMedCrossRefGoogle Scholar
  18. Crone NE, Miglioretti DL, Gordon B, Lesser RP (1998) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis: II. Event-related synchronization in the gamma band. Brain 121:2301–2315PubMedCrossRefGoogle Scholar
  19. Curtis CE, D’Esposito M (2006) Selection and maintenance of saccade goals in the human frontal eye fields. J Neurophysiol 95:3923–3927PubMedCrossRefGoogle Scholar
  20. DeSouza JF, Menon RS, Everling S (2003) Preparatory set associated with pro-saccades and anti-saccades in humans investigated with event-related FMRI. J Neurophysiol 89:1016–1023PubMedCrossRefGoogle Scholar
  21. Duncan J (2001) An adaptive coding model of neural function in prefrontal cortex. Nat Rev Neurosci 2:820–829PubMedCrossRefGoogle Scholar
  22. Funahashi S (2006) Prefrontal cortex and working memory processes. Neuroscience 139:251–261PubMedCrossRefGoogle Scholar
  23. Gaymard B, Rivaud S, Cassarini JF, Dubard T, Rancurel G, Agid Y, Pierrot-Deseilligny C (1998) Effects of anterior cingulate cortex lesions on ocular saccades in humans. Exp Brain Res 120:173–183PubMedCrossRefGoogle Scholar
  24. Gaymard B, Lynch J, Ploner C, Condy C, Rivaud-Pechoux S (2003) The parieto-collicular pathway: anatomical location and contribution to saccade generation. Eur J Neurosci 17:1518–1526PubMedCrossRefGoogle Scholar
  25. Grosbras MH, Lobel E, LeBihan D, Berthoz A, Leonards U (1998) Evidence for a pre-SEF in humans. NeuroImage 7:988Google Scholar
  26. Grosbras MH, Lobel E, Van de Moortele PF, Le Bihan D, Berthoz A (1999) An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. Cereb Cortex 9:705–711PubMedCrossRefGoogle Scholar
  27. Grosbras MH, Leonards U, Lobel E, Poline JB, LeBihan D, Berthoz A (2001) Human cortical networks for new and familiar sequences of saccades. Cereb Cortex 11:936–945PubMedCrossRefGoogle Scholar
  28. Grosbras MH, Paus T (2002) Transcranial magnetic stimulation of the human frontal eye field: effects on visual perception and attention. J Cognit Neurosci 14:1109–1120CrossRefGoogle Scholar
  29. Grosbras MH, Laird A, Paus T (2005) Cortical regions involved in eye movements, shifts of attention, and gaze perception. Hum Brain Mapping 25:140–154CrossRefGoogle Scholar
  30. Guitton D, Buchtel HA, Douglas RM (1985) Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Exp Brain Res 58:455–472PubMedCrossRefGoogle Scholar
  31. Heide W, Kompf D (1998) Combined deficits of saccades and visuo-spatial orientation after cortical lesions. Exp Brain Res 123:164–171PubMedCrossRefGoogle Scholar
  32. Heide W, Binkofski F, Seitz RJ, Posse S, Nitschke MF, Freund HJ, Kompf D (2001) Activation of frontoparietal cortices during memorized triple-step sequences of saccadic eye movements: an fMRI study. Eur J Neurosci 13:1177–1189PubMedCrossRefGoogle Scholar
  33. Herter TM, Guitton D (2004) Accurate bidirectional saccade control by a single hemicortex. Brain 127:1393–1402PubMedCrossRefGoogle Scholar
  34. Husain M, Mannan S, Hodgson T, Wojciulik E, Driver J, Kennard C (2001) Impaired spatial working memory across saccades contributes to abnormal search in parietal neglect. Brain 124:941–952PubMedCrossRefGoogle Scholar
  35. Isoda M, Tanji J (2003) Contrasting neuronal activity in the supplementary and frontal eye fields during temporal organization of multiple saccades. J Neurophysiol 90:3054–3065PubMedCrossRefGoogle Scholar
  36. Kahane P, Minotti L, Hoffmann D, Lachaux J, Ryvlin P (2004) Invasive EEG in the definition of the seizure onset zone: depth electrodes. In: Handbook of clinical neurophysiology. Pre-surgical assessment of the epilepsies with clinical neurophysiology and functional neuroimaging. In: Rosenow F, Lüders HO (Eds) Elsevier ScienceGoogle Scholar
  37. Koechlin E, Ody C, Kouneiher F (2003) The architecture of cognitive control in the human prefrontal cortex. Science 302:1181–1185PubMedCrossRefGoogle Scholar
