All Title Author
Keywords Abstract

PLOS ONE  2014 

A Unified Comparison of Stimulus-Driven, Endogenous Mandatory and ‘Free Choice’ Saccades

DOI: 10.1371/journal.pone.0088990

Full-Text   Cite this paper   Add to My Lib

Abstract:

It has been claimed that saccades arising from the three saccade triggering modes–stimulus-driven, endogenous mandatory and ‘free choice’–are driven by distinct mechanisms. We tested this claim by instructing observers to saccade from a white or black fixation disc to a same polarity (white or black) disc flashed for 100 or 200 ms presented either alone (Exo), or together with an opposite (Endo) or same (EndoFC) polarity disc (blocked and mixed sessions). Target(s) and distractor were presented at three inter-stimulus intervals (ISIs) relative to the fixation offset (ISI: ?200, 0, +200 ms) and were displayed at random locations within a 4°-to-6° eccentricity range. The statistical analysis showed a global saccade triggering mode effect on saccade reaction times (SRTs) with Endo and EndoFC SRTs longer by about 27 ms than Exo-triggered ones but no effect for the Endo-EndoFC comparison. SRTs depended on both ISI (the “gap-effect”), and target duration. Bimodal best fits of the SRT-distributions were found in 65% of cases with their count not different across the three triggering modes. Percentages of saccades in the ‘fast’ and ‘slow’ ranges of bimodal fits did not depend on the triggering modes either. Bimodality tests failed to assert a significant difference between these modes. An analysis of the timing of a putative inhibition by the distractor (Endo) or by the duplicated target (EndoFC) yielded no significant difference between Endo and EndoFC saccades but showed a significant shortening with ISI similar to the SRT shortening suggesting that the distractor-target mutual inhibition is itself inhibited by ‘fixation’ neurons. While other experimental paradigms may well sustain claims of distinct mechanisms subtending the three saccade triggering modes, as here defined reflexive and voluntary saccades appear to differ primarily in the effectiveness with which inhibitory processes slow down the initial fast rise of the saccade triggering signal.

