- Email: [email protected]
Insights into blindsight
Milner – Insights into blindsight
Update Meetings
Insights into blindsight Toward a science of consciousness (Tucson III): 27 April – 2 May 1998, Tucson, Arizona, USA.
One of the highlights of the third meeting of ‘Toward a Science of Consciousness’ was the plenary session on blindsight. The definition of the term ‘blindsight’ remains, some 25 years after its coinage by Larry Weiskrantz, controversial. In the general view, it refers to any residual visual function, unaccompanied by visual awareness, that can be observed in patients who have suffered major (usually hemianopic) field defects following damage to the striate cortex (V1) or to the optic radiations (which connect the lateral geniculate nucleus to the cortex). Despite the controversy, the term seems destined to stick, and to survive the recent attempt by Zeki and ffytche1 to introduce the (arguably more respectable) Greek-derived term ‘agnosopsia’ to refer to such phenomena of vision without awareness. The two presentations in the plenary session at Tucson were given by Petra Stoerig (with co-authors A. Cowey and R. Goebel) and by Robert Kentridge (with co-authors C.A. Heywood and L. Weiskrantz). Stoerig first reviewed briefly the evidence for blindsight in humans and monkey subjects, and described how increasingly careful studies have been done to control for the possible artefacts that critics have identified over the years. She then went on to present new neuroimaging data that revealed an intriguing pattern of activation in the occipito-temporal regions of the cerebral cortex of three hemianopic patients when they viewed complex visual stimuli in the ‘blind’ hemifield. The activated areas included those that have been designated V4 and LO, which may be regarded as likely homologues of areas V4 and TEO in the monkey’s ‘ventral stream’. The stimuli consisted of coloured drawings of natural objects, such as fruit. Importantly, there was no activation in the damaged or deafferented area V1 on the lesioned side of the brain, even when reversing checkerboard patterns (a powerful stimulus to striate cortex) were presented. In separate observations, the investigators also found activation of the motion complex (including MT/V5) ipsilateral to the lesion, in response to spiral checkerboard motion. The reported activation of the motion complex, which forms a part of the ‘dorsal stream’ of cortical visual areas, replicates a previous neuroimaging study of a blindsight patient2. It is reasonable to assume that the activation comes about via the second major visual route from the eye to the brain, which passes through the superior colliculus in the midbrain and pulvinar nucleus of the thalamus. The activation of
areas within the occipito-temporal ‘ventral stream’ however, has not been previously reported in hemianopic subjects, and is surprising in the light of animal research. This work has shown that (at least in anaesthetized monkeys) neurones in the ventral stream lose their responsiveness to visual stimuli when area V1 is removed, or deactivated through cooling, although neurones in the dorsal stream (e.g. in area MT) remain active3,4. There are several possible interpretations of these new results, each of which should lead to even more interesting experiments. For example, it could be that the ventral-stream activation comes about through pathways that convey colour information to the cortex through extrastriate routes. Cowey and Stoerig (e.g. Ref. 5) have shown in several studies that ‘colour blindsight’ can occur, and indeed have argued that this phenomenon might be mediated by neurones surviving in the LGN which could carry information directly to extrastriate visual areas such as V2 and V4, bypassing the striate cortex. This route could be more fully elucidated by carrying out further neuroimaging studies with hemianopic patients in which colour variations in an abstract pattern are contrasted with luminance variations only6, or in which coloured line drawings are contrasted with achromatic line drawings. A second possibility is that the activation seen in response to the drawings reflects form processing, or at least the processing of object contours, in the absence of striate cortex (any apparent blindsight for form is probably reducible to blindsight for line orientation and perhaps other elementary attributes like line length; see Ref. 7). However, work by Perenin and Rossetti8 suggests that, as with motion processing, such contour processing is dependent upon dorsal-stream systems rather than ventral ones in hemianopic patients. These authors reported that their hemianopic patient was able to carry out visually guided motor acts (rotating the wrist to post a card, or opening the hand to grasp a block) in response to stimuli in the blind field, but was not able to report them verbally or manually. They interpret their data in the light of the model of Milner and Goodale9 in which the dorsal stream is seen as primarily dedicated to the visual control of action. Milner and Goodale suggested that where blindsight for contour was demonstrated, it might be the result of the activation of such visuomotor systems. They took a similar line in explaining blindsight for location and motion (e.g. in terms of incipient eye movement control), while