  38. Knutson KM, Wood JN, Grafman J (2004) Brain activation in processing temporal sequence: an fMRI study. NeuroImage 23:1299–1307PubMedCrossRefGoogle Scholar
  39. Lachaux JP, Hoffmann D, Minotti L, Berthoz A, Kahane P (2006) Intracerebral dynamics of saccade generation in the human frontal eye field and supplementary eye field. NeuroImage 30:1302–1312PubMedCrossRefGoogle Scholar
  40. Lang W, Petit L, Hollinger P, Pietrzyk U, Tzourio N, Mazoyer B, Berthoz A (1994) A positron emission tomography study of oculomotor imagery. NeuroReport 5:921–924PubMedCrossRefGoogle Scholar
  41. Law I, Svarer C, Rostrup E, Paulson OB (1998) Parieto-occipital cortex activation during self-generated eye movements in the dark. Brain 121:2189–2200PubMedCrossRefGoogle Scholar
  42. Lepsien J, Pollmann S (2002) Covert reorienting and inhibition of return: an event-related fMRI study. J Cognit Neurosci 14:127–144CrossRefGoogle Scholar
  43. Lobel E, Berthoz A, Leroy-Willig A, Le Bihan D (1996) fMRI study of voluntary saccadic eye movements in humans. NeuroImage 3:396CrossRefGoogle Scholar
  44. Lobel E, Kahane P, Leonards U (2001) Localization of the human frontal eye fields: anatomical and functional findings from functional magnetic resonance imaging and intracerebral electrical stimulation. J Neurosurg 95:804–815PubMedGoogle Scholar
  45. Luppino G, Matelli M, Camarda R, Rizzolatti G (1993) Corticocortical connections of area F3 (SMA-proper) and area F6 (pre-SMA) in the macaque monkey. J Comp Neurol 338:114–140PubMedCrossRefGoogle Scholar
  46. Milea D, Lehericy S, Rivaud-Pechoux S, Duffau H, Lobel E, Capelle L, Marsault C, Berthoz A, Pierrot-Deseilligny C (2003) Antisaccade deficit after anterior cingulate cortex resection. NeuroReport 14:283–287PubMedCrossRefGoogle Scholar
  47. Milea D, Lobel E, Lehericy S, Pierrot-Deseilligny C, Berthoz A (2005) Cortical mechanisms of saccade generation from execution to decision. Annuals of the New York Academy of Sciences 1039:232–238CrossRefGoogle Scholar
  48. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 24:167–202PubMedCrossRefGoogle Scholar
  49. Miller BT, D’Esposito M (2005) Searching for “the top” in top-down control. Neuron 48:535–538PubMedCrossRefGoogle Scholar
  50. Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5:218–228PubMedCrossRefGoogle Scholar
  51. Nobre AC, Gitelman DR, Dias EC, Mesulam MM (2000) Covert visual spatial orienting and saccades: overlapping neural systems. NeuroImage 11:210–216PubMedCrossRefGoogle Scholar
  52. O’Driscoll GA, Wolff AL, Benkelfat C, Florencio PS, Lal S, Evans AC (2000) Functional neuroanatomy of smooth pursuit and predictive saccades. NeuroReport 11:1335–1340PubMedCrossRefGoogle Scholar
  53. Olk B, Chang E, Kingstone A, Ro T (2006) Modulation of antisaccades by transcranial magnetic stimulation of the human frontal eye field. Cereb Cortex 16:76–82PubMedCrossRefGoogle Scholar
  54. Ozyurt J, Rutschmannb RM, Greenleeb MW (2006) Cortical activation during memory-guided saccades. NeuroReport 17:1005–1009PubMedCrossRefGoogle Scholar
  55. Parton A, Parashkev N, Hodgson TL, Mort D, Thomas D, Ordidge R, Morgan PS, Jackson S, Rees G, Husain M (2006) Role of the human supplementary eye field in the control of saccadic eye movements. Neuropsychologia 45:997–1008PubMedCrossRefGoogle Scholar
  56. Paus T (1996) Location and function of the human frontal eye field: a selective review. Neuropsychologia 34:475–483PubMedCrossRefGoogle Scholar
  57. Perry RJ, Zeki S (2000) The neurology of saccades and cover shifts in spatial attention: an event-related fMRI study. Brain 123:2273–2288PubMedCrossRefGoogle Scholar
  58. Petit L, Tzourio N, Orssaud C, Pietrzyk U, Berthoz A, Mazoyer B (1995) Functional neuroanatomy of the human visual fixation system. Eur J Neurosci 7:169–174PubMedCrossRefGoogle Scholar
  59. Petit L, Orssaud C, Tzourio N, Crivello F, Berthoz A, Mazoyer B (1996) Functional anatomy of a prelearned sequence of horizontal saccades in humans. J Neurosci 16:3714–3726PubMedGoogle Scholar
