The Saccadic Re-Centering Bias is Associated with Activity Changes in the Human Superior Colliculus

Center for Cognitive Neuroscience, Duke University Durham, NC, USA.
Frontiers in Human Neuroscience (Impact Factor: 3.63). 11/2010; 4:193. DOI: 10.3389/fnhum.2010.00193
Source: PubMed


Being able to effectively explore our visual world is of fundamental importance, and it has been suggested that the straight-ahead gaze (primary position) might play a special role in this context. We employed fMRI in humans to investigate how neural activity might be modulated for saccades relative to this putative default position. Using an endogenous cueing paradigm, saccade direction and orbital starting position were systematically manipulated, resulting in saccades toward primary position (centripetal) and away from primary position (centrifugal) that were matched in amplitude, directional predictability, as well as orbital starting position. In accord with earlier research, we found that fMRI activity in the superior colliculus (SC), as well as in the frontal eye fields and the intraparietal sulcus, was enhanced contralateral to saccade direction across all saccade conditions. Furthermore, the SC exhibited a relative activity decrease during re-centering relative to centrifugal saccades, a pattern that was paralleled by faster saccadic reaction times. In contrast, activity within the cortical eye fields was not significantly modulated during re-centering saccades as compared to other saccade types, suggesting that the re-centering bias is predominantly implemented at a subcortical rather than cortical processing stage. Such a modulation might reflect a special coding bias facilitating the return of gaze to a default position in the gaze space in which retinotopic and egocentric reference frames are aligned and from which the visual world can be effectively explored.

