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The Mccollough Effect Reveals Orientation Discrimination in a Case of Cortical Blindness G

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The Mccollough Effect Reveals Orientation Discrimination in a Case of Cortical Blindness G View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector The McCollough effect reveals orientation discrimination in a case of cortical blindness G. Keith Humphrey*, Melvyn A. Goodale*, Maurizio Corbettat and Salvatore Aglioti* *Department of Psychology, University of Western Ontario, London, Ontario, Canada N6A 5C2. tDepartment of Neurology, Washington University Medical School, St. Louis, Missouri 63110, USA. Dipartimento Di Scienze Neurologiche E Della Visione, Sezione di Fisiologia Umana, Universita Degli Studi di Verona, Verona 37134, Italy. Background: The McCollough effect is a colour after- demonstrated that the patient, P.B., has a profound effect that is contingent on the orientation of the patterns impairment in form perception and is even unable to used to induce it. To produce the effect, two differently discriminate between 900 differences in the orientation of oriented grating patterns - such as a red-and-black verti- grating stimuli. He is also unable to use orientation infor- cal grating and a green-and-black horizontal grating - mation to control his reaching or grasping. Nevertheless, are viewed alternately for a few minutes. After this period P.B. can name and discriminate different colours reliably, of adaptation, if the black-and-white test gratings are including those used to induce the McCollough effect. viewed in the same orientation as the adaptation patterns, After adaptation with red-and-green gratings, P.B. appro- the white sections of the vertical grating will appear pale priately reported the orientation-contingent aftereffect green and the white sections of the horizontal grating colours, even though he continued to be unable to will appear pink. The McCollough effect indicates that discriminate the orientations of the test patterns. colour- and orientation-coding mechanisms interact at Conclusions: These results indicate that at some level in some point during visual processing; but the question P.B.'s visual system orientation is being coded, but it is at remains as to whether this interaction occurs at an early or a level that he is unable to use in making orientation later stage in the cortical visual pathways. In an attempt to judgements or in visuomotor control. Given the massive answer this question, we studied a patient who had suf- insult to the extrastriate cortex in P.B., it is likely that the fered extensive damage to extrastriate visual areas of the anatomical locus of the mechanisms underlying the brain, which had left him able to see colour but little else. McCollough effect is within primary visual cortex or Results: Neuropsychological and perceptual tests even earlier in the visual pathway. Current Biology 1995, 5:545-551 Background a series of strategic (and answerable) questions for vision researchers, one of which was: 'Does the McCollough Colour aftereffects contingent on pattern orientation effect belong to early vision or to some higher-level were first reported in 1965 by Celeste McCollough [1]. cortical stage?' Several aspects of the McCollough effect To induce a McCollough effect, two differently oriented suggest that it involves an adaptation of mechanisms at grating patterns, such as a red-and-black vertical grating an early stage of visual processing (for reviews see [2,4]). and a green-and-black horizontal grating, are viewed In particular, it has been proposed that area 17 (or V1) alternately for a few minutes (see Fig. 1). After such of the visual cortex has the requisite properties for adaptation, black-and-white versions of the test patterns mediating the McCollough effect (for example, see are presented to subjects. White sections of the vertical [2,9,10]). McCollough [1] originally proposed that the test grating appear to the viewer to be tinted green, effect results from the colour adaptation of neurons in whereas the white sections of the horizontal test grating the visual cortex that code for local orientation - appear pink. If, however, the test patterns are rotated neurons fitting this description have been found in area 450 from the adapted orientations, colour aftereffects are V1. Michael [11] has suggested that the effect reflects not reported. adaptation of striate neurons that code simultaneously for both orientation and colour. It has also been hypoth- Since McCollough's original report, numerous studies esized that the colour-selective cells found in the 'blobs' of this aftereffect have confirmed and extended her ini- of area V1 [12,13] could be the site of the colour com- tial findings (for reviews see [2-4]), and several accounts ponent of this effect. To produce the effect, these of its functional role in vision have been proposed colour-sensitive cells would have to interact with other [2,5-7]. One of the issues that has concerned researchers cells in area V1 that