accepting Cowey and Stoerig’s evidence for the involvement of ventralstream areas in colour blindsight. The third and perhaps most intriguing possibility for explaining the ventral-stream activation found by Stoerig and colleagues was raised by a questioner from the floor at the plenary session. No doubt inspired by an earlier presentation by Richard Gregory, this questioner asked whether the ventral-stream activation might be generated by a top-down process, in which the person tries to make sense of the absent or rudimentary information available from the ‘blind’ field by constructing perceptual ‘hypotheses’. This idea could be tested in a number of ways. For example, it might be predicted that even when no blindsight for contour was present in a hemianopic patient (perhaps even when the blindness is caused by ocular or peripheral optic pathway damage, such that no visual information can reach the brain at all), one might still be able to record activity in the occipito-temporal region if the person is led to expect shapes in the blind field. The other presentation, by Bob Kentridge, was equally thoughtprovoking. It included work that tells against the recent idea by Fendrich and colleagues10 that apparent blindsight might be attributable to preserved islands of intact cortex within area V1. The work of Kentridge and colleagues11 shows that in at least one well-studied patient (GY), there is no patchiness of blindsight across the hemianopic field as would be expected if there were such preserved cortical islands. They failed to find any such variation even when eye movements were minimized by various means and monitored by a dual Purkinje-image eyetracker11. Kentridge went on to describe more recent studies in which GY’s ability to attend selectively within his hemianopic field was examined. This question touches on one of the most basic issues in modern research into consciousness – namely, what is the relationship between attention and consciousness, and can the two be dissociated? Milner and Goodale9 summarized physiological evidence that the gating processes correlated with selective attention are widely distributed among the cortical areas subserving visual processing, and in particular that these processes can be seen within both the dorsal and ventral streams. More recent research has strengthened this conclusion. Milner and Goodale also proposed that the conscious experience that (generally) goes with visual perception receives its contents via the
Copyright © 1998, Elsevier Science Ltd. All rights reserved. 1364-6613/98/$19.00
PII: S1364-6613(98)01185-1
Trends in Cognitive Sciences – Vol. 2, No. 7,
July 1998
237
Update
Milner – Insights into blindsight
Meetings ventral stream, whereas the visuomotor control mediated by the dorsal stream proceeds without directly influencing or requiring visual awareness. They went on to make the inference that attentional processes can operate either to select for action or to select for perception, and that only in the latter case would they be closely correlated with awareness. Kentridge reported data that are consistent with these ideas. Using variations of the Posner cueing paradigm, he and his colleagues have found highly convincing evidence that GY can direct his visuospatial attention within his hemianopic field. For example, GY showed much faster reaction times to targets at a location that was validly cued by a central symbolic prime, than to target locations that were invalidly cued. Thus, GY seems to be well able to distribute his attention differentially within his ‘blind’ field. Furthermore, the authors went on to show that GY was even responsive to attentional cues placed in his hemianopic field itself: in other words his attention could be directed by cues that he could not see to targets that he could not see! Admittedly, however, the use of a brighter attentional cue (for which GY usually reports some kind of indefinable sensation) did yield larger attentional effects. Moreover, when asked to use a cue at one of two locations in his blind field to direct his attention to the other
location, GY succeeded only when the brighter cues were used. Kentridge inferred from this that the voluntary use of cues to direct attention might require conscious processing of the cue, while more automatic orienting of attention might not. Where does this new burst of blindsight research take us? I believe it marks at last a move away from the somewhat sterile debates over the reality of blindsight, into more interesting realms of investigation, in which the fact of blindsight allows us to ask important new questions about the neural and psychological correlates of visual awareness. If this optimism is justified, then the second 25 years of blindsight research promise to build on the first 25 years in some profoundly exciting ways.
