Intact hemisphere and corpus callosum compensate for visuomotor functions after early visual cortex damage.

Unilateral damage to the primary visual cortex (V1) leads to clinical blindness in the opposite visual hemifield, yet nonconscious ability to transform unseen visual input into motor output can be retained, a condition known as "blindsight." Here we combined psychophysics, functional magnetic resonance imaging, and tractography to investigate the functional and structural properties that enable the developing brain to partly overcome the effects of early V1 lesion in one blindsight patient. Visual stimuli appeared in either the intact or blind hemifield and simple responses were given with either the left or right hand, thereby creating conditions where visual input and motor output involve the same or opposite hemisphere. When the V1-damaged hemisphere was challenged by incoming visual stimuli, or controlled manual responses to these unseen stimuli, the corpus callosum (CC) dynamically recruited areas in the visual dorsal stream and premotor cortex of the intact hemisphere to compensate for altered visuomotor functions. These compensatory changes in functional brain activity were paralleled by increased connections in posterior regions of the CC, where fibers connecting homologous areas of the parietal cortex course.

Dynamic Changes in Amygdala Psychophysiological Connectivity Reveal Distinct Neural Networks for Facial Expressions of Basic Emotions.

The quest to characterize the neural signature distinctive of different basic emotions has recently come under renewed scrutiny. Here we investigated whether facial expressions of different basic emotions modulate the functional connectivity of the amygdala with the rest of the brain. To this end, we presented seventeen healthy participants (8 females) with facial expressions of anger, disgust, fear, happiness, sadness and emotional neutrality and analyzed amygdala's psychophysiological interaction (PPI). In fact, PPI can reveal how inter-regional amygdala communications change dynamically depending on perception of various emotional expressions to recruit different brain networks, compared to the functional interactions it entertains during perception of neutral expressions. We found that for each emotion the amygdala recruited a distinctive and spatially distributed set of structures to interact with. These changes in amygdala connectional patters characterize the dynamic signature prototypical of individual emotion processing, and seemingly represent a neural mechanism that serves to implement the distinctive influence that each emotion exerts on perceptual, cognitive, and motor responses. Besides these differences, all emotions enhanced amygdala functional integration with premotor cortices compared to neutral faces. The present findings thus concur to reconceptualise the structure-function relation between brain-emotion from the traditional one-to-one mapping toward a network-based and dynamic perspective.

Pupil response as a predictor of blindsight in hemianopia.

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%.

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.

Spatiotemporal profiles of visual processing with and without primary visual cortex.

The spatiotemporal profiles of visual processing are normally distributed in two temporal phases, each lasting about 100 ms. Within each phase, cortical processing begins in V1 and traverses the visual cortical hierarchy. However, the causal role of V1 in starting each of these two phases is unknown. Here we used magnetoencephalography to study the spatiotemporal profiles of visual processing and the causal contribution of V1 in three neurologically intact participants and in a rare patient (GY) with unilateral destruction of V1, in whom residual visual functions mediated by the extra-geniculostriate pathways have been reported. In healthy subjects, visual processing in the first 200 ms post-stimulus onset proceeded in the two usual phases. Normally perceived stimuli in the left hemifield of GY elicited a spatiotemporal profile in the intact right hemisphere that closely matched that of healthy subjects. However, stimuli presented in the cortically blind hemifield produced no detectable response during the first phase of processing, indicating that the responses in extrastriate visual areas during this phase are determined by the feedforward progression of activity initiated in V1. The first responses occurred during the second processing phase, in the ipsilesional high-level visual areas. The activity then spread forward toward higher-level areas and backward toward lower-level areas. However, in contrast to responses in the intact hemisphere, the back-propagated activity in the early visual cortex did not exhibit the classic retinotopic organization and did not have well-defined response peaks.

Subcortical connections to human amygdala and changes following destruction of the visual cortex.

Nonconscious [1-6], rapid [7, 8], or coarse [9] visual processing of emotional stimuli induces functional activity in a subcortical pathway to the amygdala involving the superior colliculus and pulvinar. Despite evidence in lower mammals [10, 11] and nonhuman primates [12], it remains speculative whether anatomical connections between these structures exist in the human brain [13-15]. It is also unknown whether destruction of the visual cortex, which provides a major input to the amygdala, induces modifications in anatomical connections along this subcortical pathway. We used diffusion tensor imaging to investigate in vivo anatomical connections between human amygdala and subcortical visual structures in ten age-matched controls and in one patient with early unilateral destruction of the visual cortex. We found fiber connections between pulvinar and amygdala and also between superior colliculus and amygdala via the pulvinar in the controls as well as in the patient. Destruction of the visual cortex led to qualitative and quantitative modifications along the pathways connecting these three structures and the changes were confined to the patient's damaged hemisphere. The present findings thus show extensive neural plasticity in the anatomical connections between subcortical visual structures of old evolutionary origin involved in the processing of emotional stimuli.

Consciousness of the first order in blindsight.

