Ординатура / Офтальмология / Английские материалы / The Neuropsychology of Vision_Fahle, Greenlee_2003

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Chapter 9

Unconscious perception: blindsight

L. Weiskrantz

Introduction

The definition of ‘blindsight’ can now be obtained directly from the Concise Oxford dictionary (and other dictionaries): ‘Medicine: a condition in which the sufferer responds to visual stimuli without consciously perceiving them’. It is associated with damage to V1, primary visual cortex. The historical background to the origin of the oxymoron stems originally from animal work, because it has been known for some decades that monkeys with V1 removal can nevertheless carry out particular visual discriminations with moderate success. Prima facie, this is not surprising because V1 is not the only target in the brain for signals originating in the retina, although it is the major one. There are several other pathways from the retina to subcortical targets that remain intact after damage to V1, the largest one being the superior colliculus, from which information can reach a very wide distribution of other cerebral areas, both cortical and subcortical (Cowey and Stoerig 1991; Benevento and Yoshida 1981; Herandez-Gonzales and Reinoso-Suarez 1994; Fries 1981; Yukie and Iwai 1981). In man, in seeming contrast to the animal findings, subjects with V1 damage are said to be densely ‘blind’ in the corresponding part of the affected visual fields, the field defect having a size and shape to be expected from the classical retinocortical maps (Holmes 1918). And so the question arises: can these disparate patterns of results be reconciled, or are humans and monkeys qualitatively different in this respect despite the similarity of their visual anatomy?

There are some serious difficulties that stand in the way of an answer. The first is topological: the striate cortex of the human is mainly buried in the medial surface in the calcarine fissure, whereas in the monkey the macular projection is on the lateral surface and readily accessible. Therefore, in the human brain, it is rare for any lesion of the striate cortex to occur without damage to overlying tissue, including visual association cortex, whereas it is relatively easy for lesions restricted to striate cortex to be studied in experimental animals. The difference is important for two reasons. First, the effect of enlarging a striate cortex lesion in the monkey so as to include posterior association cortex is reported to lead to a significant reduction in residual visual capacity (Pasik and Pasik 1971). Secondly, it is becoming clear that these closely adjoining more anterior cortical regions are functionally segregated and may have partially specialized capacities of a modular type, e.g. colour, movement, spatial features, form, etc.

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(cf. Cowey 1985; Zeki 1978, 1993). As at least some of these regions are likely to be damaged in the human whenever striate cortex is also damaged, the pattern of deficits can differ considerably from patient to patient with relatively slight differences in the disposition of the lesions. This means that comparisons between experimental striate lesions in monkey and clinically occurring lesions in the human are not typically comparisons of like with like and, moreover, there are inherent, but structurally sound, sources of variance in the clinical material. A further difference is that lesions to striate cortex in a clinical population will have variable histories of onset and subsequent course, or may even have been present prenatally. The classical animal studies were based largely on adolescent or mature animals with lesions that had an abrupt onset rather than a developmental history.

A second serious difficulty is methodological. Residual vision in the animal is, of course, studied by behavioural methods, typically by making reward contingent upon a particular response choice between alternative stimuli. For systematic studies of particular dimensions of discrimination, or even of detection per se, a long history of prior training and large series of trials are usually necessary. In contrast, human visual assessment is rarely carried out in such a fashion in the clinic. Instead, patients in clinical examination are asked to respond to a verbal instruction to report whether and what they ‘see’.

But when patients with field defects caused by occipital lesions are studied psychophysically with ‘animal-type’ forced-choice methodology—requiring them to make differential responses to the stimuli whether or not they verbally acknowledge ‘seeing’ them—unsuspected visual capacities may be uncovered that do not necessarily correlate with the patients’ reported experiences and that are often radically and surprisingly different. Good discriminative capacity was demonstrated some years ago in well-studied patients despite their claiming to have no visual experience whatever in their blind fields (Pöppel et al. 1973; Weiskrantz et al. 1974; cf. an early report by Bard 1905), giving rise to the term ‘blindsight’—visual discrimination in the absence of acknowledged awareness (Sanders et al. 1974; Weiskrantz.et al. 1974; Weiskrantz 1986). The history and some of the related background issues are also discussed more fully elsewhere (Weiskrantz 1972, 1980, 1986, 1998, 2001; Stoerig and Cowey 1997; Cowey and Stoerig 1991, 1992). ‘Blindsight’ originally applied only to human subjects, deriving from the contrast between human and animal results, but, as will be seen, the concept can now be applied both to humans and monkeys.

