Elsevier

NeuroImage

Volume 32, Issue 4, 1 October 2006, Pages 1747-1759
NeuroImage

Exploring the visual world: The neural substrate of spatial orienting

https://doi.org/10.1016/j.neuroimage.2006.04.221Get rights and content

Abstract

Inspecting the visual environment, humans typically direct their attention across space by means of voluntary saccadic eye movements. Neuroimaging studies in healthy subjects have identified the superior parietal cortex and intraparietal sulcus as important structures involved in visual search. However, in apparent contrast, spatial disturbance of free exploration typically is observed after damage of brain structures located far more ventrally. Lesion studies in such patients disclosed the inferior parietal lobule (IPL) and temporo-parietal junction (TPJ), the superior temporal gyrus (STG) and insula, as well as the inferior frontal gyrus (IFG) of the right hemisphere. Here we used functional magnetic resonance imaging to investigate the involvement of these areas in active visual exploration in the intact brain. We conducted a region of interest analysis comparing free visual exploration of a dense stimulus array with the execution of stepwise horizontal and vertical saccades. The comparison of BOLD responses revealed significant signal increases during exploration in TPJ, STG, and IFG. This result calls for a reappraisal of the previous thinking on the function of these areas in visual search processes. In agreement with lesion studies, the data suggest that these areas are part of the network involved in human spatial orienting and exploration. The IPL dorsally of TPJ seem to be of minor importance for free visual exploration as these areas appear to be equally involved in the execution of spatially predetermined saccades.

Introduction

Efficient visual exploration is an indispensable skill for conscious perception of the environment. Scanning complex scenes and stimulus arrays for specific target stimuli (e.g. single objects which are relevant for ongoing activities) require prospective planning and execution of eye movements based on a stable representation of space. The outstanding importance of intact search behavior becomes evident in humans suffering from disorders of visual exploration after brain damage (Mort and Kennard, 2003). Among them, patients with spatial neglect after lesions of the right hemisphere demonstrate a remarkably strong and consistent bias of spontaneous activity towards the right, ipsilesional side of space. Recordings of visual and tactile exploration revealed the patients' center of active search to be shifted markedly towards the ipsilesional hemispace (Karnath, 2001). Interestingly, the manipulation of visual, vestibular, and proprioceptive information about the apparent orientation of the patient's body in space reduces this bias (Karnath et al., 1993, Pizzamiglio et al., 1990, Rubens, 1985). These findings suggested that the integration of multimodal sensory input into long-lasting egocentric representations of space relies crucially on those structures that are found damaged in stroke patients showing a horizontal bias of eye and head orientation (Karnath, 1997, Karnath and Dieterich, 2006).

Various lesion studies have identified a restricted number of cortical regions straddling the sylvian fissure in the right hemisphere that are associated with the occurrence of spatial neglect, namely the inferior parietal lobule (IPL) and temporo-parietal junction (TPJ) (Heilman et al., 1983, Mort et al., 2003a, Vallar and Perani, 1986), the superior temporal gyrus (STG) and adjacent insular cortex (Karnath et al., 2001, Karnath et al., 2004), and – much less frequently – inferior frontal gyrus (IFG) (Husain and Kennard, 1996). Interestingly, several neuroimaging studies conducted with healthy subjects to investigate the neural substrates involved in processes of attentional orienting and visual search in the intact brain revealed activations that were essentially at odds with the anatomical findings in brain-damaged patients showing spatial neglect. Typically, they observed activations of the superior parietal lobule (SPL) and intraparietal sulcus (IPS) (Corbetta et al., 1995, Donner et al., 2000, Donner et al., 2002, Donner et al., 2003, Gitelman et al., 2002, Hopfinger et al., 2000, Leonards et al., 2000, Makino et al., 2004, Muller et al., 2003, Nobre et al., 2002, Olivers et al., 2004), i.e. activations that were far more dorsal to the typical lesion sites observed in patients with spatial neglect.

