Detecting the wrong signals?

Detecting the wrong signals?

Forum TRENDS in Cognitive Sciences Vol.6 No.10 October 2002 443 Book Review Detecting the wrong signals? Out of Mind: Varieties of Unconscious Pro...

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TRENDS in Cognitive Sciences Vol.6 No.10 October 2002

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Book Review

Detecting the wrong signals? Out of Mind: Varieties of Unconscious Processes edited by Beatrice De Gelder, Edward de Haan and Charles Heywood, Oxford University Press, 2001. £49.95/$85.00 (296 pages) ISBN 0 19 850630 9

‘Out of Mind’ is a collection of papers that arose from a symposium to mark the award of an honorary degree to Professor Larry Weiskrantz at Tilberg University in 1998, and to celebrate his distinguished contributions to the renaissance of ‘consciousness studies’. As one would expect, the papers range widely over the topics of blindsight, unconscious processing and implicit processing. The unifying theme is that the brain contains many parallel and partially independent modalities of information processing, and that only a subset of these – possibly a small subset – is conscious. Nearly all the essays in the collection are interesting. The book provides an excellent opportunity for a sceptic about ‘blindsight’ to assess the evidence and to see how it all hangs together. This ‘sceptical psychophysicist’ was confused on a first reading by the lumping together of many disparate phenomena under the ‘blindsight’ label. In its restricted sense, blindsight refers to the ability of an observer to make a correct verbal or non-verbal decision about some attribute of a visual stimulus, in the absence of any acknowledged verbal awareness of the presence of that stimulus. Weiskrantz’s definition rejects even the poor ‘yes/no’ detection performance of subject GY as relevant to blindsight. A ‘yes/no’ task (according to Weiskrantz) asks the observer whether the stimulus was present or absent, not whether they were aware of it, and it is therefore irrelevant to blindsight. The sole criterion for blindsight thus appears to be that, in conversation, the observer denies awareness of the stimulus that they have correctly detected in a psychophysical http://tics.trends.com

task. This seems clear enough, but in that case, it is difficult to understand why claims for the existence of ‘blindsight’ are buttressed (as they are in Chapter 2) by appeals to the pervasiveness of ‘implicit processing’. The latter, as I understand it, refers to (or at least includes) cases where a stimulus can be shown to affect some aspect of behaviour when it is not detected in a psychophysical task; for example, semantic priming by a stimulus that has a d′ ≈ 0 in a two-alternative forced-choice task for its presence/absence (d′ is a criterion-free measure of the sensitivity of the observer to the presence of a stimulus). Chapter 4 defines covert processing as those cases ‘when a stimulus which fails to elicit conscious experience nevertheless exerts influences on behaviour’ (p. 63). This definition is wide enough to include any case where a stimulus affects behaviour (for example, an eye movement or the ERG) without being detectable, but the peculiarity of ‘blindsight’ is that detection is itself ‘covert’. This important distinction is muddied by treating blindsight as just another case of covert or implicit processing. In trying to order these issues in my own mind, I found it helpful to start from the minimalist model of the observer that is called ‘Signal Detection Theory’ (SDT). In SDT there is a physical stimulus, a set of analysers, which have different responses to stimuli, and a decision stage in which the observer makes use of the pattern of response in the analysers to try to answer some question about the stimulus [1,2]. Analysers can be subject to linear or to non-linear combinations before the decision stage. The stimuli and/or the analysers are subject to noise, which produces errors at the decision stage. The ideal observer monitors the analyser(s) that provide the best information about the stimulus and uses maximum-likelihood as the decision rule; the real observer [3], as opposed to the ideal, might monitor irrelevant analysers as well, and therefore suffer as a result if noise is independent across analysers (uncertainty). The real observer might even fail to monitor the correct analyser at all, in which case the stimulus might affect some other aspect of behaviour (such as the pupillary response) without being detected above chance. Even with this minimalist model we can see the potential for several kinds of ‘unconscious processing’. There is no

