ReviewBlindsight in action: what can the different sub-types of blindsight tell us about the control of visually guided actions?
Introduction
Blindsight refers to the residual visual abilities that some patients with visual field defects demonstrate for stimuli placed in their blind fields (Pöppel et al., 1973, Weiskrantz et al., 1974, Perenin and Jeannerod, 1975). That is, although patients with primary occipital (area V1) lesions are essentially blind in one visual hemifield, they can nevertheless demonstrate above chance performance when responding to stimuli placed in their blind field. For example, when asked to guess, under the appropriate conditions, the location of a target that was briefly illuminated in the blind hemifield, some patients guess the location accurately on greater than 50% of trials (Weiskrantz et al., 1974, Zihl and Werth, 1984a, Zihl and Werth, 1984b). Initially, the most common residual ability demonstrated by blindsight patients was the ability to localize, either by pointing or eye movements, targets presented to the blind field. This ability to localize blind field targets has also been demonstrated in hemidecorticated patients (Perenin and Jeannerod, 1978, Ptito et al., 1991). Taken together, these results suggest subcortical involvement in the residual functions of these patients (see Jeannerod and Rossetti, 1993, Rossetti and Pisella, 2002 for review). However, since the earliest work on blindsight, a wide range of residual functions have been described, ranging from motion, form and wavelength discrimination, to remarkable demonstrations of semantic priming from words presented to the blind field (Danckert et al., 1998, Magnussen and Mathiesen, 1989, Marcel, 1998, Morland et al., 1999, Stoerig and Cowey, 1989). Although still somewhat controversial, the performance of blindsight patients suggests that visual information is able to reach extrastriate visual cortex via pathways that do not depend on processing in area V1 (see Stoerig and Cowey (1997) for review). That is, it has been suggested that the residual pathway which runs from the eye directly to the superior colliculus and from there to the pulvinar nucleus of the thalamus is responsible for the ability to localize blind field targets (Weiskrantz et al., 1974, Zihl and Werth, 1984a, Zihl and Werth, 1984b). The many and varied residual abilities demonstrated by some blindsight patients may suggest, however, that blindsight relies on not one, but many residual pathways (Danckert and Goodale, 2000).1 Accordingly, visual projections from subcortical structures, and in particular from the pulvinar, may project not only onto parietal but also onto temporal cortex. In addition, there is some recent anatomical evidence from the macaque monkey that demonstrated direct koniocellular inputs from the interlaminar layers of the LGN to the middle temporal (MT) motion-sensitive region of visual cortex (Sincich et al., 2004). This finding provides evidence for an alternate residual pathway that may subserve the Riddoch phenomenon (see below for a more detailed description of Riddoch phenomenon; Zeki and Ffytche (1998); see also Benevento and Yoshida (1981) for discussion of other LGN inputs to prestriate cortex).
In this selective review we will suggest a new taxonomy for describing the various residual capacities demonstrated by blindsight patients. It is important to note that this taxonomy is intended to describe distinct types of residual behaviours demonstrated by blindsight patients. While some discussion of the neural networks underlying these distinct behaviours is obviously warranted, at this stage such a discussion is necessarily speculative. We will then explore in more detail one of the proposed definitions of a blindsight capability—namely ‘action-blindsight’ in which patients with V1 lesions are able to localize blind field targets by virtue of motor actions (e.g. pointing, grasping or saccades). Finally, we will examine how action-blindsight can inform models of visually guided action.
Section snippets
A new taxonomy for residual behaviours in blindsight
The earliest demonstrations of blindsight involved asking the patient to motorically guess the location of a target that had been briefly flashed in the blind field (Pöppel et al., 1973, Weiskrantz et al., 1974, Perenin and Jeannerod, 1975). Weiskrantz first coined the term ‘blindsight’ to account for the paradoxical observation of accurate eye and arm movements directed toward a visual target that was not consciously perceived. Since these early demonstrations, localization of targets
Conclusion: action-blindsight—the automatic pilot in slow motion?