Among the large body of investigations on visual search behavior (Corbetta et al., 1995, Donner et al., 2000, Donner et al., 2002, Donner et al., 2003, Gitelman et al., 2002, Hopfinger et al., 2000, Leonards et al., 2000, Makino et al., 2004, Muller et al., 2003, Nobre et al., 2002, Olivers et al., 2004), those studies stand out which investigated visual search of target stimuli among numerous similar distracters (Gitelman et al., 2002, Nobre et al., 2002), i.e. tasks that are very similar to the typical exploration tasks used in the clinical diagnosis of patients with neglect (Gauthier et al., 1989, Ota et al., 2001, Weintraub and Mesulam, 1985). Gitelman et al. (2002) have compared free exploratory eye movements across a digit array with the instructed execution of horizontal saccades directed to predetermined targets. With respect to the cortical surface, the analysis revealed increased activation of the posterior parietal cortex (PPC) surrounding the intraparietal sulcus (IPS) and extending to visual association areas, the anterior insula and frontal eye fields (FEF). No significant signal differences were found in those areas typically lesioned in patients with spatial neglect (Heilman et al., 1983, Husain and Kennard, 1996, Karnath et al., 2001, Karnath et al., 2004, Mort et al., 2003a, Vallar and Perani, 1986). However, it must be pointed out that the authors focused their analysis on a certain number of regions (FEF, PPC, supplementary eye fields, anterior cingulate cortex, anterior insula, posterior temporal-occipital junction, basal ganglia, superior colliculi, and posterior thalami) by decreasing the statistical thresholds used for the detection of significant signal increases within these ROIs. This is a widely accepted procedure introduced by Worsley et al. (1996) allowing for a specific examination of the potential involvement of selected brain regions at the expense of valid and reliable findings in other areas (Turkheimer et al., 2004). Yet, most of those regions which have been reported as typical lesion sites in patients with spatial neglect (Heilman et al., 1983, Husain and Kennard, 1996, Karnath et al., 2001, Karnath et al., 2004, Mort et al., 2003a, Vallar and Perani, 1986) were not included as ROIs and thus were ‘disadvantaged’ in this analysis. A PET study by Nobre et al. (2002) employed a very similar behavioral paradigm but analyzed the data without any a priory assumptions of critical ROIs. This work found significant differences between free exploration and exogenously determined saccades being essentially confined to the superior parietal and occipital cortex (Nobre et al., 2002). Again, these results were inconsistent with the findings from numerous lesion studies in patients with exploratory disorders (Heilman et al., 1983, Husain and Kennard, 1996, Karnath et al., 2001, Karnath et al., 2004, Mort et al., 2003a, Vallar and Perani, 1986). Nobre et al. (2002) could not find evidence for a differential involvement of these latter areas in exploration tasks in comparison to the execution of predetermined saccades.

Up to now, a direct examination – i.e. a region of interest analysis (Turkheimer et al., 2004, Worsley et al., 1996) – of the contribution of those areas to active visual search which have been reported to be typically lesioned in patients showing a bias in spatial exploration, namely IPL, TPJ, STG, and IFG (Heilman et al., 1983, Husain and Kennard, 1996, Karnath et al., 2001, Karnath et al., 2004, Mort et al., 2003a, Vallar and Perani, 1986), is still missing. Thus, we conducted an fMRI experiment which was supposed to closely resemble the clinical tasks known to be sensitive to the patients' behavioral bias. We investigated visual exploration of a letter array similar to the cancellation task of Weintraub and Mesulam (1985). Brain activity has been compared in a search volume consisting of the bilateral IPL, TPJ, STG, and IFG during the execution of free exploratory eye movements with the activity during the execution of stepwise horizontal and vertical saccades to predetermined target positions.

Section snippets

Procedures

Thirteen right handed healthy subjects (8m/5f, mean age: 29 years, range: 20–47 years) participated in the experiment. All subjects gave their informed consent to participate in the study which has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. All subjects underwent 3 measurements of 750 s duration each. Visual exploration (VE) and two control tasks were applied in a block design (Fig. 1). The visual exploration control task (VEC)

Eye movements

The mean numbers of eye movements in the three conditions (VE: 229.4, SD 48.1; VEC: 131.6, SD 41.6; SC: 125.4, SD 38.3) have been compared in a repeated-measures ANOVA. The analysis revealed a significant effect of the factor condition (F1.051 = 41.5; P < 0.001). Pairwise post hoc comparisons employing paired t tests revealed significant differences between VE and VEC (t12 = 6.081; P < 0.001) and between VE and SC (t12 = 6.971; P < 0.001) indicating that the subjects executed a higher number of

Discussion

Our study was motivated by the inconsistent findings from neuroimaging studies of visual search in healthy subjects on the one hand and lesion mapping studies in patients with spatially biased free visual exploration on the other hand. While the former have identified the SPL and IPS as important structures involved in visual search, the latter found brain areas located far more ventrally. Therefore, we performed a region of interest analysis to specifically address a potential involvement of

Acknowledgments

This work was supported by grants from the Deutsche Forschungsgemeinschaft awarded to the first and third author (SFB550-A4, GK Kognitive Neurobiologie). This work was supported by grants from the Deutsche Forschungsgemeinschaft awarded to the first and third author (SFB550-A4, GK Kognitive Neurobiologie). We would like to thank Axel Lindner and Zoe Kourtzi for providing fMRI compatible eye tracking devices.

References (79)

  • N.G. Muller et al.

    The functional neuroanatomy of visual conjunction search: a parametric fMRI study

    NeuroImage

    (2003)
  • M. Niemeier et al.

    Stimulus-driven and voluntary saccades are coded in different coordinate systems

    Curr. Biol.

    (2003)
  • A.C. Nobre et al.

    Filtering of distractors during visual search studied by positron emission tomography

    NeuroImage

    (2002)
  • T. Paus

    Location and function of the human frontal eye-field: a selective review

    Neuropsychologia

    (1996)
  • J.D. Schmahmann et al.

    Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space

    NeuroImage

    (1999)
  • N. Tzourio-Mazoyer et al.

    Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain

    NeuroImage

    (2002)
  • G. Vallar et al.

    The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man

    Neuropsychologia

    (1986)
  • S.C. Blank et al.

    Speech production: Wernicke, Broca and beyond

    Brain

    (2002)
  • V.P. Clark et al.

    Responses to rare visual target and distractor stimuli using event-related fMRI

    J. Neurophysiol.

    (2000)
  • M. Corbetta et al.

    Control of goal-directed and stimulus-driven attention in the brain

    Nat. Rev., Neurosci.

    (2002)
  • M. Corbetta et al.

    Superior parietal cortex activation during spatial attention shifts and visual feature conjunction

    Science

    (1995)
  • M. Corbetta et al.

    Voluntary orienting is dissociated from target detection in human posterior parietal cortex

    Nat. Neurosci.

    (2000)
  • M. Corbetta et al.

    Neural basis and recovery of spatial attention deficits in spatial neglect

    Nat. Neurosci.

    (2005)
  • J.T. Crinion et al.

    Temporal lobe regions engaged during normal speech comprehension

    Brain

    (2003)
  • K.R. Daffner et al.

    The central role of the prefrontal cortex in directing attention to novel events

    Brain

    (2000)
  • M. D'Esposito et al.

    Prefrontal cortical contributions to working memory: evidence from event-related fMRI studies

    Exp. Brain Res.

    (2000)
  • T. Donner et al.

    Involvement of the human frontal eye field and multiple parietal areas in covert visual selection during conjunction search

    Eur. J. Neurosci.

    (2000)
  • T.H. Donner et al.

    Parietal activation during visual search in the absence of multiple distractors

    NeuroReport

    (2003)
  • J. Downar et al.

    A multimodal cortical network for the detection of changes in the sensory environment

    Nat. Neurosci.

    (2000)
  • J. Downar et al.

    A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities

    J. Neurophysiol.

    (2002)
  • A. Ellison et al.

    An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS

    Brain

    (2004)
  • M. Fruhmann-Berger et al.

    Spontaneous eye and head position in patients with spatial neglect

    J. Neurol.

    (2005)
  • K.-M.G. Fu et al.

    Auditory cortical neurons respond to somatosensory stimulation

    J. Neurosci.

    (2003)
  • L. Gauthier et al.

    The bells test: a quantitative and qualitative test for visual neglect

    Int. J. Clin. Exp. Neuropsychol.

    (1989)
  • Gharabaghi, A., Fruhmann Berger, M., Tatagiba, M., Karnath, H.-O., in press. The role of right superior temporal gyrus...
  • O.J. Grüsser et al.

    Localization and responses of neurons in the parieto-insular cortex of awake monkeys (Macaca fascicularis)

    J. Physiol.

    (1990)
  • O.J. Grüsser et al.

    Vestibular neurones in the parieto-insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses

    J. Physiol.

    (1990)
  • K.M. Heilman et al.

    Localizations of lesions in neglect

  • J.B. Hopfinger et al.

    The neural mechanisms of top-down attentional control

    Nat. Neurosci.

    (2000)
  • Cited by (58)

    • Altered Connectivity During a False-Belief Task in Adults With Autism Spectrum Disorder

      2020, Biological Psychiatry: Cognitive Neuroscience and Neuroimaging
    • A naturalistic viewing paradigm using 360° panoramic video clips and real-time field-of-view changes with eye-gaze tracking: Naturalistic viewing paradigm based on 360° panoramic video and real-time eye gaze

      2020, NeuroImage
      Citation Excerpt :

      Himmelbach et al. (2006) reported that the caudal STG along with the bilateral temporoparietal junction (TPJ) and IFG are part of the network related to voluntary visual orientation and exploration (Himmelbach et al., 2006). In addition, Suchan et al. (2014) reported possible pathways connecting the ROIs found in the study by Himmelbach et al. (2006), including a connection between the right IFG (rIFG) and the right STG (Suchan et al., 2014). We also identified the caudal STG region and the vicinity of the rIFG reported by Suchan et al. (2014) in the first step of the multiple regression.

    • Remodelling the attentional system after left hemispheric stroke: Effect of leftward prismatic adaptation

      2019, Cortex
      Citation Excerpt :

      The superior temporal region was repeatedly shown to be involved in visual attention. It is activated during attention to contralateral, visual targets (Macaluso & Frith, 2000) or the exploration of dense stimuli (Himmelbach, Erb, & Karnath, 2006). It is also part of larger attentional networks, such as those underlying the reorienting of attention (Thiel, Zilles, & Fink, 2004) or the transfer to allocentric frame of reference (Neggers, Van der Lubbe, Ramsey, & Postma, 2006).

    View all citing articles on Scopus
    View full text