Categories of residual visual capacities

The evidence regarding blindsight capacities is necessarily based on a relatively small number of intensively studied subjects (the two most exhaustively studied being D.B. and G.Y.), as is often the case in neuropsychology, especially as lengthy testing psychophysical sessions are required. Taking the evidence collectively, not all necessarily found in all subjects, the findings are as follows.

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Localizing

Several subjects investigated by a number of investigators have demonstrated a capacity to localize stimuli within their ‘blind’ fields, either by making a saccade to the supposed locus of the stimulus, typically a briefly flashed spot (Pöppel et al. 1973), or by pointing or touching the locus of a target on a perimeter screen (Weiskrantz et al. 1974). In yet another study, G.Y. was trained to give a numerical score on a ruled scale to successfully describe the locus (Barbur et al. 1980). The accuracy is typically not as high as in the intact visual field, but nevertheless can be very impressive. Successful detection is obviously a necessary prerequisite for localization, but detection has also been studied independently of localizing (Barbur et al. 1980; Stoerig 1987; Stoerig et al. 1985; Stoerig and Pöppel 1986; Weiskrantz 1986; Azzopardi and Cowey 1997).

Acuity

There is not much systematic evidence, but D.B.’s acuity has been measured with Moirè fringe interference gratings (approximating to sine-wave gratings). The reduction in acuity for the region 16–20 eccentric is about 2 octaves as compared to the mirrorsymmetric region of the intact field (2.5 cycles/ compared with 10 cycles/ ; Weiskrantz 1986). G.Y.’s acuity has not been measured directly, but the contrast sensitivity function in his scotoma (using a grating of 12 12 , with its centre 9 from the fixation point) falls to zero at approximately 7 cycles/ , which also is approximately a drop of about 2 octaves compared to his intact field with this stimulus situation (Barbur et al. 1994a; Weiskrantz et al. 1998).

Orientation

D.B. is unusual in repeatedly demonstrating a good discriminative capacity for orientation in the frontal plane. Although impaired relative to his good field, he could nevertheless discriminate a difference in orientation of 10 between two gratings presented successively and briefly, even at an eccentricity of 45 in the impaired field, with no acknowledged experience of the gratings or even of a flash. Most other subjects who have been tested have shown rather less residual capacity for orientation (e.g. Barbur et al. 1980). G.Y. does not show orientation discrimination using gratings, but positive evidence has been obtained using single lines (Morland et al. 1996).

Colour

Initial evidence for wavelength discrimination in D.B. was at best marginal and slim, although he was not studied extensively (Weiskrantz et al. 1974, but recent unpublished evidence reveals substantial colour discrimination in him). The situation has been advanced considerably in more recent studies. Stoerig and Cowey (1989, 1991, 1992; Cowey and Stoerig 1999) measured the spectral sensitivity functions of the blind fields of a number of hemianopes and found them to be qualitatively normal, although with quantitatively reduced sensitivity. The spectral sensitivity profiles include the humps

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and troughs thought to reflect colour opponency. They also show the characteristic loss of long wavelength sensitivity following dark adaptation, the ‘Purkinje shift’. Moreover, wavelength discrimination, e.g. red versus green, but even of more closely spaced wavelengths, is possible in some subjects (Stoerig and Cowey 1992), using forced-choice guessing. Barbur et al. (1994b) demonstrated good discrimination between ‘coloured’ patches and achromatic patches matched in luminance, using a two-alternative forcedchoice paradigm in G.Y. Ruddock and his colleagues (Brent et al. 1994) have also found good discrimination between red and achromatic stimuli in G.Y. In this connection it would appear that the discriminative sensitivity of the blind field is biased towards the red end of the spectrum. Using pupillometry (see below) a strong inference can be made that successive colour contrast is intact in G.Y. and another hemianopic blindsight subject (Barbur et al. 1999, and recently confirmed in unpublished data with D.B. by Barbur and Weiskrantz).

It should be stressed that in all of these studies, the subjects never reported any experience of colour per se. Here is Stoerig and Cowey’s comment about the subjects’ commentaries in their spectral sensitivity study, which involved repeated measures of thresholds of chosen wavelengths, revealing qualitatively normal sensitivity functions:

. . . the patients were often asked whether they could perceive anything when the blind field was tested. Throughout the experiments, which involved from 2 to 4 three-hour sessions per month for approximately six months, they consistently claimed that this was not the case and that they never saw or felt anything that was related to stimulus presentation (1991, p. 1496).

