Detection and discrimination of chromatic targets in hemianopic macaque monkeys and humans.

We measured the ability of three macaque monkeys with unilateral removal of primary visual cortex to detect 9 degrees, 200-ms targets presented at random in the upper or lower quadrants of the normal and hemianopic visual fields. The white or variously coloured target could differ from the background in both colour and luminance, or in either of them. Blue and red targets were detectable at any luminance contrast, but green and white targets were barely or not at all detectable at and near isoluminance in the hemianopic field. Blue and red targets were better detected than white targets at the same luminance difference. However, when both the target and the background were dynamically luminance-masked, detection in the hemianopic field failed at isoluminance whatever the colour. In addition, the monkeys were unable to discriminate between simultaneously presented red and green or blue and green targets in the hemianopic field when both targets had similar luminance contrast with the background. Two hemianopic patients tested on a subset of the tasks performed similarly to the monkeys. Together, the results indicate that the residual colour-opponent system that survives damage to V1 is involved in the detection of chromatic changes but cannot sustain simultaneous discrimination between pairs of colours.

Neural correlates of religious experience.

The commonsense view of religious experience is that it is a preconceptual, immediate affective event. Work in philosophy and psychology, however, suggest that religious experience is an attributional cognitive phenomenon. Here the neural correlates of a religious experience are investigated using functional neuroimaging. During religious recitation, self-identified religious subjects activated a frontal-parietal circuit, composed of the dorsolateral prefrontal, dorsomedial frontal and medial parietal cortex. Prior studies indicate that these areas play a profound role in sustaining reflexive evaluation of thought. Thus, religious experience may be a cognitive process which, nonetheless, feels immediate.

The neuroanatomy of phenomenal vision: a psychological perspective.

Somewhere in the visual system, phenomenal vision--the seeing of colors, brightness, depths, shades, and motion--is generated not only from the distribution of light on the retina, but also when the eyes are closed, in dreams, hallucinations, phosphenes, and (possibly) imagery. Whether these different forms of phenomenal vision share a common substrate although their origins are different (optical, mechanical, electrical, endogenous) is discussed in the light of evidence from neuropsychological and functional imaging studies. Whereas extrastriate visual cortical areas appear to be involved in all types of phenomenal vision that have been studied, the necessity of a contribution from primary visual cortex is demonstrated by the loss of conscious vision that follows its destruction. If both extrastriate and primary cortical activation are needed, the latter may not just provide an indispensable input, but may also need to receive the output of the extrastriate processing via reentrant connections.

Sustained extrastriate cortical activation without visual awareness revealed by fMRI studies of hemianopic patients.

Patients with lesions in the primary visual cortex (V1) may show processing of visual stimuli presented in their field of cortical blindness even when they report being unaware of the stimuli. To elucidate the neuroanatomical basis of their residual visual functions, we used functional magnetic resonance imaging in two hemianopic patients, FS and GY. In the first experiment, a rotating spiral stimulus was used to assess the responsiveness of dorsal stream areas. Although no response was detectable within denervated or destroyed early visual cortex, motion-sensitive areas (hMT+/V5) ipsilateral to the lesion showed a strong sustained hemodynamic response. In GY, this activation was at least as strong as that of his contralesional hMT+/V5 to the stimulus in the normal hemifield. In the second experiment, coloured images of natural objects were used to assess the responsiveness of ventral stream areas. Again, no activity was detectable in ipsilesional early visual areas, but extrastriate areas in the lateral occipital cortex (hMT+/V5 and LO) and within the posterior fusiform gyrus (V4/V8) showed a robust sustained hemodynamic response. In both experiments, we observed that ipsilesional areas responded to stimuli presented in either hemifield, whereas the normal hemisphere responded preferentially to stimuli in the sighted hemifield. As only one subject occasionally noticed the onset of stimulation in the impaired field, the unexpectedly strong sustained activity in ipsilesional dorsal and ventral cortical areas appears to be insufficient to generate conscious vision.

Is V1 necessary for conscious vision in areas of relative cortical blindness?

Visual field defects result from postgeniculate lesions. It is generally assumed that absolute defects are caused by total destruction or denervation of primary visual cortex (V1) and that the degraded but conscious vision that remains or returns in relative or partial defects is mediated by compromised V1 cortex that retains a sufficiently large population of functional neurons. We here report the results of three patients with long-standing postgeniculate lesions who underwent functional magnetic resonance imaging while their partial defect was stimulated with high-contrast reversing checkerboard stimuli. Although the stimulation evoked conscious visual impressions in all three, in only one patient did it activate perilesional V1. In the other two we found no evidence for perilesional activation, indicating that some conscious vision may return in the absence of functional ipsilesional V1.

