Review
Blindsight in action: what can the different sub-types of blindsight tell us about the control of visually guided actions?

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Abstract

Blindsight broadly refers to the paradoxical neurological condition where patients with a visual field defect due to a cortical lesion nevertheless demonstrate implicit residual visual sensitivity within their field cut. The aim of this paper is twofold. First, through a selective review of the blindsight literature we propose a new taxonomy for the subtypes of residual abilities described in blindsight. Those patients able to accurately act upon blind field stimuli (e.g. by pointing or saccading towards them) are classified as having ‘action-blindsight’, those whose residual functions can be said to rely to some extent upon attentive processing of blind field stimuli are classified as demonstrating ‘attention-blindsight’, while finally, patients who have somewhat accurate perceptual judgements for blind field stimuli despite a complete lack of any conscious percept, are classified as having ‘agnosopsia’—literally meaning ‘not knowing what one sees’. We also address the possible neurological substrates of these residual sensory processes. Our second aim was to investigate the most striking subtype of blindsight, action-blindsight. We review the data relevant to this subtype and the hypotheses proposed to account for it, before speculating on how action-blindsight may inform our normal models of visuomotor control.

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

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