implication in SDT that the observer can verbally report which analysers were used for a particular detection task. Some analysers might affect detection without the observer being able to report their individual output. In ‘crowding’, for example, the observer cannot report the orientation of individual tilted lines but adaptation reveals that orientation-tuned analysers are still active [4]; the explanation may be that in crowded arrays there is obligatory averaging over stimuli before they reach the decision stage [5]. Gratings of too high a spatial or temporal frequency to be resolved nevertheless have psychophysically measurable effects [6,7]. The design of these experiments is formally very similar to many of the demonstrations of implicit processing discussed in this book, for example, priming by undetectable stimuli. (Read ‘adaptation’ for ‘priming’ and you get the picture.) Yet the psychophysical experiments are carried out entirely within the framework of SDT, and pose no problems for that theory. SDT can also be used as a framework for understanding other dissociations between stimulus analysers and decision. Consider a task where the observer must report the orientation of a slightly tilted line. In this experiment, thresholds are raised if the line is embedded in vertical distracters and lowered again if the relevant stimulus is ‘cued’. In SDT the explanation is ‘uncertainty’, which causes the observer to monitor irrelevant noise sources in the decision stage when the stimulus is uncued [8]. Uncertainty is a pervasive principle that should be taken into account before asserting implicit processing. Yet in the first paragraph of the Introduction to this book we read the following evidence for implicit processing: ‘A patient with Korsakoff’s psychosis was informed of MacCurdy’s name and address, which, unsurprisingly, was rapidly forgotten. When subsequently asked to select, by guesswork, from among 10 alternative forenames, surnames, street names and numbers, the patient performed with astonishing accuracy’. In SDT there is no such thing as an ‘undetectable stimulus’. Detection is limited by noise, which produces a probabilistic relation between stimulus strength and detection performance (the psychometric function). To be meaningful, therefore, claims for implicit processing of ‘undetectable’ stimuli should quote the

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d′ value of the stimulus, or even better, present the whole psychometric function. Few (if any) of the claims in this book pass this simple test. We learn, for example, that emotional faces can activate the amygdala (Chapters 11–13), even when they are made undetectable by backward masking, yet d′ values are nowhere stated. The idea that an observer’s amygdala has a lower threshold for recognizing a facial emotion than the psychophysical observer is an interesting and exciting one, but before we believe it, we need to establish that the haemodynamic fMRI response in the amygdala is a more reliable signal to the presence of an emotional face than the detection performance of the observer: rather along the lines of the comparison between the neurometric and psychometric functions for neurones and monkeys, respectively [9]. In the latter case, there would have been endless possibilities for debate about whether the monkey was or was not ‘aware’ of activity in MT/V5 neurones, had SDT not been used. Azzopardi and Cowey (Chapter 1) report a very welcome application of SDT to the ubiquitous ‘blindsight’ patient GY. Their subtle approach is to compare GY’s performance on a ‘yes/no’ and a two-alternative forced-choice task (2AFC). GY was given a scale to express his confidence in both his ‘yes’ and his ‘no’ responses. In SDT multiple confidences correspond to multiple criteria. In other words, the observer is assumed to have access to the likelihood ratio on any particular trial, and to be able to assign it to the appropriate ‘bin’between two confidence intervals. GY was able to do this, but his sensitivity (d′) thus measured was considerably lower than in the 2AFC task, which is criterion-free. Azzopardi and Cowey infer from these findings that GY’s detection process is not the same as that of normal observers with weak signals. Ironically, the first paper to compare yes/no and 2AFC in normal observers also found that yes/no performance was poorer than 2AFC [10]. The difference was much smaller than in GY, and was not found in Azzopardi and Cowey’s normal observers. The author of that paper (Nachmias) conjectured that normal observers use sub-optimal strategies in ‘yes/no’ tasks. One such might be to put the confidence intervals too close together, so that they become confused. As Azzopardi and Cowey note, inability to maintain stable criteria in yes/no tasks will masquerade as a reduction in d′. http://tics.trends.com

TRENDS in Cognitive Sciences Vol.6 No.10 October 2002

The consequences of using indiscriminable confidence intervals were apparent in an experiment that found no correlation at all between performance and confidence in normal observers [11]. It can be argued that this was because they required their observers to use the whole of a nine-point confidence scale in circumstances when they were actually very uncertain on all trials [12]. Clearly, there are constraints on the observer’s ability to maintain stable criteria, and the relative sensitivity in yes/no and 2AFC tasks can be manipulated to produce a discrepency between yes/no and 2AFC performance. It is a moot point whether we conclude that GY is fundamentally different from normal observers, or that he lies on a continuum described by SDT. In any case, as noted earlier, Weiskrantz rejects the ‘yes/no’ task as a measure of blindsight. His argument is that GY was being asked a question about the stimulus, not about his awareness of it. Although this might seem to be cutting the cake pretty fine, the distinction between objective and subjective judgements is a valid one. An experienced observer might see the Muller-Lyer illusion, yet judge that the lines are really the same length . The problem underlying the whole unconscious perception debate is how to measure awareness, when objective measures are by definition excluded. In practice, awareness is inferred from the observer’s own reports. Note that this is not the same as putting priority on verbal behaviour, because the blindsight patient can verbally report the stimulus, but on a particular kind of verbal behaviour: the ability to talk about having a perception rather than just having one. Leibnitz would have said that GY is having a perception, but not an ‘apperception’; the philosopher would not have found this surprising, because it is exactly the state he ascribed to the normal observer during sleep, and to his ‘windowless’ monads. The patient DF, described by Milner and Dijkerman (Chapter 14), appears to be in a similar state, as she can correctly guide her actions to stimuli without being able to give a verbal account of the stimulus. The authors conclude that DF is completely unaware of her actions, but this is surely an unwarranted and unbelievable conclusion. The data show only that she cannot use her actions to infer the nature of the stimulus. The idea that the ‘dorsal pathway’ is an unconscious automaton runs counter to the experience of athletes, to the involvement