3 Gross, C.G. (1991) Contribution of striate
David Milner
8 Perenin, M.T. and Rossetti, Y. (1996) Grasping
cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and inferior temporal cortex Neuropsychologia 29, 497–515 4 Bullier, J., Girard, P. and Salin, P-A. (1994) The role of area 17 in the transfer of information to extrastriate visual cortex, in Cerebral Cortex, Vol. 10: Primary Visual Cortex in Primates (Peters, A. and Rockland, K.S., eds), pp. 301–330, Plenum Press 5 Cowey, A. and Stoerig, P. (1992) Reflections on blindsight, in The Neuropsychology of Consciousness (Milner, A.D. and Rugg, M.D., eds), pp. 11–38, Academic Press 6 Zeki, S. et al. (1991) A direct demonstration of functional specialization in human visual cortex J. Neurosci. 11, 641–649 7 Weiskrantz, L. (1987) Residual vision in a scotoma: a follow-up study of ‘form’ discrim ination Brain 110, 77–92
School of Psychology, University of St Andrews,
without form discrimination in a hemianopic field NeuroReport 7, 793–797
Fife, UK KY16 9JU.
9 Milner, A.D. and Goodale, M.A. (1995) The
tel: +44 1334 462065
Visual Brain in Action, Oxford University Press
fax: +44 1334 463042
10 Fendrich, R., Wessinger, C.M. and Gazzaniga,
e-mail: [email protected]
M.S. (1992) Residual vision in a scotoma: implications
References 1 Zeki, S. and ffytche, D.H. (1998) The Riddoch
1489–1491
syndrome: insights into the neurobiology of
11 Kentridge,
2 Barbur, J.L. et al. (1993) Conscious visual without
V1
Brain
blindsight
R.W.,
Science
Heywood,
258,
C.A.
and
Weiskrantz, L. (1997) Residual vision in
conscious vision Brain 121, 25–45 perception
for
116,
1293–1302
multiple retinal locations within a scotoma: implications for blindsight J. Cogn. Neurosci. 9, 191–202
Monitor
Summaries of recently published papers of interest to cognitive scientists. Readers who would like to contribute to this section, by identifying appropriate papers and writing short summaries, should contact the Editor.
Faces, trust and the amygdala Extensive animal studies have demonstrated that the amygdala is involved in emotional and social functions with emphasis on fear and aggression in particular1. In humans the neuropsychological and functional neuroimaging evidence indicates that this structure plays a role in the recognition of emotional facial expressions2. Adolphs, Tranel and Damasio now provide evidence that the human amygdala is involved in human social judgments that are based upon facial appearance3. Three subjects with complete bilateral damage to the amygdala were asked to look at a series of 100 pictures of unfamiliar faces. The task was to judge from the appearance of
238
the pictures whether the individuals depicted were approachable and trustworthy. The results demonstrated that the patients with bilateral damage to the amygdala judged unfamiliar faces to be more approachable and trustworthy than did brain-damaged control subjects. (Subjects with unilateral damage to the amygdala did not differ from controls.) Moreover, this impairment in social judgment was most obvious for those faces that the control group rated the most unapproachable and untrustworthy individuals. Indeed, the subjects with bilateral amygdala damage were not impaired when rating the 50 most positively rated faces. Interestingly, this impairment in
Copyright © 1998, Elsevier Science Ltd. All rights reserved. 1364-6613/98/$19.00 Trends in Cognitive Sciences – Vol. 2, No. 7,
July 1998
social judgment did not extend to judgments based on written or verbal descriptions of individuals. The authors contend that these data suggest that the amygdala appears to be necessary for the retrieval of information, particularly in response to visual stimuli, on the basis of prior social experience or an innate bias with respect to certain classes of face. Future research will be required to elaborate upon these findings to determine whether the role of the amygdala in social judgment of faces is based upon innate or acquired information. References 1 Kling, A.S. and Brothers, L.A. (1992) in The Amygdala:
Neurobiological
Aspects
of
Emotion, Memory and Mental Dysfunction (Aggleton, J.P., ed.), pp. 353–378, John Wiley & Sons 2 Adolphs, R. Tranel, D., Damasio, H. and Damasio, A. (1994) Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala Nature 372, 669–672 3 Adolphs, R., Tranel, D. and Damasio, A.R. (1998)
The
human
amygdala
judgment Nature 393, 470–474
in
social
Update Meetings
Insights into blindsight Toward a science of consciousness (Tucson III): 27 April – 2 May 1998, Tucson, Arizona, USA.