At suprathreshold levels, detection and awareness of visual stimuli are typically synonymous in nonclinical populations. But following postgeniculate lesions, some patients may perform above chance in forced-choice detection paradigms, while reporting not to see the visual events presented within their blind field. This phenomenon, termed "blindsight," is intriguing because it demonstrates a dissociation between detection and perception. It is possible, however, for a blindsight patient to have some "feeling" of the occurrence of an event without seeing per se. This is termed blindsight type II to distinguish it from the type I, defined as discrimination capability in the total absence of any acknowledged awareness. Here we report on a well-studied patient, D.B., whose blindsight capabilities have been previously documented. We have found that D.B. is capable of detecting visual patterns defined by changes in luminance (first-order gratings) and those defined by contrast modulation of textured patterns (textured gratings; second-order stimuli) while being aware of the former but reporting no awareness of the latter. We have systematically investigated the parameters that could lead to visual awareness of the patterns and show that mechanisms underlying the subjective reports of visual awareness rely primarily on low spatial frequency, first-order spatial components of the image.

Collicular vision guides nonconscious behavior.

Following destruction or deafferentation of primary visual cortex (area V1, striate cortex), clinical blindness ensues, but residual visual functions may, nevertheless, persist without perceptual consciousness (a condition termed blindsight). The study of patients with such lesions thus offers a unique opportunity to investigate what visual capacities are mediated by the extrastriate pathways that bypass V1. Here we provide evidence for a crucial role of the collicular-extrastriate pathway in nonconscious visuomotor integration by showing that, in the absence of V1, the superior colliculus (SC) is essential to translate visual signals that cannot be consciously perceived into motor outputs. We found that a gray stimulus presented in the blind field of a patient with unilateral V1 loss, although not consciously seen, can influence his behavioral and pupillary responses to consciously perceived stimuli in the intact field (implicit bilateral summation). Notably, this effect was accompanied by selective activations in the SC and in occipito-temporal extrastriate areas. However, when instead of gray stimuli we presented purple stimuli, which predominantly draw on S-cones and are thus invisible to the SC, any evidence of implicit visuomotor integration disappeared and activations in the SC dropped significantly. The present findings show that the SC acts as an interface between sensory and motor processing in the human brain, thereby providing a contribution to visually guided behavior that may remain functionally and anatomically segregated from the geniculo-striate pathway and entirely outside conscious visual experience.

Unseen facial and bodily expressions trigger fast emotional reactions.

The spontaneous tendency to synchronize our facial expressions with those of others is often termed emotional contagion. It is unclear, however, whether emotional contagion depends on visual awareness of the eliciting stimulus and which processes underlie the unfolding of expressive reactions in the observer. It has been suggested either that emotional contagion is driven by motor imitation (i.e., mimicry), or that it is one observable aspect of the emotional state arising when we see the corresponding emotion in others. Emotional contagion reactions to different classes of consciously seen and "unseen" stimuli were compared by presenting pictures of facial or bodily expressions either to the intact or blind visual field of two patients with unilateral destruction of the visual cortex and ensuing phenomenal blindness. Facial reactions were recorded using electromyography, and arousal responses were measured with pupil dilatation. Passive exposure to unseen expressions evoked faster facial reactions and higher arousal compared with seen stimuli, therefore indicating that emotional contagion occurs also when the triggering stimulus cannot be consciously perceived because of cortical blindness. Furthermore, stimuli that are very different in their visual characteristics, such as facial and bodily gestures, induced highly similar expressive responses. This shows that the patients did not simply imitate the motor pattern observed in the stimuli, but resonated to their affective meaning. Emotional contagion thus represents an instance of truly affective reactions that may be mediated by visual pathways of old evolutionary origin bypassing cortical vision while still providing a cornerstone for emotion communication and affect sharing.

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 patient's 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/ degrees 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.

Fear recognition in the voice is modulated by unconsciously recognized facial expressions but not by unconsciously recognized affective pictures.

Multisensory integration is a powerful mechanism for increasing adaptive responses, as illustrated by binding of fear expressed in a face with fear present in a voice. To understand the role of awareness in intersensory integration of affective information we studied multisensory integration under conditions of conscious and nonconscious processing of the visual component of an audiovisual stimulus pair. Auditory-event-related potentials were measured in two patients (GY and DB) who were unable to perceive visual stimuli consciously because of striate cortex damage. To explore the role of conscious vision of audiovisual pairing, we also compared audiovisual integration in either naturalistic pairings (a facial expression paired with an emotional voice) or semantic pairings (an emotional picture paired with the same voice). We studied the hypothesis that semantic pairings, unlike naturalistic pairings, might require mediation by intact visual cortex and possibly by feedback to primary cortex from higher cognitive processes. Our results indicate that presenting incongruent visual affective information together with the voice translates as an amplitude decrease of auditory-event-related potentials. This effect obtains for both naturalistic and semantic pairings in the intact field, but is restricted to the naturalistic pairings in the blind field.

Prime-sight in a blindsight subject.

A subject (D.B.) who had no experience of visual stimuli in a field defect caused by visual cortex damage but could discriminate them ('blindsight') nevertheless reported visible after-images of the stimuli when they were turned off ('prime-sight'). This was investigated using projected visual stimuli of varying colors, contrasts, shapes and spatial frequencies, and by measuring the properties of the after-images, including their duration, size scaling, color and interocular transfer, comparing the capacity of the blindsight and prime-sight modes. These phenomena offer a unique opportunity to compare conscious and unconscious neural events in response to the same visual events.