Ceri T. Trevethan

Increased sensitivity after repeated stimulation of residual spatial channels in blindsight

Lesions of the occipital cortex result in areas of cortical blindness affecting the corresponding regions of the patients visual field. The traditional view is that, aside from some spontaneous recovery in the first few months after the damage, when acute effects have subsided the areas of blindness are absolute and permanent. It has been found, however, that within such field defects some residual visual capacities may persist in the absence of acknowledged awareness by the subject (blindsight type 1) or impaired awareness (type 2). Neuronal pathways mediating blindsight have a specific and narrow spatial and temporal bandwidth. A group of cortically blind patients (n = 12) carried out a daily detection “training” task over a 3-month period, discriminating grating visual stimuli optimally configured for blindsight from homogeneous luminance-matched stimuli. No feedback was given during the training. Assessment of training was by psychophysical measurements carried out before and after training and included detection of a range of spatial frequencies (0.5–7 cycles per degree), contrast detection at 1 cycle per degree, clinical perimetry, and subjective estimates of visual field defect. The results show that repeated stimulation by appropriate visual stimuli can result in improvements in visual sensitivities in the very depths of the field defect.

Spatial channels of visual processing in cortical blindness

Blindsight is the ability of some cortically blind patients to discriminate visual events presented within their field defect. We have examined a fundamental aspect of visual processing, namely the detection of spatial structures presented within the field defect of 10 cortically blind patients. The method outlined is based on the detection of high‐contrast stimuli and is effective in flagging a ‘window of detection’ in the spatial frequency spectrum, should it exist. Here we report on the presence of a narrowly tuned psychophysical spatial channel optimally responding to frequencies less than 4 cycles/° in eight out of 10 patients tested. The two patients who did not show any evidence of blindsight appear to have intact midbrain structures, but have lesions that extend from the occipital cortex to the thalamus. In addition, we have recorded subjective reports of awareness of the visual events in each trial. Detection scores of eight blindsight patients were subsequently subdivided based on the subjective reports of awareness. It appears that the psychophysical spatial channel‐mediating responses in the absence of any awareness of the visual event have a narrower frequency response than those involved when the patients report some awareness of the visual event. The findings are discussed in relation to previous reports on the incidence of blindsight and performance on tasks involving spatial processing.

Psychophysical and pupillometric study of spatial channels of visual processing in blindsight

To date no systematic method has been used for characterising the residual capacity of blindsight subjects that would allow comparison and generalisation across all subjects. The detection of isoluminant gratings of varying spatial and temporal frequencies commends itself for detailed between-subject comparison, and for mapping results onto physiological properties in relation to neuronal circuitry. We report the ability of a blindsight subject (CS) to detect suprathreshold sine-wave gratings over a range of spatial and temporal frequencies using psychophysical techniques. A band-pass spatial channel with an upper cutoff below 3.5 cycles/deg is specified. The data also have been analysed to compare differences between two types of blindsight performances, type I and type II. Spatial gratings were also used to elicit a pupillary grating response, offering an objective method that is free of verbal nuances and response bias, and the resulting band-pass channel can be used both for clinical screening and for prediction and comparisons with psychophysical profiles. Finally, we have compared our results with those reported in studies of a well-known subject, GY, which demonstrate remarkable similarities. Implications are discussed in relation to blindsight research.

Can blindsight be superior to ‘sighted-sight’? ☆

DB, the first blindsight case to be tested extensively (Weiskrantz, 1986) has demonstrated the ability to detect and discriminate a range of visual stimuli presented within his perimetrically blind visual field defect. In a temporal two alternative forced choice (2AFC) detection experiment we have investigated the limits of DBs detection ability within his field defect. Blind field performance was compared to his sighted field performance and to an age-matched control group (n=6). DB reliably detected the presence of a small (2 degrees ), low contrast (7%), 4.6c/ degrees Gabor patch with the same space-averaged luminance as the background presented within his blind field but performed at chance levels at the same eccentricity (11.3 degrees ) within his sighted field. Investigation of detection as a function of stimulus contrast revealed DBs ability to detect the presence of an 8% contrast stimulus within his blind field, compared to 12% in his sighted field. No significant difference in detection performance between DBs sighted field and the performance of six age-matched control participants suggests poor sighted field performance does not account for the results. Monocular testing also rules out differences between the eyes as an explanation, suggesting that DB demonstrates superior detection for certain stimuli within his visual field defect compared to normal vision.