References

[1]  Kopecz K (1995) Saccadic reaction times in gap/overlap paradigms: a model based on integration of intentional and visual information on neural, dynamic fields. Vision Res 35(20): 2911–2925. doi: 10.1016/0042-6989(95)00066-9
[2]  Forbes K, Klein RM (1996) The magnitude of the fixation offset effect with endogenously and exogenously controlled saccades. J Cogn Neurosci 8(4): 344–352. doi: 10.1162/jocn.1996.8.4.344
[3]  Klein RM, Shore DI (2000) Relationships among modes of visual orienting In: Monsell S, Driver J, editors. Attention and performance: XVIII Control of cognitive processes,. Cambridge MA: MIT Press. 195–208.
[4]  Mort DJ, Perry RJ, Mannan SK, Hodgson TL, Anderson E, et al. (2003) Differential cortical activation during voluntary and reflexive saccades in man. Neuroimage 18(2): 231–246. doi: 10.1016/s1053-8119(02)00028-9
[5]  Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5(3): 218–228. doi: 10.1038/nrn1345
[6]  Walker R, McSorley E (2006) The parallel programming of voluntary and reflexive saccades. Vision Res 46(13: 2082–93. doi: 10.1016/j.visres.2005.12.009
[7]  Kennard C, Mannan SK, Nachev P, Parton A, Mort DJ, et al. (2005) Cognitive processes in saccade generation. Ann N Y Acad Sci 1039(1): 176–83. doi: 10.1196/annals.1325.017
[8]  Walker R, Walker DG, Husain M, Kennard C (2000) Control of voluntary and reflexive saccades. Exp Brain Res 130(4): 540–544. doi: 10.1007/s002219900285
[9]  Matsumora T, Koida K, Komatsu H (2008) Relationship Between Color Discrimination and Neural Responses in the Inferior Temporal Cortex of the Monkey. J Neurophysiol 100: 3361–3374. doi: 10.1152/jn.90551.2008
[10]  Stanford TR, Shankar S, Massoglia DP, Costello GM, Salinas E (2010) Perceptual decision making in less than 30 milliseconds. Nat Neurosci 13(3): 379–385. doi: 10.1038/nn.2485
[11]  Walker R, Deubel H, Schneider WX, Findlay JM (1997) Effect of Remote Distractors on Saccade Programming: Evidence for an Extended Fixation Zone. J Neurophysiol 78(2): 1108–1119.
[12]  Walker R, Kentridge RW, Findlay JM (1995) Independent contributions of the orienting of attention, fixation offset and bilateral stimulation on human saccadic latencies. Exp Brain Res 103: 294–310. doi: 10.1007/bf00231716
[13]  Watanabe K, Funahashi S (2007) Prefrontal delay-period activity reflects the decision process of a saccade direction during a free-choice ODR task. Cereb Cortex 17: 88–100. doi: 10.1093/cercor/bhm102
[14]  Reingold EM, Stampe DM (2002) Saccadic inhibition in voluntary and reflexive saccades. J Cogn Neurosci 14(3): 371–388. doi: 10.1162/089892902317361903
[15]  Cotti J, Panouilleres M, Munoz DP, Vercher J-L, Pélisson D, et al. (2009) Adaptation of reactive and voluntary saccades: different patterns of adaptation revealed in the antisaccade task. J Physiol 587(1): 127–138. doi: 10.1113/jphysiol.2008.159459
[16]  Wurtz RH, Goldberg ME (1972) Activity of superior colliculus in behaving monkey 3 Cells discharging before eye movements. J Neurophysiol 35: 575–586.
[17]  Leach JCD, Carpenter RHS (2001) Saccadic choice with asynchronous targets: evidence for independent randomisation. Vision Res 41: 3437–3445. doi: 10.1016/s0042-6989(01)00059-1
[18]  Nachev P, Rees G, Parton A, Kennard C, Husain M (2005) Volition and Conflict in Human Medial Frontal Cortex. Curr Biol 15(1): 122–128. doi: 10.1016/j.cub.2005.01.006
[19]  Henik A, Rafal R, Rhodes D (1994) Endogenously generated and visually guided saccades after lesions of the human frontal eye fields. J Cogn Neurosci 6(4): 400–411. doi: 10.1162/jocn.1994.6.4.400
[20]  Pierrot-Deseilligny C, Rivaud S, Gaymard B, Agid Y (1991) Cortical control of reflexive visually-guided saccades. Brain 114 (3): 1473–85. doi: 10.1093/brain/114.3.1473
[21]  Pierrot-Deseilligny C, Rivaud S, Gaymard B, Agid Y (1991) Cortical control of memory-guided saccades in man. Exp Brain Res 83: 607–617. doi: 10.1007/bf00229839