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Available from: Mircea Ariel Schoenfeld
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    • "† 7 Reflexive saccades > fixation Simó et al., 2005 [6]* 10 Reflexive saccades > fixation Nelles et al., 2007 [38] 10 Reflexive saccades > fixation de Haan et al., 2008 [39] 10 Reflexive saccades > fixation Ettinger et al., 2008 [40] 36 Reflexive saccades > fixation Haller et al., 2008 [41] 14 Reflexive saccades > fixation Ettinger et al., 2009 [42] 24 Reflexive saccades > fixation Nelles et al., 2009 [43] 11 Reflexive saccades > fixation Petit et al., 2009 [44] 27 Reflexive saccades > fixation Schraa-Tam et al., 2009 [21] 18 Reflexive saccades > fixation van Broekhoven et al., 2009 [45] 17 Reflexive saccades > fixation Krebs et al., 2010 [46]* 16 Reflexive saccades > fixation Grosbras et al., 2001 [47]* 9 Memory-guided saccades > fixation Matsuda et al., 2004 [5] 21 Antisaccades > fixation Sugiura et al., 2004 [48] 19 Memory-guided saccades > fixation Camchong et al., 2006 [49] 14 Memory-guided saccades > fixation Tu et al., 2006 [50]* 10 Antisaccades > fixation Ettinger et al., 2008 [51] 17 Antisaccades > fixation Fukumoto-Motoshita et al., 2009 [52] 18 Antisaccades > fixation Camchong et al., 2008 [3] 15 Antisaccades + memory-guided saccades > fixation DeSouza et al., 2003 [53] ‡ 10 Antisaccades + reflexive saccades > fixation performed and for each voxel, the beta coefficient was obtained for the stimulus timing as convolved with the hemodynamic response. The anatomical and functional images were warped to Talairach space. "
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    ABSTRACT: Saccades are rapid eye movements that move the eyes to a location of interest. Regions within posterior parietal cortex (PPC) have consistently shown activation in brain imaging studies of saccades, ostensibly reflecting shifts of visual attention and the transformation of sensory input into motor commands. Saccades range from the most basic reflexive glances toward a target to more complex saccades, which require some form of cognitive control (such as working memory or inhibition of reflexive responses). This study sought to summarize and parse the relative contribution of various brain regions (and parietal regions in particular) to reflexive and complex saccades. We conducted an activation likelihood estimation (ALE) meta-analysis of functional MRI studies of saccades in healthy adult humans. Twenty-two studies were identified that met our criteria. These studies provided 338 participants and 375 foci for the meta-analysis, which was conducted using the GingerALE application from BrainMap. Separate analyses were conducted for all saccades, reflexive saccades only, and complex saccades only. In addition, a subtraction analysis was done to determine significant differences in activation probability between reflexive and complex saccades. No part of this digital document may be reproduced, stored in a retrieval system or transmitted commercially in any form or by any means. The publisher has taken reasonable care in the preparation of this digital document, but makes no expressed or implied warranty of any kind and assumes no responsibility for any errors or omissions. No liability is assumed for incidental or consequential damages in connection with or arising out of information contained herein. This digital document is sold with the clear understanding that the publisher is not engaged in rendering legal, medical or any other professional services.
    Full-text · Chapter · Jul 2012
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    • "Specifically , we employed a centrally cued saccade paradigm with five positions along the horizontal meridian that enabled the comparison of centripetal recentering saccades to isoamplitude centrifugal saccades starting from the same fixation position and having identical directional probability (cf. Krebs et al. 2010a). In line with the commonly observed contralateral layout of attentional orienting and the anticipatory visual-field shifts observed in LIP neurons, our analysis aimed at identifying neural activity occurring contralateral to the direction of the upcoming saccade over posterior sites, thereby providing evidence for location-specific attentional shifts. "
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    ABSTRACT: Being able to effectively explore the visual world is of fundamental importance, and it has been suggested that the straight-ahead gaze position within the egocentric reference frame ("primary position") might play a special role in this context. In the present study we employed human electroencephalography (EEG) to examine neural activity related to the spatial guidance of saccadic eye movements. Moreover, we sought to investigate whether such activity would be modulated by the spatial relation of saccade direction to the primary gaze position (recentering saccades). Participants executed endogenously cued saccades between five equidistant locations along the horizontal meridian. This design allowed for the comparison of isoamplitude saccades from the same starting position that were oriented either toward the primary position (centripetal) or further away from it (centrifugal). By back-averaging time-locked to the saccade onset on each trial, we identified a parietally distributed, negative-polarity EEG deflection contralateral to the direction of the upcoming saccade. Importantly, this contralateral presaccadic negativity, which appeared to reflect the location-specific attentional guidance of the eye movement, was attenuated for recentering saccades relative to isoamplitude centrifugal saccades. This differential electrophysiological signature was paralleled by faster saccadic reaction times and was substantially more apparent when time-locking the data to the onset of the saccade rather than to the onset of the cue, suggesting a tight temporal association with saccade initiation. The diminished level of this presaccadic component for recentering saccades may reflect the preferential coding of the straight-ahead gaze position, in which both the eye-centered and head-centered reference frames are perfectly aligned and from which the visual world can be effectively explored.
    Full-text · Article · Dec 2011 · Journal of Neurophysiology
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    • "Despite these difficulties, it has been possible to retinotopically map the human SC (DuBois and Cohen 2000; Katyal et al. 2010; Schneider and Kastner 2005), record visual responses to static and moving stimuli (Schneider and Kastner 2005; Sylvester et al. 2007), and demonstrate attentional modulations (Gitelman et al. 2002; Himmelbach et al. 2007; Katyal et al. 2010; Schneider and Kastner 2009), all with functional magnetic resonance imaging (fMRI). However, despite the critical role the SC plays in oculomotor control, very few studies have attempted to record oculomotor signals from the human SC (Anderson et al. 2008; Krebs et al. 2010a, 2010b; Petit and Beauchamp 2003). This may in part be due to the further technical challenges faced when attempting to record eye movement responses within a high magnetic field. "
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    ABSTRACT: A natural visual scene contains more information than the visual system has the capacity to simultaneously process, requiring specific items to be selected for detailed analysis at the expense of others. Such selection and inhibition are fundamental in guiding search behavior, but the neural basis of these mechanisms remains unclear. Abruptly appearing visual items can automatically capture attention, but once attention has been directed away from the salient event, return to that same location is slowed. In non-human primates, signals associated with attentional capture (AC) and subsequent inhibition of return (IOR) have been recorded from the superior colliculus (SC)--a structure known to play a pivotal role in reflexive spatial orienting. Here, we sought to establish whether similar signals could be recorded from the human SC, as well as early retinotopic cortical visual areas, where signals associated with AC and IOR have yet to be investigated with respect to oculomotor responses. Using an optimized oculomotor paradigm together with high-field, high-spatial resolution functional magnetic resonance imaging and high-speed eye tracking, we demonstrate that BOLD signal changes recorded from the human SC correlate strongly with our saccadic measures of AC and IOR. A qualitatively similar pattern of responses was found for V1, but only the inhibitory response associated with IOR persisted through V2 and V3. Although the SC plays a role in mediating these automatic attentional biasing signals, the source of these signals is likely to lie in higher cortical areas.
    Full-text · Article · Jul 2011 · Journal of Neurophysiology
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