Brain, Vol. 126, No. 2, 265-266,
February 2003
© 2003 Guarantors of Brain
doi: 10.1093/brain/awg023
Editorial |
Mind—the gap, after 65 years: visual conditioning in cortical blindness
1 Department of Experimental Psychology, University of Oxford, UK
In the 1937 issue of Brain, an article appeared by Donald Marquis and Ernest Hilgard on the effects of total (and histologically confirmed) bilateral removal of striate cortex in six monkeys: ‘... The monkey seemed completely blind ... The threat reflex was permanently abolished and no evidence of object vision was ever seen in any of the animals’ (p. 4) (Marquis and Hilgard, 1937
). The methodology of classical conditioning of the eyelid response in animals and humans was already well developed by that time. In this paradigm a light signal serves as the conditioned stimulus for the unconditioned blast of air to the eyeball, and in association elicits a closure of the eyelid. These authors realised that, notwithstanding the apparent blindness, it could provide objective, quantitative evidence as to whether there was a residual sensitivity to light in the absence of visual cortex in the monkey. They had already applied the method to the same question in other species (for historical review see Weiskrantz, 1961). Here was the outcome: ‘The results of the conditioning experiments stand in clear contrast to the seemingly complete object blindness of the monkey after removal of both occipital lobes. Conditioned responses to light were established in three monkeys after bilateral operation. Their characteristics may be directly compared with conditioned responses of four unoperated normal monkeys ... With the exception of a slight increase in latency of the response no difference could be detected’ (p. 6). ‘The similarity of the conditioned responses in normal and operated monkeys provides evidence that the visual cortex is not an essential part of the neural mechanism for responses to light stimuli. This is further supported by the demonstrated possibility of retention of a conditioned response established prior to operation’ (p.11).
Some 65 years later, the paper by Hamm et al. (2003) in this issue provides a demonstration of the successful establishment of classical conditioning to a visual stimulus in a human subject with bilateral loss of striate cortex. Like the monkey, the human subject was completely blind (both behaviourally and experientially) but, nevertheless, showed good evidence of intact visual function when a visual stimulus (an outline drawing of an airplane) served as a conditioned stimulus—in this case in association with a rather more severe unconditioned stimulus (electric shock) than the milder aversive air blast to the eye used with the monkeys.
Why has it taken 65 years for the gap between these studies of two primates to be closed? One reason is that Marquis and Hilgard, in keeping with prevailing view at the time, severely cautioned against ‘interpreting human cerebral function on the basis of animal experiments’, but without providing human evidence. Today the comparative parallels are more evident (Stoerig and Cowey, 1997). A practical reason is that clinical bilateral cortical blindness without disruptive additional deficits is relatively rare. Blindsight in hemianopic subjects has been extensively studied, but without a classical conditioning paradigm for its establishment. In fact, it has been unnecessary because the use of two-alternative forced-choice ‘guessing’ methodology has demonstrated a range of visual capacities without the need for a deliberate injection of an aversive unconditioned stimulus (Weiskrantz, 1986; Stoerig and Cowey, 1992). But bilateral cases have special interest because it is possible in hemianopia that the intact visual cortex may indirectly play a role even when stimuli are wholly confined to the blind hemifield, and there is good evidence of intact-blind hemifield interactions (e.g. Marzi et al., 1986). A further reason is that the refined measurement of a profile of psychophysiological responses requires specialized technical expertise.
Yet another reason is that a number of neuropsychological syndromes, and especially blindsight in hemianopia, have shaped the Zeitgeist today to be more open to the possibility of intact function even when a patient or his physician insists that there is none. But the Zeitgeist has also recently undergone another expansion, as reflected in the title of the Hamm et al. paper (‘Affective blindsight ...’), namely in considering that emotionally significant visual stimuli may enjoy a privileged processing route in the brain, especially to activate the ‘fear module’. Fear is unquestionably induced by the anticipation of electric shock to the forearm and evokes a characteristic set of physiological responses. The conditioned outline drawing of an airplane came to evoke the responses characteristic of fear.
‘Affective blindsight’ as a term was first used by De Gelder, following the report of successful forced-choice discrimination of positive versus negative facial expressions projected into the hemianopic blind field (De Gelder et al., 1999). In an fMRI study (Morris et al., 2001) of a blindsight subject (GY) differential amygdala responses were found to the presentation of fearful and fear-conditioned faces in the blind field (in their study the fear conditioning was established in the intact visual field, but shown to be effective in the blind field). The amygdala responses covaried with neural activity in the posterior thalamus and superior colliculus, both of which have been implicated in non-striate visual function in monkeys. An alternative approach to blindsight through brain damage is to render stimuli invisible in normal subjects by means of backward masking. Thus, Morris et al. (1999) reported stronger activation in the amygdala to fearful stimuli in an imaging study using such a paradigm.
A number of points await further research. The conditioning experiment by Hamm et al. was carried out only 3 days after the patient’s admission. Long-term changes could be of considerable significance if they are followed up, as one hopes they will be. In this context, bilateral cases enjoy a special place, because hemianopic subjects are usually perfectly content to depend wholly on their intact hemifields and hence to deprive their blind fields of the specific practice that could be helpful, whereas a bilateral case would of necessity be forced to use subcortical extra-striate routes for visual processing. The potential capacity could be of considerable interest.
Also, the question of whether emotional stimuli, conditioned or unconditioned, have some special priority over extra-striate routes will no doubt be subjected to further refinement in the new field of ‘affective blindsight’. Some recent evidence, for example, suggests that emotional expressions of faces presented to the blind field are processed differently from non-facial emotional objects (De Gelder et al., 2002). And what was the reported experience of the Hamm et al. subject—did he experience fear without knowing why?
The importance of the amygdala in emotional processing is well established, and the route over which visual effects can reach it, with or without striate cortex, is of great interest, but it is not clear, as an empirical fact, whether a stimulus is rendered more discriminable or detectable in the blind field if it is either naturally emotive or is made more emotive via classical conditioning. Nothing could be more neutrally boring than a 2 cycle/degree sine-wave grating, and yet blindsight subjects can discriminate it, and other equally boring spatiotemporally-defined stimuli, from a luminous matched background (Weiskrantz, 1986; Sahraie et al., 2002). A brightness difference is not a requisite, as Hamm et al. suggest. There is now an opportunity to extend the skill and attention that Hamm et al. apply to the psychophysiology to the properties of the visual stimuli themselves.
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