of the dorsal pathway in ‘neglect’ (Driver and Vuilleumier, Chapter 7), and to some neuroimaging data (see [13] for a review). Perhaps I am missing something, but I can see nothing in the description of DF to suggest that she is unaware of visual space or of her actions. ‘Blindsight’, then (as opposed to implicit or covert awareness) is a curious condition in which a patient perceives visual stimuli but has no knowledge of having perceived them. Whatever the blindsight patient is experiencing, he is unable to communicate it to us. It is disappointing to learn that no conceivable SDT experiment, or other objective test, is able to capture this phenomenon, but in psychophysics as elsewhere it is sometimes important to acknowledge that ‘Le meglio è l’inmico del bene’ (‘The best is the enemy of the good’). This ‘skeptical psychophysicist’ remains agnostic about the evidence for ‘blindsight’ in the restricted sense, but finds no problem in principle with the idea that there are experiences that cannot be communicated. After all, this is notoriously the case with sensations such as the colour red, which we can certainly experience, but not describe. When we consider the diverse populations of cell types in the brain, the multiple pathways for perception, and the recency of language in our evolution, the wonder is not that language does rather a poor job in describing perception, but that, like Dr Johnson’s dog walking on its hind legs, it can perform the task at all. Michael J. Morgan Applied Vision Research Centre, City University, Northampton Square, London, UK EC1V 0HB References 1 Green, D.M. and Swets, J.A. (1966) Signal Detection Theory and Psychophysics. (1st edn), John Wiley & Sons 2 Graham, N.V.S. (1989) Visual Pattern Analysers. Oxford Psychology Series (Vol. 16) (Broadbent, D.E. et al., ed.), Oxford University Press 3 McKee, S.P. (1985) The challenge of the real observer. In Frontiers of Visual Science: Proceedings of the 1985 Symposium, pp. 38–50, National Academy Press 4 He, S., Cavanagh, P. and Intriligator, J. (1996) Attentional resolution and the locus of visual awareness. Nature 383, 334–337 5 Parkes, L. et al. (2001) Compulsory averaging of crowded orientation signals in human vision. Nat. Neurosci. 4, 739–744 6 MacLeod, D.I.A. and He, S. (1992) Visible flicker from invisible patterns. Nature 362, 256–258 7 Smallman, H.S. et al. (1996) Fine-grain of the neural representation of human spatial vision. J. Neurosci. 16, 1852–1859

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8 Pelli, D.G. (1986) Uncertainty explains many aspects of visual contrast detection and discrimination. J. Opt. Soc. Am. Ser. A 2, 1508–1532 9 Newsome, W.T., Britten, K.H. and Movshon, J.A. (1989) Neuronal correlates of a perceptual decision. Nature 341, 52–54 10 Nachmias, J. (1981) On the psychometric function for contrast detection. Vis. Res. 21, 215–223 11 Kolb, F.C. and Braun, J. (1995) Blindsight in normal observers. Nature 377, 336–338 12 Morgan, M.J., Mason, A.J.S. and Solomon, J.S. (1997) ‘Blindsight’ in normal observers. Nature 385, 401–402 13 Rees, G (2001) Neuroimaging of visual awareness in patients and normal subjects. Curr. Opin. Neurobiol. 11, 150–156

Pretending primates Pretending and Imagination in Animals and Children edited by Robert W. Mitchell. Cambridge University Press, 2002. £55.00 (388 pages) ISBN 0 521 77030 0