The continuum of detection and awareness of visual stimuli within the blindfield: from blindsight to the sighted-sight.

PURPOSE We investigated systematically the effect of repeated exposure on detection and reported awareness of visual stimuli presented deep within the field defect of 5 hemianopic patients. METHODS An objective measure of sensitivity (detection in a temporal two-alternative forced-choice paradigm) and subjective reports of awareness were recorded on trial by trial bases. Visual stimulus to be detected was a temporally modulated (10 Hz) circular patch (6° diameter) of vertical grating (1 c/°). Hemianopic patients took part in the study 8 to 15 months after injury, so that the findings could not be attributed to spontaneous recovery. RESULTS Initially, high contrast (90%) target stimuli were detected at or near chance level with little reported awareness. In 4 of 5 cases, repeated stimulation led to improved sensitivity, indicated by increased detection scores and higher incidence of awareness. In a fifth case, there was no change in sensitivity despite extensive exposure (>22,000 trials). CONCLUSIONS At retinal locations deep within the field defect, repeated stimulation can lead to blindsight performance (type I detection without awareness), followed by detection with reported awareness (type II blindsight), and eventual reported visual experiences. The findings indicate that conscious awareness of stimuli lies on a continuous spectrum and repeated systematic training can lead to improved visual sensitivity.

Spatial and temporal processing in a subject with cortical blindness following occipital surgery

Blindsight subjects are typically better at discriminating rapid, transient visual events than those with gradual on/off-sets. Surprisingly, the detailed investigation of temporal characteristics of mechanisms mediating blindsight is only reported in one subject (GY). It is of interest to establish whether these characteristics are similar to those in other cases of blindsight. Here, we report on a systematic study of spatio-temporal properties of mechanisms mediating blindsight in a subject VN. VN has a lower right quadranopia following surgical removal of the left occipital cortex above the calcarine sulcus, therefore, there are no remaining islands of intact visual cortex within this area. Similar to GY, the blindsight mechanisms in VN have narrowly tuned band-pass temporal characteristics with a peak sensitivity at 20Hz and above chance performance at temporal frequencies >/=10 and </=33Hz. The spatial channel in VN has low-pass characteristics with an upper cut-off <3.5c/ degrees. There is extensive spatial summation in the blindfield whereas no temporal summation was found in the time range tested (50-1600ms). In agreement with our previous reports, pupillary responses can predict the existence of residual vision within the field defect and show similar spatial characteristics to those obtained psychophysically. The spatio-temporal characteristics of blindsight in VN reported here are similar to those reported in subjects with ischaemic lesions, suggesting that such visual capacities need not necessarily be attributed to spared areas of visual cortex.

Pupil response as a predictor of blindsight in hemianopia.

Significance The paper follows up the suggestion that pupillometry may reveal the presence of residual visual function of which subjects are unaware (blindsight) in the field defects caused by visual cortex lesions. In a group of 19 subjects with hemi-field cortical blindness, the pupil responses in the majority matched the psychophysical findings for the sensitive spatial frequencies, indicating that it is useful to carry out pupillometry in cortical blind fields as a predictor of intact visual psychophysical function for further rehabilitation procedures. Significantly above-chance detection of stimuli presented within the field defect of patients with postgeniculate lesions is termed “blindsight.” It has been proposed that those with blindsight are more likely to benefit from visual rehabilitation by repeated stimulation, leading to increased visual sensitivity within their field defect. Establishing the incidence of blindsight and developing an objective and reliable method for its detection are of great interest. Sudden onsets of a grating pattern in the absence of any change in light flux result in a transient constriction of the pupil, termed “pupil grating response.” The existence of pupil grating responses for stimuli presented within the blindfield has previously been reported in a hemianopic patient and two monkeys with removal of the primary visual cortex unilaterally. Here, we have systematically investigated the presence of a spatial channel of processing at a range of spatial frequencies using a psychophysical forced-choice technique and obtained the corresponding pupil responses in the blindfield of 19 hemianopic patients. In addition, in 13 cases we determined the pupil responses in a sighted field location that matched the blindfield eccentricities. Our findings demonstrate that blindfield pupil responses are similar to those for the sighted field, but attenuated in amplitude. Pupillometry correctly characterized the presence or absence of a significant psychophysical response and thus is worth measuring in the cortically blindfields as a predictor of intact psychophysical capacity. The incidence of blindsight where detection performance had been investigated psychophysically over a range of spatial frequencies was 70%.

