|Larry Weiskrantz (2007), Scholarpedia, 2(4):3047.||doi:10.4249/scholarpedia.3047||revision #91068 [link to/cite this article]|
Blindsight is defined by the Oxford Concise Dictionary as "Medicine: a condition in which the sufferer responds to visual stimuli without consciously perceiving them," implicitly referring, of course, to human patients. The historical origins, however, stem from animal research and neuroanatomy. The primate retina, including that of humans, sends its major neural output (after a relay in the thalamus) to the visual cortex ("V1", "striate cortex"). When the striate cortex is removed or blocked in monkeys, the animals can still carry out visual discriminations although their capacity changes in certain ways. That they can still do so is perhaps not surprising because the output from the eye also reaches a number of other brain targets lying in the midbrain and thalamus that remain intact even when V1 is entirely removed (cf. review by Cowey and Stoerig, 1991). The surprise is that human subjects with loss of V1 claim they are blind.
History and the species difference
Blindsight grew out of efforts either to contrast or to unify the functions of visual cortex between monkey and humans. Historically the main emphasis over more than a century was on contrast, because animals' vision appears to survive the removal of visual cortex far better than that of humans. It took some time for the animal evidence to become clear because of uncertainties about the exact limits of primary visual cortex and also because observations were often based on gross observation rather than experimental tests. But in recent years it has become even more clear that monkeys without primary visual cortex can discriminate shapes, demonstrate contrast sensitivity functions over a range of spatial frequencies, have measurable acuity, although reduced from normal. In certain situations they appear to show a remarkable sensitivity to small and brief visual events, and will fixate them or reach for them; and they are very sensitive to detection of movement. In contrast, human subjects are phenomenally blind, although some early neurologists of World War I victims, e.g., Poppelreuter, Riddoch claimed that there could be some residual function, also supported by Teuber and colleagues studying World War II victims. But the prevailing consensus among neurologists has remained that summarized by William James in 1890, "The literature is tedious ad libitum......The occipital lobes are indispensable for vision in man. Hemiopic disturbance comes from lesion of either one of them, and total blindness, sensorial as well as psychic, from destruction of both." This striking apparent contrast between man and other animals gave rise to theories of a gradual drifting in the brain towards a cortical specialisation as the phylogenetic ladder is ascended, an "encephalisation of function,." which was really not much more than a restatement of the apparent species contrast (see review by Weiskrantz, 1961). In any case, given the preserved anatomical similarities, why should such a major species difference obtain?
Or does it? A move towards unity came when human subjects were tested in ways similar to animal tests, e.g., by having them reach out to touch briefly presented stimuli as developed by Humphrey (1974 with monkeys, or to move their eyes to their locus. The first study to measure eye movements was by Pöppel Held and Frost in 1973, based on evidence that midbrain pathways were implicated in the saccadic control, which survive visual cortex removal. Even though their subjects said they could not see the stimuli in their field defects, there was a significant, albeit weak correlation between stimulus locus and target eye position, at least out to 20 degrees eccentricity
The first and most intensively studied blindsight patient
Soon afterwards a patient, DB, at the National Hospital in London became the focus of study. DB's occipital cortex was removed surgically from his right hemisphere to ablate a benign tumour that had invaded it. The saccade findings of Pöppel et al were confirmed but the subject was then tested using "monkey-type" tests in which he had to reach out to locate a stimulus or to guess which of two alternative stimuli had been presented to him. The method of testing for visual capacity is usually deeply different in humans and in other animals. Humans are typically asked to give descriptions or to comment on visual appearances and differences, whereas animals are trained to make alternative choices for which they are usually rewarded, devoid of any commentary. Even when a human subject is asked to make a discrimination between, say, two wavelengths, he is usually explicitly instructed verbally as to what colour attribute he should be responding, and more importantly there is an important implicit assumption that he will be aware of that attribute, or will tell us if he is not. But what would obtain if the human subject is tested in a manner that is closer to animal methodology, being asked simply to make a forced-choice "guess" or choice between the visual stimuli whether or not he cannot "see" them, e.g., whether a visual event is located at A or B, or whether it is colour A or colour B, or falls in one temporal interval or a second temporal interval, or whether its shape, or colour, or brightness, are different in one or the other interval - in other words, tested in the same forced-choice discriminative way as animals are?