[22]  Schiller PH, Chou I (2000) The effects of anterior arcuate and dorsomedial frontal cortex lesions on visually guided eye movements: 2. Paired and multiple targets. Vision Res 40(10–12): 1627–1638. doi: 10.1016/s0042-6989(00)00058-4
[23]  Brown MR, DeSouza JF, Goltz HC, Ford K, Menon RS, et al. (2004) Comparison of memory- and visually guided saccades using event-related fMRI. J Neurophysiol 91(2): 873–889. doi: 10.1152/jn.00382.2003
[24]  Nachev P, Kennard C, Husain M (2008) Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9(11): 856–69. doi: 10.1038/nrn2478
[25]  Schall JD (2001) Neural basis of deciding, choosing and acting. Nat Rev Neurosci 2(1): 33–42. doi: 10.1038/35049054
[26]  Gaymard B, Ploner CJ, Rivaud-Péchoux S, Pierrot-Deseilligny C (1999) The frontal eye field is involved in spatial short-term memory but not in reflexive saccade inhibition. Exp Brain Res 129: 288–301. doi: 10.1007/s002210050899
[27]  Rolfs M, Vitu F (2007) On the limited role of target onset in the gap task: Support for the motor-preparation hypothesis. J Vision 7: 1–20. doi: 10.1167/7.10.7
[28]  Saslow MG (1967) Effects of components of displacement-step stimuli upon latency of saccadic eye movements. J Opt Soc Am 57: 1024–1029. doi: 10.1364/josa.57.001024
[29]  Bompas A, Sumner P (2011) Saccadic Inhibition Reveals the Timing of Automatic and Voluntary Signals in the Human Brain. J Neurosci 31(35): 12501–12512. doi: 10.1523/jneurosci.2234-11.2011
[30]  Reingold EM, Stampe DM (2004) Saccadic inhibition in reading. J Exp Psychol Hum Percept Perform 30(1): 194–211. doi: 10.1037/0096-1523.30.1.194
[31]  Fischer B, Weber H, Biscaldi M, Aiple F, Otto P, Stuhr V (1993) Separate populations of visually guided saccades in humans: reaction times and amplitudes. Exp Brain Res 4: 528–541. doi: 10.1007/bf00229043
[32]  Kirchner H, Thorpe SJ (2006) Ultra-rapid object detection with saccadic eye movements: visual processing speed revisited. Vision Res 46(11): 1762–1776. doi: 10.1016/j.visres.2005.10.002
[33]  Fischer B, Rampsperger E (1984) Human express saccades: extremely short reaction times of goal directed eye movements. Exp Brain Res 57: 191–195. doi: 10.1007/bf00231145
[34]  Cardoso-Leite P, Gorea A, Mamassian P (2007) Temporal order judgment and simple reaction times: Evidence for a common processing system. J Vision 7: 1–14. doi: 10.1167/7.6.11
[35]  Otto TU, Mamassian P (2012) Noise and correlations in parallel perceptual decision making. Curr Biol 22(15): 1391–1396. doi: 10.1016/j.cub.2012.05.031
[36]  Boucher L, Palmeri TJ, Logan GD, Schall JD (2007) Inhibitory control in mind and brain: an interactive race model of countermanding saccades. Psychol Rev 114(2): 376–97. doi: 10.1037/0033-295x.114.2.376
[37]  Purcell BA, Heitz RP, Cohen JY, Schall JD, Logan GD, et al. (2010) Neurally constrained modeling of perceptual decision making. Psychol Rev 117(4): 1113–1143. doi: 10.1037/a0020311
[38]  Trappenberg TP, Dorris MC, Munoz DP, Klein RM (2001) A model of saccade initiation based on the competitive integration of exogenous and endogenous signals in the superior colliculus. J Cogn Neurosci 13(2): 256–271. doi: 10.1162/089892901564306
[39]  Marino RA, Trappenberg TP, Dorris MC, Munoz DP (2012) Spatial interactions in the superior colliculus predict saccade behavior in a neural field model. J Cogn Neurosci 24(2): 315–336. doi: 10.1162/jocn_a_00139
[40]  D L Sparks and R Hartwich-Young (1989) The deep layers of the superior colliculus. In Wurtz RH, Goldberg ME, editors. The neurobiology of saccadic eye-movements. Amsterdam: Elsevier. 213–255.
[41]  Gezeck S, Fischer B, Timmer J (1997) Saccadic reaction times: a statistical analysis of multimodal distributions. Vision Res 37(15): 2119–2131. doi: 10.1016/s0042-6989(97)00022-9