are sensitive to both orientation and is the locus in the visual system of the mechanisms that spatial frequency, but which exhibit a broadband mediate the effect. Indeed, Julesz [8] has recently posed response to wavelength [9]. Correspondence to: G. Keith Humphrey. E-mail address: [email protected] © Current Biology 1995, Vol 5 No 5 545 546 Current Biology 1995, Vol 5 No 5 of objects [15,16]. Her colour perception, however, appears to be quite normal [17], and so we were able to examine her susceptibility to the McCollough effect. D.E was unable to report the orientation of simple grating stimuli, or even report whether one or two pat- terns were present. However, when she was adapted for 10 minutes with a red-and-black horizontal grating alter- nating with a green-and-black vertical grating, she reported the appropriate colour aftereffects when subse- quently presented with the black-and-white test gratings. Moreover, following a second session of adaptation, she reported the appropriate aftereffects some 20 hours later. Throughout all of this testing, she was unable to discrim- inate the orientation of any of the gratings that were successfully inducing colour percepts. In short, D.E showed McCollough effects without any ability to describe, discriminate or recognize the orientation of the inducing and test gratings. Given the pattern of D.E's brain damage, these findings are consistent with the hypothesis that primary visual cortex (or area V1) has the requisite properties for supporting the McCollough effect. It should be pointed out, however, that despite D.F's profound deficits in perception of form and orientation, she is able to orient her hand appropriately in anticipa- tion of grasping those same objects that she is unable to discriminate perceptually [15,16,18]. This suggests that, while D.F cannot make use of visual information about orientation and form for perceptual discrimination, she can use it for the control of skilled actions. Indeed, Goodale and Milner have used these observations as part of a proposal that the visual mechanisms mediating object perception are both functionally and neurally distinct from those underlying the visual control of skilled movements directed at those objects [19,20]. The sparing of form information for the control of skilled actions in D.E also suggests another possible interpretation for her ability to experience an orientation-contingent colour aftereffect. Specifically, because D.E can use orien- tation information to control her grasp and other motor Fig. 1. An illustration of typical induction and testing conditions outputs, it is possible that the orientation coding, beyond for the McCollough effect. Also illustrated is the simulated after- area V1, supporting this behaviour is somehow linked effect, given the induction conditions seen in the figure (see text for details). The colour characteristics of the aftereffect will vary with her intact colour processing. Thus, although it is somewhat as a function of adaptation conditions. In most experi- unlikely, the mediation of the McCollough effect in D.E ments, the inducing stimuli are presented as computer-generated may have occurred in areas beyond V1. What is clearly images or as projected slides. needed is a demonstration that the McCollough effect can occur in an individual with extrastriate damage of a such a Our recently published findings [14] are also consistent nature that any processing of form that may remain in area with the notion that area V1 is the site where the V1 is prevented from reaching those higher cortical areas McCollough effect is mediated. We studied a patient, D.E, that mediate perception and the visual control of action. who had developed a profound visual-form agnosia as a result of carbon monoxide poisoning. Although magnetic We recently had an opportunity to study the McCollough resonance imaging (MRI) revealed a pattern of damage effect in a patient who was essentially cortically blind. consistent with anoxia, most of the damage in the pos- Like D.F, this new patient, P.B., shows a profound terior portion of D.E's brain was evident in areas 18 and insensitivity to visual form, and is unable to recognize the 19, with area 17 (or V1) remaining largely intact. D.F has simplest of geometrical shapes. Patient P.B., however, has great difficulty recognizing even the simplest of geometric none of the spared visuomotor abilities that are seen in forms, and is very poor at discriminating the orientation D.F. Thus, we see no evidence for the processing of McCollough effect and cortical blindness Humphrey et al. RESEARCH PAPER 547 visual form for either perceptual discrimination or visuo- motor control. P.B., like D.F, does show remarkably intact colour perception, so we were able to use his spared colour perception to assess whether he was subject to the McCollough effect. The results obtained provided us with additional support for the view that the inter- action between colour and form that underlies the McCollough effect takes place in area V1 or earlier.
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