Movement and transient stimuli

There are a number of reports of detection of moving stimuli by subjects in their impaired fields (Brindley et al. 1969; Barbur et al. 1980; Perenin 1978). The subject has long antecedents given the classical evidence of Riddoch (1917) and Poppelreuter (1917) who described gunshot-wound cases who reported seeing moving but not stationary stimuli. D.B. showed a good ability to detect moving targets, although with a reduced sensitivity depending on the location in the blind field (Weiskrantz 1986). A number of parametric psychophysical studies of directional discrimination of moving spots or bars have been carried out by Barbur and his colleagues on G.Y. (Barbur et al. 1993; Sahraie et al. 1997, 1998; Weiskrantz et al. 1995), measuring the limits of velocity and contrast for successful directional discrimination in the blind field. A clear capacity remains but with reduced sensitivity. It was some of these studies that led to the experimental exploration of the distinction between ‘awareness’ and ‘unawareness’ modes, and also to brain imaging (see below).

While there is no doubt that blindsight subjects can detect moving bars or spots and discriminate their direction of movement, other modes of movement discrimination, viz. the discrimination of direction of movement of random dot kineograms and plaids has been found lacking, at least in G.Y. (Azzopardi et al. 1998; Cowey and Azzopardi in press).

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Movement is, of course, one form of a transient stimulus. But it has been clear for some time that the transients exemplified by sharp temporal onset/offset of stationary stimuli are also of particular significance in the blind field. Weiskrantz et al. (1991) carried out a systematic study in G.Y. by varying the temporal slope of the Gaussian envelope of the onset and offset of stimuli in a two-alternative forced-choice paradigm for gratings versus homogeneous patches (of equal luminance). Performance improved as the temporal slope increased. In a related study, the manipulation of spatial as well as temporal transients also allowed a specification to be made of both the spatial and the temporal parameters required for good detection. This made it clear that, in G.Y., his blind field possesses a narrowly tuned spatiotemporal visual ‘channel’, with a peak of about 1 cycle/ and a cut-off (‘acuity’) of about 7 cycles/ (Barbur et al. 1994a). Subsequently, this has been linked to a closely similar channel in monkeys revealed by pupillometry (see below).

A somewhat different approach had been used in an early study of D.B. in which the temporal rate of onset was varied systematically over a wide range in a forced-choice discrimination between a circular, homogeneous luminous disc versus no stimulus. Although the sharper the rate of onset the better the performance, D.B. still performed reliably well above chance, and without acknowledged awareness, even with extremely slow rates of onset (Weiskrantz 1986, chapter 9). Hence, a rapid temporal transient is not a necessary feature for good detection. It also indicates that this mode of blindsight is quite different from the early reports by Riddoch (1917) of conscious reports of vigorous movement in the blind field. A similar point emerges from a pupillometric analysis (see below).

‘Form’

Most early reports of evidence for form discrimination have been negative, or weak (cf. Weiskrantz 1986). The situation may be different, however, if the subject is asked to reach for and grasp solid objects in his or her blind field. Both Marcel (1998) and

Perenin and Rossetti (1996) have reported that the subject’s hand adopts the appropriate arrangement for a shape in advance of grasping it when reaching for an object in the blind field. Such a result would be nicely in accord with the thesis forwarded by Milner and Goodale (1995) that the shape and orientation of objects can be involved in directed visual actions towards the objects even when subjects are unable to perceive the objects correctly.

On the other hand, Milner and Goodale’s distinction (between the ‘action’ mode and the ‘perception’ mode—linked by them to separate mediation by the dorsal and ventral visual streams) would not easily account for the striking claim by Marcel (1998) that words flashed into the blind field can influence the interpretation of meanings of words subsequently shown in the intact field. He reports, for example, that the word ‘money’ flashed into the blind field will bias the reported meaning of the ambiguous word ‘bank’ subsequently shown in the intact field—i.e. bank can either be related to

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‘money’ or to ‘river’. This intriguing report is isolated and deserves to be followed up. It would require a considerable expansion of the known capacity for residual processing of stationary shapes in the blind field.

Emotional content

There are claims that conditioned aversive properties of stimuli in normal human subjects can give rise to autonomic responses, even when the subjects have no awareness of them (Øhman and Soares 1998; Esteves et al. 1994). Moreover, functional imaging experiments have demonstrated that conditioned fear stimuli rendered invisible by backward masking can nevertheless activate the amygdala via a colliculopulvinar pathway (Morris et al. 1999, 2001; Breiter et al. 1996). This may or may not lead to an observable behavioural reaction. When a fear-evoking stimulus, such as a strange doll, is presented to the blind hemifield of a monkey with unilateral V1 removal, the animal appears to ignore it completely although it emits loud shrieks of fear and outrage when it is confronted in the normal visual field. Nor does the monkey react, for example, to a highly prized banana in the blind field (Cowey 1967; Cowey and Weiskrantz 1963). On the other hand, no concurrent measures of autonomic activity have been made, and it is possible that emotion-provoking stimuli would produce responses in the absence of overt behavioural responses, just as, for example, galvanic skin responses can be recorded to familiar faces in prosopagnosic patients who in perceptual tests cannot distinguish familiar from unfamiliar faces (Tranel and Damasio 1985).