We have previously demonstrated that a greater degree of sparing of the PPC is associated with more robust action-blindsight (Danckert et al., 2003). In those same patients we attempted to explore the possibility that automatic corrections of pointing movements would also be possible even though the patients were never aware of the presence of the targets or perturbations in target locations (Danckert and Rossetti, unpublished data). That is, if action-blindsight does indeed depend on the
Acknowledgements
The authors wish to thank Claude Prablanc, Denis Pélisson, Laure Pisella, Gilles Rode, Alain Vighetto, Hisaaki Ota, Aarlenne Khan and Masami Ishihara for numerous fruitful discussions. This work was supported by funds from the McDonnel-Pew foundation (YR), from Lyon University (JD), from the Leverhulme International Research Exchange Trust (JD and YR), from Programme Hospitalier de Recherche CLinique (PHRC 30251 to YR) and from the Natural Sciences and Engineering Research Council of Canada
References (75)
- et al.
Size-contrast illusions deceive the eye but not the hand
Curr. Biol.
(1995) - et al.
A conscious route to unconscious vision
Curr. Biol.
(2000) - et al.
Measuring unconscious actions: exploring the kinematics of pointing movements to targets in the blind field of two patients with cortical hemianopia
Neuropsychologia
(2003) - et al.
Inhibitory tagging of locations in the blind field of hemianopic patients
Conscious Cogn.
(1997) - et al.
Visual illusion and action
Neuropsychologia
(1996) - et al.
Separate visual pathways for perception and action
Trends Neurosci.
(1992) - et al.
Differences in the visual control of pantomimed and natural grasping movements
Neuropsychologia
(1994) - et al.
Effects of temporal cuing on residual visual discrimination in blindsight
Neuropsychologia
(1999) - et al.
A possible role of the superior colliculus in eye–hand coordination
Prog. Brain Res.
(2001) - et al.
Detection of moving and stationary gratings in the absence of striate cortex
Neuropsychologia
(1989)
Residual vision in cortically blind hemifields
Neuropsychologia
Visual function within the hemianopic field following early hemidecortication in man. I Spatial localization
Neuropsychologia
Implicit short-lived motor representation of space in brain-damaged and healthy subjects
Conscious Cogn.
Varieties of vision: from blind responses to conscious recognition
Trends Neurosci.
Contributions to the study of ‘blindsight’ I. Can stray light account for saccadic localization in patients with postgeniculate visual field defects?
Neuropsychologia
Contributions to the study of ‘blindsight’ II. The role of specific practice for saccadic localization in patients with postgeniculate visual field defects
Neuropsychologia
Topographic organization of human visual areas in the absence of input from primary cortex
J. Neurosci.
The afferent and efferent organisation of the lateral geniculo-prestriate pathways in the macaque monkey
J. Comp. Neurol.
A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing
J. Neurophys.
Direct evidence for the contribution of the superior colliculus in the control of visually guided reaching movements in the cat
J. Physiol.
Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas
Exp. Brain Res.
Investigating form and colour perception in blindsight using an interference task
Neuroreport
A temporal analysis of graspining in the ebbinghuas illusion: planning versus online control
Exp. Brain Res.
Disorders of Space Exploration and Cognition
Postural and synergic control for three-dimensional movements of reaching and grasping
J. Neurophys.
Role of the parietal cortex in updating reaching movements to a visual target
Nat. Neurosci.
Functional anatomy of non-visual feedback loops during reaching: a positron emission tomography study
J. Neurosci.
Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements
J. Neurophys.
Neurology of saccades and smooth pursuit
Curr. Opin. Neurol.
Visual activity in areas V3a and V3 during reversible inactivation of area V1 in the macaque monkey
J. Neurophys.
Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1
J. Neurophys.
Dynamic illusion effects in a reaching task: evidence for separate visual representations in the planning and control of reaching
J. Exp. Psychol. Hum. Percept Perform
Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement
Nature
A neurological dissociation between perceiving objects and grasping them
Nature
Postural invariance in three-dimensional reaching and grasping movements
Exp. Brain Res.
Grasping after a delay shifts size-scaling from absolute to relative metrics
J. Cogn. Neurosci.
Cited by (145)
Blindsight: Functions, methods and neural substrates
2021, Encyclopedia of Behavioral Neuroscience: Second EditionNeural Mechanism of Blindsight in a Macaque Model
2021, NeuroscienceIs the primary visual cortex necessary for blindsight-like behavior? Review of transcranial magnetic stimulation studies in neurologically healthy individuals
2021, Neuroscience and Biobehavioral ReviewsVisual fixation in disorders of consciousness: Development of predictive models to support differential diagnosis
2021, Physiology and Behavior