One of the highlights of the third meeting of ‘Toward a Science of Consciousness’ was the plenary session on blindsight. The definition of the term ‘blindsight’ remains, some 25 years after its coinage by Larry Weiskrantz, controversial. In the general view, it refers to any residual visual function, unaccompanied by visual awareness, that can be observed in patients who have suffered major (usually hemianopic) field defects following damage to the striate cortex (V1) or to the optic radiations (which connect the lateral geniculate nucleus to the cortex). Despite the controversy, the term seems destined to stick, and to survive the recent attempt by Zeki and ffytche1 to introduce the (arguably more respectable) Greek-derived term ‘agnosopsia’ to refer to such phenomena of vision without awareness. The two presentations in the plenary session at Tucson were given by Petra Stoerig (with co-authors A. Cowey and R. Goebel) and by Robert Kentridge (with co-authors C.A. Heywood and L. Weiskrantz). Stoerig first reviewed briefly the evidence for blindsight in humans and monkey subjects, and described how increasingly careful studies have been done to control for the possible artefacts that critics have identified over the years. She then went on to present new neuroimaging data that revealed an intriguing pattern of activation in the occipito-temporal regions of the cerebral cortex of three hemianopic patients when they viewed complex visual stimuli in the ‘blind’ hemifield. The activated areas included those that have been designated V4 and LO, which may be regarded as likely homologues of areas V4 and TEO in the monkey’s ‘ventral stream’. The stimuli consisted of coloured drawings of natural objects, such as fruit. Importantly, there was no activation in the damaged or deafferented area V1 on the lesioned side of the brain, even when reversing checkerboard patterns (a powerful stimulus to striate cortex) were presented. In separate observations, the investigators also found activation of the motion complex (including MT/V5) ipsilateral to the lesion, in response to spiral checkerboard motion. The reported activation of the motion complex, which forms a part of the ‘dorsal stream’ of cortical visual areas, replicates a previous neuroimaging study of a blindsight patient2. It is reasonable to assume that the activation comes about via the second major visual route from the eye to the brain, which passes through the superior colliculus in the midbrain and pulvinar nucleus of the thalamus. The activation of
areas within the occipito-temporal ‘ventral stream’ however, has not been previously reported in hemianopic subjects, and is surprising in the light of animal research. This work has shown that (at least in anaesthetized monkeys) neurones in the ventral stream lose their responsiveness to visual stimuli when area V1 is removed, or deactivated through cooling, although neurones in the dorsal stream (e.g. in area MT) remain active3,4. There are several possible interpretations of these new results, each of which should lead to even more interesting experiments. For example, it could be that the ventral-stream activation comes about through pathways that convey colour information to the cortex through extrastriate routes. Cowey and Stoerig (e.g. Ref. 5) have shown in several studies that ‘colour blindsight’ can occur, and indeed have argued that this phenomenon might be mediated by neurones surviving in the LGN which could carry information directly to extrastriate visual areas such as V2 and V4, bypassing the striate cortex. This route could be more fully elucidated by carrying out further neuroimaging studies with hemianopic patients in which colour variations in an abstract pattern are contrasted with luminance variations only6, or in which coloured line drawings are contrasted with achromatic line drawings. A second possibility is that the activation seen in response to the drawings reflects form processing, or at least the processing of object contours, in the absence of striate cortex (any apparent blindsight for form is probably reducible to blindsight for line orientation and perhaps other elementary attributes like line length; see Ref. 7). However, work by Perenin and Rossetti8 suggests that, as with motion processing, such contour processing is dependent upon dorsal-stream systems rather than ventral ones in hemianopic patients. These authors reported that their hemianopic patient was able to carry out visually guided motor acts (rotating the wrist to post a card, or opening the hand to grasp a block) in response to stimuli in the blind field, but was not able to report them verbally or manually. They interpret their data in the light of the model of Milner and Goodale9 in which the dorsal stream is seen as primarily dedicated to the visual control of action. Milner and Goodale suggested that where blindsight for contour was demonstrated, it might be the result of the activation of such visuomotor systems. They took a similar line in explaining blindsight for location and motion (e.g. in terms of incipient eye movement control), while