Good visual performance without awareness in DB
The result of using this methodology was that DB could succeed in a variety of discriminations by "guesswork" in his blind field, even though he said he did not "see" them. He could, for example, tell whether a grating was oriented in one or another direction, whether a stimulus was moving or stationary. His visual acuity could be measured by varying the spacing of a grating, with forced-choice guesses about whether there were "lines" or "no lines." While not absolutely normal, his ability to reach out and locate the position of stimuli in his blind field was remarkably good. In fact, his ability matched reasonably well that of monkeys without primary visual cortex. The most remarkable feature undoubtedly was the high level of visual proficiency in making discriminations in the absence of acknowledged awareness by him. He was astonished when shown his results, as were Weiskrantz and Warrington when conducting the tests that demonstrated his impressive performance without awareness. DB remained convinced that he was simply guessing and was at chance. These first results, by Weiskrantz and coworkers, were published in Brain in 1974. It was the first account of a hemianopic subject's performance over a wide range of visual tasks combined with his parallel "commentaries" about them. In later research the pattern was formalized by the addition of "commentary response keys" as well as "discrimination response keys."
The oxymoron "blindsight" was generated as a result of Weiskrantz having to respond urgently to produce a title for a seminar he was invited to give to Oxford neurologists, and under this pressure he spontaneously came up with "Blindsight and Hindsight" - "blindsight" to describe the striking behavioural results and "hindsight" to suggest an implication of the midbrain visual pathways for its mediation. The term first appeared in print in a short article in Lancet in 1974 (Sanders et al., 1974) describing the phenomenon of visual function in a field defect. The term stuck - so much so that it eventually appeared in standard dictionaries.
DB and others
DB continued to be the subject of sustained study over ten years by Weiskrantz in collaboration with Warrington, resulting in a book "Blindsight" in 1986, with a second edition in 1998, in which DB's capacity to detect, to discriminate orientation, movement, form, under a variety of conditions was studied and their possible implications considered.. It early became apparent, also, that rapid transient events, e.g., rapid movement or sudden onset/offsets, produced a "feeling" or "knowing" that some event had occurred even though it was not "seen". This was dubbed Blindsight Type 2 in contrast to the situation in which there was absolutely no reported experience, Type 1.
DB later returned as a focus of interest and a number of follow-up studies appeared well into 2007 (Weiskrantz et al., 2002; Trevethan et al.,.in press). The basic phenomenon of "unconscious" visual capacity remains, although his sensitivity has improved markedly. Other subjects, e.g., GY, also have been studied by workers in several countries. More recently it has become clear that the phenomenon is not rare. Sahraie et al. (2003) have studied a large population of patients with relatively restricted visual cortical damage and residual function was been found in the large majority.
Varieties of blindsight
Types of visual attributes that can be discriminated by blindsight subjects in the absence of their experience of the stimuli include colour, different orientation of lines or gratings, simple shapes, motion, onset and termination of visual events. Interestingly, the emotional expression of unseen faces in the blind field can be "guessed" at better than chance levels. There are, however, changes in relation to normal vision. The subjects= acuity is reduced, relative to their normal seeing fields, but is still creditable. Motion perception is retained for simple displacement of a bar or a spot, but more complex motion patterns ("third order motion") seem to be seriously affected. Good colour discrimination remains (again, in the absence of any experience of colour per se,) but there is a shift towards a relative increase in sensitivity of long wave-lengths (red) and a decrease of middle wave-lengths (green). Otherwise the spectral sensitivity curve, and its change under dark adaptation, is relatively normal. The optimal stimuli for blindsight subjects lie in the low range of spatial frequencies (1 to 3 cycles/degree) combined with temporal oscillation in the range of 5-33 Hz (cf Sahraie et al., 2003). Emotional stimuli can also be discriminated by blindsight subjects, without awareness, and the amygdala is activated by fearful stimuli (DeGelder et al., 2001, 2002; Morris et al., 2001; Pegna et al., 2004)
Learning from the pupil
Because the difficulty and resistance that a subject may have in being asked to discriminate something they cannot see, other methods of assessing residual function have been developed, useful for screening of brain-damaged subjects for possible rehabilitation (cf. review by Weiskrantz, 1990). Some of these methods depend upon asking the subject to discriminating stimuli lying entirely in their intact, seeing hemifields, but demonstrating that their performance can be altered by the presentation of stimuli in their blind fields, which may enhance or interfere. By far the most quantitatively sensitive method depends upon changes in the diameter of the pupil, which constricts not only to increase in light energy, but to a wide variety of stimuli without any energy change (Barbur and Forsyth, 1986). These include sine-wave gratings, movement, and colour. The acuity of the blind field can be accurately measured by pupillometry, as well the sensitivity to colour and colour after-images, which appear to mirror the blindsight capacity as measured by forced-choice guessing. The pupil can also be used to measure capacities in animals, where verbal report of course is impossible, with concordant findings) between human and monkey hemianopes (Weiskrantz et al., 1998).