Does localisation blindsight extend to two-dimensional targets?

Residual sensorimotor skills which survive compromise of the geniculostriate visual system may depend on activity of the dorsal stream of extrastriate occipitoparietal cortex. These circuits are crucial for controlling hand and eye movements to targets in a three-dimensional world. Remarkably, demonstrations of above chance localisation by hand and by eye in blindsight patients have used luminous targets that were only varied in one spatial dimension. These limitations result in experimental confounds. In the present study we examined saccadic and manual localisation in a well-studied patient (DB) to positions that were varied in 1 or 2 dimensions, using targets which control for luminance artefacts. We found that his good manual localisation without awareness in 1D conditions was relatively preserved when the targets were varied in 2D. In stark contrast, saccadic performance was completely attenuated with 2D targets. These paradoxical results are difficult to reconcile with feedforward models of eye-hand coordination and with accounts of localisation that depend on intact multidimensional representations of the visual fields in non-geniculostriate systems.

Does delay impair localisation in blindsight

The unconscious sensorimotor skills which survive compromise of the geniculostriate visual pathway have been linked with activity of the dorsal stream of extrastriate occipitoparietal cortex. These sensorimotor circuits are thought to operate in real time. Therefore, an introduction of a delay between visual stimulus presentation and the patients subsequent motor response should severely compromise sensorimotor tasks such as localisation (moving hand or eye to the location of a previously presented visual target). We tested this hypothesis in patient DB, a well-studied case of blindsight whose localisation abilities were first documented in the 1970s. Using eye tracking and hand movement recording technologies, as well as stimuli that control for light scatter, we verified the original observations of DBs manual and saccadic localisation. Remarkably, the introduction of a 4s delay did not compromise his ability to localise with either eye or hand. A control experiment reveals that this skill does not depend on an opportunity to make a decision at the time of stimulus presentation, circumventing the delay using memory. These data suggest that DBs manual and saccadic localisation skills do not depend on the circuits of the dorsal stream, or that delay, contrary to theory, does not severely compromise dorsal sensorimotor skills.

Evidence for perceptual learning with repeated stimulation after partial and total cortical blindness.

Lesions of occipital cortex result in loss of sight in the corresponding regions of visual fields. The traditional view that, apart from some spontaneous recovery in the acute phase, field defects remain permanently and irreversibly blind, has been challenged. In patients with partial field loss, a range of residual visual abilities in the absence of conscious perception (blindsight) has been demonstrated (Weiskrantz, 1986). Recent findings (Sahraie et al., 2006, 2010) have also demonstrated increased visual sensitivity in the field defect following repeated stimulation. We aimed to extend these findings by systematically exploring whether repeated stimulation can also lead to increased visual sensitivity in two cases with total (bilateral) cortical blindness. In addition, for a case of partial blindness, we examined the extent of the recovery as a function of stimulated region of the visual field, over extended periods of visual training. Positive auditory feedback was provided during the training task for correct detection of a spatial grating pattern presented at specific retinotopic locations using a temporal two alternative forced-choice paradigm (Neuro-Eye Therapy). All three cases showed improved visual sensitivity with repeated stimulation. The findings indicate that perceptual learning can occur through systematic visual field stimulation even in cases of bilateral cortical blindness.