  60. Petit L, Clark VP, Ingeholm J, Haxby JV (1997) Dissociation of saccade-related and pursuit-related activation in the human frontal eye fields as revealed by fMRI. J Neurophysiol 77:3386–3390PubMedGoogle Scholar
  61. Pierrot-Deseilligny C, Ploner CJ, Muri RM, Gaymard B, Rivaud-Pechoux S (2002) Effects of cortical lesions on saccadic eye movements in humans. Ann N Y Acad Sci 956:216–229PubMedCrossRefGoogle Scholar
  62. Pierrot-Deseilligny C, Muri RM, Ploner CJ, Gaymard B, Demeret S, Rivaud-Pechoux S (2003) Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain 126:1460–1473PubMedCrossRefGoogle Scholar
  63. Pierrot-Deseilligny C, Milea D, Muri RM (2004) Eye movement control by the cerebral cortex. Curr Opin Neurobiol 17:17–25CrossRefGoogle Scholar
  64. Pierrot-Deseilligny C, Muri RM, Nyffeler T, Milea D (2005) The role of the human dorsolateral prefrontal cortex in ocular motor behaviour. Ann N Y Acad Sci 1039:239–251PubMedCrossRefGoogle Scholar
  65. Ploner CJ, Gaymard BM, Rivaud-Pechoux S, Baulac M, Clemenceau S, Samson SF, Pierrot-Deseilligny C (2001) Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. Cereb Cortex 10:1211–1216CrossRefGoogle Scholar
  66. Postle BR, Berger JS, Taich AM, D’Esposito M (2000) Activity in human frontal cortex associated with spatial working memory and saccadic behavior. J Cognit Neurosci 12:2–14CrossRefGoogle Scholar
  67. Rizzolatti G, Riggio L, Dascola I, Umilta C (1987) Reorienting attention across the horizontal and vertical meridians: evidence in favor of a premotor theory of attention. Neuropsychologia 25:31–40PubMedCrossRefGoogle Scholar
  68. Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31:889–901PubMedCrossRefGoogle Scholar
  69. Rosano C, Krisky CM, Welling JS, Eddy WF, Luna B, Thulborn KR, Sweeney JA (2002) Pursuit and saccadic eye movement subregions in human frontal eye field: a high-resolution fMRI investigation. Cereb Cortex 12:107–115PubMedCrossRefGoogle Scholar
  70. Sakamoto A, Luders H, Burgess R (1991) Intracranial recordings of movement-related potentials to voluntary saccades. J Clin Neurophysiol 8:223–233PubMedCrossRefGoogle Scholar
  71. Schall JD (2001) Neural basis of deciding, choosing and acting. Nat Rev Neurosci 2:33–42PubMedCrossRefGoogle Scholar
  72. Schall JD (2004) On the role of frontal eye field in guiding attention and saccades. Vision Res 44:1453–1467PubMedCrossRefGoogle Scholar
  73. Simon JD, Mangin JF, Cohen L, Le Bihan D, Dehaene S (2002) On the role of frontal eye field in guiding attention and saccades. Neuron 33:475–487PubMedCrossRefGoogle Scholar
  74. Simon JD, Kherif F, Flandin G, Poline JB, Rivière D, Mangin JF, Le Bihan D, Dehaene S (2004) Automatized clustering and functional geometry of human parietofrontal networks for language, space, and number. NeuroImage 23:1192–1202PubMedCrossRefGoogle Scholar
  75. Talairach J, Toumoux P (1988) Co-planar stereotaxic atlas of the human brain. 3-Dimensional proportional system: an approach to cerebral imaging. Thieme Medical Publishers. New YorkGoogle Scholar
  76. Tobler PN, Muri RM (2002) Role of human frontal and supplementary eye fields in double step saccades. NeuroReport 13:253–255PubMedCrossRefGoogle Scholar
  77. Yamamoto J, Ikeda A, Satow T, Matsuhashi M, Baba K, Yamane F, Miyamoto S, Mihara T, Hori T, Taki W, Hashimoto N, Shibasaki H (2004) Human eye fields in the frontal lobe as studied by epicortical recording of movement-related cortical potentials. Brain 127:873–887PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Samson Freyermuth
    • 1
  • Jean-Philippe Lachaux
    • 2
  • Philippe Kahane
    • 3
  • Alain Berthoz
    • 1
  1. 1.Laboratoire de Physiologie de la Perception et de l’Action, CNRSCollège de FranceParisFrance
  2. 2.Inserm U280. Mental processes and brain activationCentre Hospitalier Le VinatierBronFrance
  3. 3.Department of Neurology and JE2413 Research UnitGrenoble HospitalGrenobleFrance

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