The retinal projection to the pregeniculate nucleus in normal and destriate monkeys.

Taking advantage of the segregation of different classes of ganglion cell fibres in the optic tract, we investigated the ganglion cell class that projects to the pregeniculate nucleus (PGN) in the normal macaque monkey (Macaca mulatta and Macaca fascicularis) and following long-standing removal of striate cortex in one hemisphere. Confining small pellets of horseradish peroxidase and biocytin into ventral or dorsal parts of the tract unilaterally, or placing several pellets throughout the tract, we labelled the retina retrogradely and the PGN anterogradely. Classification of ganglion cells according to soma size and dendritic morphology showed that implants in the dorsal part of the tract labelled predominantly, and perhaps exclusively, P beta cells, and produced dense anterograde label in the parvocellular lateral geniculate nucleus as well in the PGN. Labelling of the PGN was sparse or absent following implants into the ventral aspect of the tract, which labelled the magnocellular geniculate nucleus anterogradely and chiefly P alpha and P gamma cells retrogradely. The finding of a projection to the PGN from P beta cells has implications for the permanent selective sparing of a subpopulation of these cells after removal of striate cortex and their contribution to wavelength processing in blindsight.

Change blindness and time to consciousness.

Detection of changes in a visual scene can be substantially delayed when the original and the modified image are separated by a brief screen flicker. We used this phenomenon of "change blindness" to find when the brain detects the mismatch in relation to when the observer reports it, and whether changes in identity and position are processed similarly. Event-related brain potentials (ERPs) recorded while the subjects searched for the change in alternating series of images showed that the epoch during which they indicated detection was characterized by a marked positivity from 300 to 700 ms. Analysis of data from image presentations preceding the subjects' response revealed a similar but smaller ERP positivity one (identity) or even two (position) epochs before detection. As each epoch lasted 1500 ms, the brain may register a change as early as 3000 ms before the observer.

Low-level phenomenal vision despite unilateral destruction of primary visual cortex.

GY, an extensively studied human hemianope, is aware of salient visual events in his cortically blind field but does not call this "vision." To learn whether he has low-level conscious visual sensations or whether instead he has gained conscious knowledge about, or access to, visual information that does not produce a conscious phenomenal sensation, we attempted to image process a stimulus s presented to the impaired field so that when the transformed stimulus T(s) was presented to the normal hemifield it would cause a sensation similar to that caused by s in the impaired field. While degradation of contrast, spatio-temporal filtering, contrast reversal, and addition of smear and random blobs all failed to match the response to a flashed bar s(f), moving textures of low contrast were accepted to match the response to a moving contrast-defined bar, s(m). Orientation and motion direction discrimination of the perceptually matched stimuli [s(m) and T(s(m))] was closely similar. We suggest that the existence of a satisfactory match indicates that GY has phenomenal vision.

Spectral sensitivity in hemianopic macaque monkeys.

We measured the increment threshold sensitivity to 2 degrees, 200-ms targets presented at a lateral and radial eccentricity of approximately 20-26 degrees in both visual hemifields of three macaque monkeys whose left striate cortex had been removed 5 years earlier, and in one normal control. As in patients with blindsight, sensitivity of the hemianopic field for blue, green and red stimuli was reduced by as little as 0.5 log units. With increasing light adaptation from scotopic to mesopic to photopic levels, there was a progressive increase in the sensitivity to long wavelengths relative to that for short and medium wavelengths. This shift in relative sensitivity ('Purkinje shift') shows that rod and cone mechanisms operate in both the normal and hemianopic fields and that the sensitivity that remains following removal of striate cortex is not mediated exclusively by rods.

Variance in transneuronal retrograde ganglion cell degeneration in monkeys after removal of striate cortex: effects of size of the cortical lesion.

The extent of transneuronal retrograde degeneration of ganglion cells in the primate retina depends on the age at which striate cortex was damaged, the survival time, the species, and retinal eccentricity. We here report on the effect of lesion size beyond striate cortex, which we assessed along with retinal ganglion cell degeneration in three groups of macaque monkeys who, in each group, had undergone striate cortical ablation at similar ages and survived for similar periods, which ranged from 302 days to 8 years. Where possible, the number of surviving projection neurones in the degenerated dLGN and its volume were also estimated. Results confirm that both geniculate and retinal degeneration correlate significantly with survival time but that the differences within a group can exceed differences between groups and are best accounted for by the extent of the damage to extra-striate visual cortex and underlying white matter.