[42]  Gezeck S, Timmer J (1998) Detecting multimodality in saccadic reaction time distributions in gap and overlap tasks. Biol Cybern 78(4): 293–305. doi: 10.1007/s004220050434
[43]  Dorris MC, Munoz DP (1995) A neural correlate for the gap effect on saccadic reaction times in monkey. J Neurophysiol 73(6): 2558–2562.
[44]  Dorris MC, Paré M, Munoz DP (1997) Neuronal activity in monkey superior colliculus related to the initiation of saccadic eye movements. J Neurosci 17(21): 8566–8579.
[45]  Munoz DP, Istvan PJ (1998) Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. J Neurophysiol 79(3): 1193–209.
[46]  Brainard DH (1997) The Psychophysics Toolbox. Spatial Vis 10: 433–436. doi: 10.1163/156856897x00357
[47]  Pelli DG (1997) The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vis 10: 437–442. doi: 10.1163/156856897x00366
[48]  Cornelissen FW, Peters EM, Palmer J (2002) The Eyelink Toolbox: eye tracking with MATLAB and the Psychophysics Toolbox. Behav Res Methods, Instruments, Comput 34(4): 613–617. doi: 10.3758/bf03195489
[49]  Boch R, Fischer B, Rampsperger E (1984) Express-Saccades of the monkey: reaction times versus intensity, size, duration, eccentricity of their targets. Exp Brain Res 55: 223–231. doi: 10.1007/bf00237273
[50]  Fischer B (1987) The Preparation of Visually Guided Saccades. Rev Physiol Biochem Pharmacol 106: 1–35. doi: 10.1007/bfb0027574
[51]  Fischer B, Gezeck S, Huber W (1995) The three-loop model: a neural network for the generation of saccadic reaction times. Biol Cybern 72(3): 185–196. doi: 10.1007/bf00201483
[52]  Ratcliff R (1979) Group Reaction Time Distributions and an Analysis of Distribution Statistics Psychol Bull. 86(3): 446–461. doi: 10.1037//0033-2909.86.3.446
[53]  Vincent SB (1912) The functions of the vibrissae in the behavior of the white rat. Behav Monogr 1(5).
[54]  Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19(6): 716–723. doi: 10.1109/tac.1974.1100705
[55]  Hellwig B, Hengstler JG, Schmidt M, Gehrmann MC, Schormann W, et al. (2010) Comparison of scores for bimodality of gene expression distributions and genome-wide evaluation of the prognostic relevance of high scoring genes. Bioinformatics 11(276): 1–18. doi: 10.1186/1471-2105-11-276
[56]  Ellision AM (1987) Effect of seed dimorphism on the density-dependent dynamics of experimental populations of Atriplex triangularis (Chenopodiaceae). Am J Bot 74(8): 1280–1288. doi: 10.2307/2444163
[57]  Muratov AL, Gnedin OY (2010) Modeling the Metallicity Distribution of Globular Clusters. Astrophys J 718(2): 1266–1288. doi: 10.1088/0004-637x/718/2/1266
[58]  Sheskin DJ (2003) Handbook of Parametric and Nonparametric Statistical Procedures, 3rd ed. New York: CRC Press.
[59]  Paré M, Munoz DP (1996) Saccadic reaction time in the monkey: advanced preparation of oculomotor programs is primarily responsible for express saccade occurrence. J Neurophysiol 76(6): 3666–3681.
[60]  Donders FC (1868/1969) On the speed of mental processes. Acta Psychol 30: 412–431. doi: 10.1016/0001-6918(69)90065-1
[61]  Miller J, Low K (2001) Motor Processes in Simple, Go/No-Go, Choice Reaction Time Tasks: A Psychophysiological Analysis. J Exp Psychol Hum Percept Perform 27(2): 266–289. doi: 10.1037/0096-1523.27.2.266
[62]  Sternberg S (2001) Separate modifiability, mental modules, the use of pure and composite measures to reveal them. Acta Psychol 106(1–2): 147–246. doi: 10.1016/s0001-6918(00)00045-7
[63]  Nachev P, Husain M, Kennard C (2008) Volition and eye movements. In: Kennard C, Leigh RJ, editors. Progress in Brain Research Vol 171. New York: Elsevier. 391–398.
[64]  Pesaran B, Nelson MJ, Andersen RA (2008) Free choice activates a decision circuit between frontal and parietal cortex. Nature 453(7193): 406–409. doi: 10.1038/nature06849
[65]  Pesaran B (2010) Neural correlations, decisions, actions Curr Opin Neurobiol. 20(2): 166–171. doi: 10.1016/j.conb.2010.03.003

Full-Text

comments powered by Disqus