Blindsight in Action: What Can the Different Sub-Types of Blindsight Tell Us About the Control of Visually Guided Actions?
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Neuroscience and Biobehavioral Reviews 29 (2005) 1035–1046 www.elsevier.com/locate/neubiorev Review Blindsight in action: what can the different sub-types of blindsight tell us about the control of visually guided actions? James Danckerta,*, Yves Rossettib,c,d aDepartment of Psychology, University of Waterloo, 200 University Avenue West, Waterloo, Ont., Canada N2L 3G1 bEspace et Action, INSERM Unite´ 534 and Universite´ Claude Bernard, 16 Avenue doyen Le´pine, 69676 Bron Cedex, France cService de Re´e´ducation Neurologique, Hoˆpital Henry Gabrielle, Universite´ Claude Bernard and Hospices Civils de Lyon, Route de Vourles, St Genis Laval Cedex, France dInstitut Fe´de´ratif des neurosciences de Lyon, 59 Boulevard Pinel, 69003 Lyon, France Received 27 July 2004; revised 13 December 2004; accepted 7 February 2005 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. q 2005 Elsevier Ltd. All rights reserved. Keywords: Blindsight; Visuomotor control; Parietal cortex Contents 1. Introduction ...................................................................................1035 2. A new taxonomy for residual behaviours in blindsight ....................................................1036 2.1. Parietal cortex and action-blindsight ............................................................1039 2.2. Action-blindsight operates in the here and now ....................................................1041 2.3. ‘Action-blindsight’ and the automatic pilot .......................................................1041 3. Conclusion: action-blindsight—the automatic pilot in slow motion? ..........................................1043 Acknowledgements . .............................................................................1045 References ....................................................................................1045 1. Introduction * Corresponding author. Tel.: C1 519 888 4567x7014; fax: C1 519 734 Blindsight refers to the residual visual abilities that some 8631. patients with visual field defects demonstrate for stimuli E-mail addresses: [email protected] (J. Danckert), [email protected] (J. Danckert), [email protected] placed in their blind fields (Po¨ppel et al., 1973; Weiskrantz (Y. Rossetti). et al., 1974; Perenin and Jeannerod, 1975). That is, although patients with primary occipital (area V1) lesions are 0149-7634/$ - see front matter q 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.neubiorev.2005.02.001 essentially blind in one visual hemifield, they can 1036 J. Danckert, Y. Rossetti / Neuroscience and Biobehavioral Reviews 29 (2005) 1035–1046 nevertheless demonstrate above chance performance when In this selective review we will suggest a new taxonomy responding to stimuli placed in their blind field. For example, for describing the various residual capacities demonstrated when asked to guess, under the appropriate conditions, the by blindsight patients. It is important to note that this location of a target that was briefly illuminated in the blind taxonomy is intended to describe distinct types of residual hemifield, some patients guess the location accurately on behaviours demonstrated by blindsight patients. While greater than 50% of trials (Weiskrantz et al., 1974; Zihl and some discussion of the neural networks underlying these Werth, 1984a,b). Initially, the most common residual ability distinct behaviours is obviously warranted, at this stage such demonstrated by blindsight patients was the ability to a discussion is necessarily speculative. We will then explore localize, either by pointing or eye movements, targets in more detail one of the proposed definitions of a blindsight presented to the blind field. This ability to localize blind capability—namely ‘action-blindsight’ in which patients field targets has also been demonstrated in hemidecorticated with V1 lesions are able to localize blind field targets by patients (Perenin and Jeannerod, 1978; Ptito et al., 1991). virtue of motor actions (e.g. pointing, grasping or saccades). Taken together, these results suggest subcortical involve- Finally, we will examine how action-blindsight can inform ment in the residual functions of these patients (see models of visually guided action. Jeannerod and Rossetti (1993) and Rossetti and Pisella (2002) for review). However, since the earliest work on 2. A new taxonomy for residual behaviours in blindsight blindsight, a wide range of residual functions have been described, ranging from motion, form and wavelength The earliest demonstrations of blindsight involved asking discrimination, to remarkable demonstrations of semantic the patient to motorically guess the location of a target that priming from words presented to the blind field (Danckert had been briefly flashed in the blind field (Po¨ppel et al., 1973; et al., 1998; Magnussen and Mathiesen, 1989; Marcel, 1998; Weiskrantz et al., 1974; Perenin and Jeannerod, 1975). Morland et al., 1999; Stoerig and Cowey, 1989). Although Weiskrantz first coined the term ‘blindsight’ to account for still somewhat controversial, the performance of blindsight the paradoxical observation of accurate eye and arm patients suggests that visual information is able to reach movements directed toward a visual target that was not extrastriate visual cortex via pathways that do not depend on consciously perceived. Since these early demonstrations, processing in area V1 (see Stoerig and Cowey (1997) for localization of targets presented to the blind field by various review). That is, it has been suggested that the residual means has been by far the most common residual ability pathway which runs from the eye directly to the superior demonstrated (e.g. Weiskrantz et al., 1974; Perenin and colliculus and from there to the pulvinar nucleus of the Jeannerod, 1975; Zihl and Werth, 1984a,b; Danckert et al., thalamus is responsible for the ability to localize blind field 2003; Kentridge et al., 1999a,b). The ability to point or targets (Weiskrantz et al., 1974; Zihl and Werth, 1984a,b). saccade towards a blind field target strongly supported the The many and varied residual abilities demonstrated by some notion that the extrageniculate pathway directly from the eye blindsight patients may suggest, however, that blindsight to the superior colliculus was responsible for this residual relies on not one, but many residual pathways (Danckert and ability (sometimes referred to as the retino-tectal pathway; Goodale, 2000).1 Accordingly, visual projections from Fig. 1). This was especially true for saccades made to blind subcortical structures, and in particular from the pulvinar, field targets given the wealth of literature demonstrating may project not only onto parietal but also onto temporal collicular involvement in the control of eye movements (see cortex. In addition, there is some recent anatomical evidence Gaymard and Pierrot-Deseillingy (1999) for review). This from the macaque monkey that demonstrated direct konio- hypothesis gained even further support from findings in cellular inputs from the interlaminar layers of the LGN to the hemidecorticated patients (Perenin and Jeannerod, 1978; middle temporal (MT) motion-sensitive region of visual Ptito et al., 1991). That is, despite having little or no cortex (Sincich et al., 2004). This finding provides evidence remaining cortex in the damaged hemisphere, these patients for an alternate residual pathway that may subserve the were nevertheless able to show above chance localization of Riddoch phenomenon (see below for a more detailed blind field targets, heavily implicating the retinofugal description of Riddoch phenomenon; Zeki and Ffytche pathway from the eye to the superior colliculus (Perenin (1998); see also Benevento and Yoshida (1981) for and Jeannerod, 1978; Ptito et al., 1991). The requirement that discussion of other LGN inputs to prestriate cortex). an action—pointing or saccading—be used to demonstrate above chance localization of blind field targets leads us to call this kind of residual function ‘action-blindsight’. 1 There has been substantial debate in the literature concerning the As distinct from action-blindsight, some patients demon- possibility that the residual abilities observed in blindsight patients are in strate residual abilities that do not completely lack