A recent study of faces with emotional expression projected to G.Y.’s blind field has some direct bearing on this surmise (de Gelder et al. 1999). He has been shown to be able to discriminate between different facial expressions in moving video images projected into his blind field, e.g. happy versus sad and angry versus fearful, and he could also identify which of four different expressions were presented on any single exposure. He failed to ‘see’ the faces as such, and he was also at chance with inverted faces. It remains unknown so far whether his autonomic system would also be sensitive to those emotional stimuli that he can discriminate in the absence of ‘seeing’. A recent functional magnetic resonance imaging (fMRI) study using a conditioned-fear paradigm in G.Y. demonstrated that the amygdala is activated by the conditioned stimulus presented to the blind field, and that the amygdala activity correlates with activity levels in the superior colliculus and pulvinar. Thus, a route that bypasses V1 remains intact for activation by events provoking emotion.

Attention in the blind field

It has been demonstrated with G.Y. that attention can confer an advantage in processing stimuli in the blind field either within an attended time interval or at an attended spatial location. A visual cue that provides information about the time window within which the targets will appear in the blind field improves G.Y.’s discrimination of their location (Kentridge et al. 1999a). Cues in the blind field that provide information

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particular problems arise in terms of the subject’s confidence in making counterintuitive judgements about stimuli he or she cannot ‘see’, or in the commentaries that accompany their choices. In other areas of cognitive neuropsychology, residual function can be tested quite readily by methods that do not directly assault credibility. For example, the amnesic patient can be asked to try to identify a word when presented with its first three letters, to enable the experimenter to infer that an earlier ‘prime’ by the word has facilitated its identification, without requiring the subject to ‘remember’ as such.

There are two general approaches to indirect methods of testing for residual visual function that allow an inference without requiring the subject to guess ‘without seeing’: (1) reflexes to visual stimuli in the blind hemifield; (2) interactions between the intact and impaired hemifields. The field has been surveyed by Weiskrantz (1990) and Stoerig and Cowey (1997).

Reflexes

Electrodermal responses to visual stimuli in the blind field (as compared with control ‘blanks’) were used by Zihl et al. (1980) to demonstrate a positive response to light, but they are difficult to relate in a directly quantitative way to the visual events. Pupillometry, in contrast, provides a direct and incisive quantitative measure, given that the pupil constricts differentially in response to visual stimuli depending on their spatial frequency, wavelength, and movement, when there is no change in the total luminance of the stimuli (Barbur and Forsyth 1986; Barbur and Thomson 1987). In this way, the pupil can be used to measure the profile of sensitivity to gratings in the blind field as a function of spatial frequency, and also to obtain the visual acuity, and these have been validated by psychophysical comparisons of the same values. Sensitivity to colour and movement can also be measured. Given that pupillometry does not depend on the subject’s verbal report, it can be used to assess the blind fields of human patients, of animals, and also of human infants (cf. Cocker et al. 1994).

The method has been used (Weiskrantz et al. 1998) to examine the spatial frequency profiles of the affected hemifields of G.Y. and also of two monkeys with unilateral removal of striate cortex (V1), using the P_Scan apparatus (Barbur et al. 1987). The results are very clear (Fig. 9.3). In both the human and the monkeys there is a narrowly tuned response of the pupil to different spatial frequencies of an achromatic grating, with a peak at approximately 1 cycle/ . The acuity (the point at which the response falls to zero as spatial frequency increases) is at about 7 cycles/ , which is a reduction of about 2 octaves compared with the intact hemifields under these conditions. G.Y.’s pupillary response could be validated by psychophysical methods because a spatial temporal tuning curve was obtained in an earlier study (Barbur et al. 1994a). The psychophysical function and the pupillary profile map on to each other quite closely (see Fig. 9.3), and confirm the potential usefulness of pupillometry as a clinical screening device. Recently, it has been possible to make the same comparison for D.B. (Weiskrantz and Cowey, unpublished), with a similar close agreement between psychophysical and pupillometric determinations (Fig. 9.4).