Effects of unseen stimuli on reaction times to seen stimuli in monkeys with blindsight.

In three macaque monkeys with unilateral removal of primary visual cortex and in one unoperated monkey, we measured reaction times to a visual target that was presented at a lateral eccentricity of 20 degrees in the normal, left, visual hemifield. When an additional stimulus was presented at the corresponding position in the right hemifield (hemianopic in three of the monkeys), it significantly slowed the reaction time to the left target if it preceded it by delays from 100-500 msec. The most effective delay depended on the particular experimental paradigm and perhaps on the experience of the monkey with the task. The results show that reaction times to seen targets in the normal hemifield of monkeys are influenced by the presentation of "unseen" targets in the anopic hemifield, as in some patients with cortically blind visual field defects.

No visual responses in denervated V1: high-resolution functional magnetic resonance imaging of a blindsight patient.

Following severe cranio-cerebral trauma that affected the optic radiation, patient FS suffers from an incomplete macula-splitting hemianopia. Within the hemianopic field, FS exhibits blindsight, i.e. he detects and discriminates visual stimuli he cannot (consciously) see. We performed functional magnetic resonance imaging (fMRI) at high spatial resolution using a large flickering stimulus field to assess visual responsiveness of deafferented V1. Contrasting strong activation of the normal contralesional visual cortex, ipsilesional V1 displayed no stimulus-related MRI signal changes. However, activation was observed in ipsilesional extrastriate cortex. We conclude that blindsight does not depend on functional islands of tissue preserved within the deafferented striate cortex.

Visual detection in monkeys with blindsight.

Monkeys with unilateral striate cortical removal show residual visual abilities in their affected hemifield. To learn whether the monkeys, like patients with blindsight, lose the phenomenal representation of the visual stimuli they nevertheless respond to, we first studied their ability to localize a briefly presented target in either hemifield. By varying the luminance of the stimuli we determined their visual sensitivity, which was reduced by 0.3-1.5 log units in the impaired hemifield; suprathreshold stimuli yielded almost perfect performance. We then presented two tests designed to show whether the monkeys categorized visual stimuli in the impaired field in the same manner as they categorize them in the normal field. In the first test, they had to respond differently according to whether one or two lights were presented, with the relative position of the two stimuli in a pair being varied. Whenever one of the paired stimuli lay in the impaired hemifield, two of the three monkeys consistently ignored it, and responded as if it had been a single stimulus in the good field. In the second test, trials consisting of a single stimulus light were interleaved with blank trials. The monkey touched the position of the light or made a different response, indicating that no light had appeared. All three monkeys responded to a light of supra-threshold luminance presented in the impaired field as if it were a blank trial. These results suggest that monkeys with striate cortical destruction, like neurological patients with similar lesions, have blindsight rather than phenomenal vision when they have to detect brief static visual targets.

Blindsight in man and monkey.

In man and monkey, absolute cortical blindness is caused by destruction of the optic radiations and/or the primary visual cortex. It is characterized by an absence of any conscious vision, but stimuli presented inside its borders may nevertheless be processed. This unconscious vision includes neuroendocrine, reflexive, indirect and forced-choice responses which are mediated by the visual subsystems that escape the direct cerebral damage and the Ensuring degeneration. While extrastriate cortical areas participate in the mediation of the forced-choice responses, a concomitant striate cortical activation does not seem to be necessary for blindsight. Whether the loss of phenomenal vision is a necessary consequence of striate cortical destruction and whether this structure is indispensable for conscious sight are much debated questions which need to be tackled experimentally.

Varieties of vision: from blind responses to conscious recognition.

Lesions in consecutive parts of the visual system cause visual deficits that spare increasingly complex residual functions. Patients with lesions up to and including primary visual cortex can show neuroendocrine, reflexive, implicit and forced-choice responses to visual stimulation but no conscious vision. In contrast, patients with lesions in higher visual cortical areas have conscious vision. Its lowest level is that of phenomenal vision, followed by object vision and recognition. These levels are dissociable. They require the integrity of different parts of the system.

No blindsight following hemidecortication in human subjects?