Wider interest and developments
The phenomenon of visual capacity in the absence of acknowledged awareness became of interest to neuroscientists pursuing the burgeoning topic of consciousness and its possible neural basis. A number of neuro-imaging studies of blindsight have been carried out, including diffusion studies directly implicating the superior colliculus (in the "hindbrain") as a likely route mediating the unconscious capacity. It also has became a topic of keen interest to philosophers because of its implications across a broad front in the philosophy of mind, for example its possible relevance to theories of higher-order-thought in relation to consciousness (Rosenthal, 1993).
With the methods of TMS (transient magnetic stimulation), it has proved possible to simulate blindsight in normal observers by temporarily disrupting visual cortical electrical activity (Ro et al., 2004), and in some cases to combine the TMS effects with neuro-imaging, as in the work of Lau.. An important possible closure has arisen from the studies by Cowey and Stoerig (1995, 1997); Stoerig and Cowey (1997) of unilateral visual cortex ablations that suggest that these animals also have blindsight akin to the human phenomenon. The monkeys show excellent sensitivity to visual events in their "blind" fields, but judge them to be "blanks" when given a choice to do so. Also,, the early animal work by Cowey (1967), Cowey and Weiskrantz, 1963), Weiskrantz and Cowey (1970) showing gradual improvement with training, with shrinkage of the field defects, is being actively pursued in human studies with positive outcomes (Sahraie et al., 2006). The phenomenon is not restricted to vision. "Blind touch" or "numbsense" has been reported with lesions of somatosensory sensitivity (Rossetti et al., 1995), as well as "deaf hearing" (Michel and Peronnet (19800, Mozaz-Garde and Cowey, 2000). Indeed, across the entire broad spectrum of neuropsychological syndromes, unconscious residual function has been found in amnesia, neglect, dyslexia, aphasia, and agnosia (cf. review by Weiskrantz, 1997). Blindsight is by means an isolated neurological condition.
Beyond the baptism of fire
As is often the case with novel, counter-intuitive phenomena in science, blindsight studies were early the focus of intense sceptical attack, with dismissive suggestions, for example, that the findings may have been artifactually generated by stray light reaching the normal visual field Also, it was suggested they really did see but were reluctant to acknowledge it, such that in signal detection terms that they had a significant d' but a strongly biassed criterion (cf. Campion et al., 1983) or that the visual cortex damage may have been incomplete giving rise to scattered islands of intact function (Fendrich et al., 1992). All of these serious questions have been directly addressed and the phenomenon remains intact (cf. summary in Weiskrantz, 1998, also Cowey, 2004). Indeed, as in other cases in the history of science, after its successful baptism of fire, the result has been that others have retrospectively tried to take personal credit for the discovery while others's very important contributions, e.g., Elizabeth Warrington's, have been overlooked, or it has been suggested, not inaccurately, that all offspring have a long period of gestation.
And, of course, no "discovery" is the work of one person or team. It is built upon a background of a large body of evidence accumulated over decades, with openings from both the animal and the early neuropathological evidence from war victims, augmented and consolidated by the happy attachment of the blindsight label and the "commentary key."
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