Over the course of the past two decades an extensive body of literature has begun to define the social-cognitive abilities (e.g. imitation, selfrecognition and gaze-following) of human and nonhuman animals. However, although pretend play has been identified as a crucial component of social-cognitive development in humans, little empirical or theoretical interest has been generated during this period into the nature of pretence in other animals. Pretending and Imagination in Animals and Children is therefore long overdue. The literature on human children has featured considerable speculation over what levels of mental representation are necessary to support pretence and whether or not children must conceive of pretend play as a mental, as opposed to a purely physical, act. This theme is revisited in several chapters in Pretending and Imagination devoted to children’s pretence. Although there is some disagreement as to the age at which children understand pretence as a mental act (contributions by Lillard, Woolley), the pervasive view adhered to through these chapters is that to engage in pretend play children need only concentrate on the actions that occur http://tics.trends.com

within the pretend scenario. This view of pretence coheres with Perner’s influential suggestion that pretend play relies on the development of an ability to entertain ‘secondary representations’ – mental representations of things in the world, not how they are but how they could be [1]. Evaluating the level of mental representational capacity necessary to support pretend play in children is important as it provides us with a framework for assessing the credibility of pretend-like behaviour in animals. Of relevance here are chapters reporting on empathic behaviour in bonobos (Ingmanson) and on chimpanzees passing DeLoache-type reasoning tasks (Boysen and Kuhlmeier) – behaviours that are likely to involve secondary representations [2]. Thus, if the distinction is drawn between capacity and expression, we have some assurance that the great apes have the basic representational ability to support pretence. In this context, reports of pretend play in the great apes (Russon, Matevia et al.) remain plausible. By contrast, Zellor presents a series of observations of behaviour in monkeys, much of which she interprets as indicative of pretend play. However, in each of these observations alternative interpretations that do not evoke pretence can be offered. Moreover, to date there is no convincing evidence for secondary representation in any non-hominoid primate [2]. Therefore, Zellor’s interpretations and the claim on the cover of the book that ‘monkeys may share capacities for imagination with children’, should be treated with a healthy level of scepticism. Even if it is accepted that the great apes are capable of pretending, there is a glaring absence of evidence in the book for these animals engaging in pretence with any reliable frequency. Moreover, the pretence catalogued in the great apes contrasts starkly with the richness and complexity of the pretending noted in human children (Kavanaugh, Myers, Taylor and Carlson). According to Roberts and Krause, who provide an intriguing explanation for this disparity, pretend play did not fully emerge in human evolution until the development of an ecological niche characterized by the prevalence of post-reproductive women and the appearance of childhood as a life stage. This ecological niche is absent in non-human primate societies and helps explain why the most convincing examples

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of pretence in the great apes come from human-reared individuals. As an introduction to the nature and development of pretending in human children and the possible analogues of such behaviour in our primate cousins, Pretending and Imagination is a welcome addition to the literature. However, it is not comprehensive. First, the chapters devoted to non-humans focus solely on primates, and hence the use of ‘animals’ in the title is somewhat misleading. Second, no chapter is dedicated to an evaluation of pretence in children with autism. Although the literature on pretence in children with autism is complex, it has driven and illuminated much of the research into normally developing children and is deserving of treatment in a book such as this. It is also relevant to note that there is a lack of consistency in the use of terms used to describe the representational nature of pretend play. For example, in various chapters ‘secondary representations’ are incorrectly referred to as either ‘metarepresentations’ or ‘second order representations’. Although reflecting the wider literature, the uninitiated reader could be confused and frustrated by the inconsistent use of these terms within the same volume. Irrespective of these criticisms, as Mitchell’s review chapter attests, there has been little modern study of pretending in non-human animals. This represents a significant gap in the literature, and Mitchell’s book is a laudable first step in addressing that gap. Given arguments that pretence might function as an ontogenetic and phylogenetic precursor to the development of a theory of mind (e.g. Refs [3,4]), the value of this endeavour should not be understated. Mark Nielsen School of Psychology, University of Queensland, Brisbane, QLD 4072, Australia. e-mail: [email protected] References 1 Perner, J. (1991) Understanding the Representational Mind, MIT Press 2 Suddendorf, T. and Whiten, A. (2001) Mental evolution and development: evidence for secondary representation in children, great apes and other animals. Psychol. Bull. 127, 629–650 3 Leslie, A. (1987) Pretense and representation: the origins of ‘theory of mind’. Psychol. Rev. 94, 412–426 4 Whiten, A. (1996) Imitation, pretence and mindreading: Secondary representation in comparative primatology and developmental psychology? In Reaching into Thought: The Minds of the Great Apes (Russon, A.W. et al., eds), pp. 300–324, Cambridge University Press

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