Using a guessing paradigm we measured visual sensitivity in the blind and normal half-fields of four cerebrally hemidecorticated patients. In the blind field, sensitivity was reduced by approximately 3 long units. Stimuli which produced significant detection also evoked conscious sensations of light and colour. Control experiments showed that although sensitivity in the blind field depended in a normal fashion on background luminance it was independent of the luminance of a local platform, and showed no spatial summation. This residual vision can be explained by intraocular light diffusion and reflection.

Visual perception and phenomenal consciousness.

In the (re-)animated debate on consciousness we focus on three questions: Who has consciousness? What is its neuronal basis? What is its function? Regarding the first, we suggest that consciousness is exclusive to living organisms able to distinguish self from non-self. It may be restricted further to organisms who possess a repertoire of overt and covert behaviour which can be voluntarily modified and suppressed. This requires an intermediary neuronal net mediating between sensory input and behavioural output. What are the properties of this net which distinguish unalloyed information processing per se from conscious representation? To tackle this second question, we use the visual system and the functional losses that result from lesions at its different levels, and differentiate a reflexive, a phenomenal, and a consciously accessible stage of visual processing. We suggest that the latter two represent two distinct aspects of consciousness. Blindsight, a neurological example of visual processing in the absence of phenomenal vision, could help to elucidate the neuronal basis of phenomenality, and the special role of striate cortex. Like the patients, our monkeys with unilateral striate cortical removal show evidence not just of residual visual processing, but of the same absence of phenomenal vision, opening routes to further exploring the details of its neuronal implementation. The second aspect, conscious access to presently or previously processed information, is likely to require higher cortical structures, and may depend on the stage of phenomenal representations. In patients with blindsight, both aspects are lost, and it is conceivable that a loss of phenomenality generally causes a loss of conscious accessibility. One important function of phenomenal representations, our third question, would then be to allow conscious retrieval and manipulation of currently processed or formerly stored information, enabling organisms to consciously think and plan.

Blindsight in monkeys.

Blindsight, the visually evoked voluntary responses of patients with striate cortical destruction that are demonstrated despite a phenomenal blindness, has attracted attention from neuroscientists and philosophers interested in problems of perceptual consciousness and its neuronal basis. It is assumed to be mediated by the numerous extra-geniculostriate cortical retinofugal pathways whose properties are studied primarily in monkeys. Like patients with blindsight, monkeys with lesions of the primary visual cortex can learn to detect, localize and distinguish between visual stimuli presented within their visual field defects. Although the patients deny seeing the stimuli they can nevertheless respond to (by forced-choice guessing) in their phenomenally blind fields, it is not known whether the monkeys experience the same absence of phenomenal vision. To determine whether they too have blindsight, or whether they actually see the stimuli in their field defects, monkeys who showed excellent detection in tasks where a visual stimulus was presented on every trial, albeit at different positions, were tested in a signal-detection task in which half the trials were blank trials, with no visual stimulus. They classified the visual stimuli presented in the field defect as blank trials, demonstrating, like patients, blindsight rather than degraded real vision.

Retinal ganglion cells labelled from the pulvinar nucleus in macaque monkeys.

In order to study the distribution and morphological classes of retinal ganglion cells that can be retrogradely labelled from the pulvinar nucleus, we made two iontophoretic injections of horseradish peroxidase into the pulvinar in each hemisphere of five macaque monkeys. The retrogradely labelled ganglion cells projecting to or through the pulvinar nucleus were examined in retinal whole-mounts. They comprise all three major ganglion cell classes. Primate gamma cells formed the great majority of classifiable cells and, like the primate alpha cells that were found in much smaller numbers, they were already known to send axons to the superior colliculus and to the pretectal complex. In contrast, the primate beta cells were hitherto thought to project solely to the dorsal lateral geniculate nucleus. This primate beta cell projection to an extrageniculate target could account in part for the substantial number of primate beta cells that escape transneuronal retrograde retinal degeneration following striate cortical ablation, and might contribute to the residual visual sensitivity that survives destruction of striate cortex and the degeneration of the lateral geniculate nucleus.

Spatial summation in blindsight.

Spatial summation curves were determined in the circumscribed visual-field defects of five patients with blindsight. Under light-adapted conditions that favor the color-opponent system, increment thresholds for white and red targets presented on a white background were measured as a function of stimulus size which ranged from 9-110 min arc. In both normal and defective hemifields, summation was linear for the red stimuli. In contrast, the curves measured with the white stimuli showed some nonlinearity in the normal hemifield, and a pronounced eccentricity-dependent notch in the field defect. The results indicate that the neurons mediating sensitivity differ in their summation properties for wavelength and intensity information.