accepting Cowey and Stoerig’s evidence for the involvement of ventralstream areas in colour blindsight. The third and perhaps most intriguing possibility for explaining the ventral-stream activation found by Stoerig and colleagues was raised by a questioner from the floor at the plenary session. No doubt inspired by an earlier presentation by Richard Gregory, this questioner asked whether the ventral-stream activation might be generated by a top-down process, in which the person tries to make sense of the absent or rudimentary information available from the ‘blind’ field by constructing perceptual ‘hypotheses’. This idea could be tested in a number of ways. For example, it might be predicted that even when no blindsight for contour was present in a hemianopic patient (perhaps even when the blindness is caused by ocular or peripheral optic pathway damage, such that no visual information can reach the brain at all), one might still be able to record activity in the occipito-temporal region if the person is led to expect shapes in the blind field. The other presentation, by Bob Kentridge, was equally thoughtprovoking. It included work that tells against the recent idea by Fendrich and colleagues10 that apparent blindsight might be attributable to preserved islands of intact cortex within area V1. The work of Kentridge and colleagues11 shows that in at least one well-studied patient (GY), there is no patchiness of blindsight across the hemianopic field as would be expected if there were such preserved cortical islands. They failed to find any such variation even when eye movements were minimized by various means and monitored by a dual Purkinje-image eyetracker11. Kentridge went on to describe more recent studies in which GY’s ability to attend selectively within his hemianopic field was examined. This question touches on one of the most basic issues in modern research into consciousness – namely, what is the relationship between attention and consciousness, and can the two be dissociated? Milner and Goodale9 summarized physiological evidence that the gating processes correlated with selective attention are widely distributed among the cortical areas subserving visual processing, and in particular that these processes can be seen within both the dorsal and ventral streams. More recent research has strengthened this conclusion. Milner and Goodale also proposed that the conscious experience that (generally) goes with visual perception receives its contents via the
Copyright © 1998, Elsevier Science Ltd. All rights reserved. 1364-6613/98/$19.00
PII: S1364-6613(98)01185-1
Trends in Cognitive Sciences – Vol. 2, No. 7,
July 1998
237
Update
Milner – Insights into blindsight
Meetings ventral stream, whereas the visuomotor control mediated by the dorsal stream proceeds without directly influencing or requiring visual awareness. They went on to make the inference that attentional processes can operate either to select for action or to select for perception, and that only in the latter case would they be closely correlated with awareness. Kentridge reported data that are consistent with these ideas. Using variations of the Posner cueing paradigm, he and his colleagues have found highly convincing evidence that GY can direct his visuospatial attention within his hemianopic field. For example, GY showed much faster reaction times to targets at a location that was validly cued by a central symbolic prime, than to target locations that were invalidly cued. Thus, GY seems to be well able to distribute his attention differentially within his ‘blind’ field. Furthermore, the authors went on to show that GY was even responsive to attentional cues placed in his hemianopic field itself: in other words his attention could be directed by cues that he could not see to targets that he could not see! Admittedly, however, the use of a brighter attentional cue (for which GY usually reports some kind of indefinable sensation) did yield larger attentional effects. Moreover, when asked to use a cue at one of two locations in his blind field to direct his attention to the other
location, GY succeeded only when the brighter cues were used. Kentridge inferred from this that the voluntary use of cues to direct attention might require conscious processing of the cue, while more automatic orienting of attention might not. Where does this new burst of blindsight research take us? I believe it marks at last a move away from the somewhat sterile debates over the reality of blindsight, into more interesting realms of investigation, in which the fact of blindsight allows us to ask important new questions about the neural and psychological correlates of visual awareness. If this optimism is justified, then the second 25 years of blindsight research promise to build on the first 25 years in some profoundly exciting ways.
3 Gross, C.G. (1991) Contribution of striate
David Milner
8 Perenin, M.T. and Rossetti, Y. (1996) Grasping
cortex and the superior colliculus to visual function in area MT, the superior temporal polysensory area and inferior temporal cortex Neuropsychologia 29, 497–515 4 Bullier, J., Girard, P. and Salin, P-A. (1994) The role of area 17 in the transfer of information to extrastriate visual cortex, in Cerebral Cortex, Vol. 10: Primary Visual Cortex in Primates (Peters, A. and Rockland, K.S., eds), pp. 301–330, Plenum Press 5 Cowey, A. and Stoerig, P. (1992) Reflections on blindsight, in The Neuropsychology of Consciousness (Milner, A.D. and Rugg, M.D., eds), pp. 11–38, Academic Press 6 Zeki, S. et al. (1991) A direct demonstration of functional specialization in human visual cortex J. Neurosci. 11, 641–649 7 Weiskrantz, L. (1987) Residual vision in a scotoma: a follow-up study of ‘form’ discrim ination Brain 110, 77–92
School of Psychology, University of St Andrews,
without form discrimination in a hemianopic field NeuroReport 7, 793–797
Fife, UK KY16 9JU.
9 Milner, A.D. and Goodale, M.A. (1995) The
tel: +44 1334 462065
Visual Brain in Action, Oxford University Press
fax: +44 1334 463042
10 Fendrich, R., Wessinger, C.M. and Gazzaniga,
e-mail: [email protected]
M.S. (1992) Residual vision in a scotoma: implications
References 1 Zeki, S. and ffytche, D.H. (1998) The Riddoch
1489–1491
syndrome: insights into the neurobiology of
11 Kentridge,
2 Barbur, J.L. et al. (1993) Conscious visual without
V1
Brain
blindsight
R.W.,
Science
Heywood,
258,
C.A.
and
Weiskrantz, L. (1997) Residual vision in
conscious vision Brain 121, 25–45 perception
for
116,
1293–1302
multiple retinal locations within a scotoma: implications for blindsight J. Cogn. Neurosci. 9, 191–202
Monitor
Summaries of recently published papers of interest to cognitive scientists. Readers who would like to contribute to this section, by identifying appropriate papers and writing short summaries, should contact the Editor.
Faces, trust and the amygdala Extensive animal studies have demonstrated that the amygdala is involved in emotional and social functions with emphasis on fear and aggression in particular1. In humans the neuropsychological and functional neuroimaging evidence indicates that this structure plays a role in the recognition of emotional facial expressions2. Adolphs, Tranel and Damasio now provide evidence that the human amygdala is involved in human social judgments that are based upon facial appearance3. Three subjects with complete bilateral damage to the amygdala were asked to look at a series of 100 pictures of unfamiliar faces. The task was to judge from the appearance of
238
the pictures whether the individuals depicted were approachable and trustworthy. The results demonstrated that the patients with bilateral damage to the amygdala judged unfamiliar faces to be more approachable and trustworthy than did brain-damaged control subjects. (Subjects with unilateral damage to the amygdala did not differ from controls.) Moreover, this impairment in social judgment was most obvious for those faces that the control group rated the most unapproachable and untrustworthy individuals. Indeed, the subjects with bilateral amygdala damage were not impaired when rating the 50 most positively rated faces. Interestingly, this impairment in
Copyright © 1998, Elsevier Science Ltd. All rights reserved. 1364-6613/98/$19.00 Trends in Cognitive Sciences – Vol. 2, No. 7,
July 1998
social judgment did not extend to judgments based on written or verbal descriptions of individuals. The authors contend that these data suggest that the amygdala appears to be necessary for the retrieval of information, particularly in response to visual stimuli, on the basis of prior social experience or an innate bias with respect to certain classes of face. Future research will be required to elaborate upon these findings to determine whether the role of the amygdala in social judgment of faces is based upon innate or acquired information. References 1 Kling, A.S. and Brothers, L.A. (1992) in The Amygdala:
Neurobiological
Aspects
of
Emotion, Memory and Mental Dysfunction (Aggleton, J.P., ed.), pp. 353–378, John Wiley & Sons 2 Adolphs, R. Tranel, D., Damasio, H. and Damasio, A. (1994) Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala Nature 372, 669–672 3 Adolphs, R., Tranel, D. and Damasio, A.R. (1998)
The
human
amygdala
judgment Nature 393, 470–474
in
social