V1 Damage Research Articles

Exogenous Spatial Attention Helps Overcome Spatial Specificity of Visual Learning in the Blind Field After V1 Damage

Exogenous Spatial Attention Helps Overcome Spatial Specificity of Visual Learning in the Blind Field After V1 Damage

Patients with V1 damage exhibit increased orientation decoding in hMT+, but only if pulvinar is intact

Patients with V1 damage exhibit increased orientation decoding in hMT+, but only if pulvinar is intact

Limited restoration of contrast sensitivity with training after V1 damage in humans.

Stroke damage to the primary visual cortex (V1) causes severe visual deficits, which benefit from perceptual retraining. However, whereas training with high-contrast stimuli can locally restore orientation and motion direction discrimination abilities at trained locations, it only partially restores luminance contrast sensitivity (CS). Recent work revealed that high-contrast discrimination abilities may be preserved in the blind field of some patients early after stroke. Here, we asked if CS for orientation and direction discrimination is similarly preserved inside the blind field, to what extent, and whether it could benefit from a visual training intervention. Thirteen subacute patients (<3 months post-V1-stroke) and 12 chronic patients (>6 months post-V1-stroke) were pre-tested, then trained to discriminate either orientation or motion direction of Gabor patches of progressively lower contrasts as their performance improved. At baseline, more subacute than chronic participants could correctly discriminate the orientation of high-contrast Gabors in their blind field, but all failed to perform this task at lower contrasts, even when 10Hz flicker or motion direction were added. Training improved CS in a greater portion of subacute than chronic participants, but no-one attained normal CS, even when stimuli contained flicker or motion. We conclude that, unlike the near-complete training-induced restoration of high-contrast orientation and motion direction discrimination abilities, V1 damage in adulthood may severely limit the residual visual system's ability to regain normal CS. Our results support the notion that CS involves different neural substrates and computations than those required for orientation and direction discrimination in V1-damaged visual systems.Significance statement Stroke-induced V1 damage in adult humans induces a rapid and severe impairment of contrast sensitivity for orientation and motion direction discrimination in the affected hemifield, although discrimination of high-contrast stimuli can persist for several months. Adaptive training with Gabor patches of progressively lower contrasts improves contrast sensitivity for both orientation and motion discriminations in the blind-field of subacute (<3 months post-stroke) and chronic (>6 months post-stroke) participants; however, it fails to restore normal contrast sensitivity. Nonetheless, more subacute than chronic stroke participants benefit from such training, particularly when discriminating the orientation of static, non-flickering targets. Thus, contrast sensitivity appears critically dependent on processing within V1, with perceptual training displaying limited potential to fully restore it after V1 damage.

Poster Session: Evidence for preserved conscious orientation discrimination in perimetrically-blind fields early after V1-damage.

Cortically-blind (CB) patients with stroke damage to the primary visual cortex (V1) lose conscious vision but many exhibit blindsight - the ability to unconsciously detect or discriminate moving or flickering targets inside their blind-fields. However, the prevalence of conscious visual abilities in CB is less clear. Having developed a new method to assess vision inside perimetrically-defined blind fields, we found that >50% of subacute CB patients (<6 months post-stroke) can consciously discriminate global motion inside their blind field. Here, we asked if they can also discriminate orientation of static targets, which do not typically elicit blindsight. In 10 subacute patients, we mapped their intact and blind hemifields using static, non-flickering, 1cpd Gabors across a wide range of luminance contrasts. Blind-field locations were labeled "preserved" if performance was >72.5% correct. Considering overall performance, only 1 participant had preserved static orientation perception in the blind-field. However, this increased to 4 participants when only considering performance at high contrasts (>50%), all of whom reported awareness of stimuli. Thus, early after V1 damage, conscious percepts for oriented, high-contrast, static targets can remain inside CB fields, similar in incidence to global motion discriminations. We are now testing additional patients to assess if these abilities persist into the chronic period and to detail their underlying neural substrates.

Inner retinal integrity correlates with preservation of fine direction discrimination in the blind-field early after V1 damage

Inner retinal integrity correlates with preservation of fine direction discrimination in the blind-field early after V1 damage

Preserved blind-field visual abilities are most prevalent very early after stroke-induced V1 damage

Preserved blind-field visual abilities are most prevalent very early after stroke-induced V1 damage

Blind-field and intact-field training differentially impact retinal thinning after V1 damage

Blind-field and intact-field training differentially impact retinal thinning after V1 damage

Attributes of preserved motion discrimination inside perimetrically-blind fields early after V1 damage

Attributes of preserved motion discrimination inside perimetrically-blind fields early after V1 damage

Unilateral V1 damage leads to micro-offsets of monocular fixation towards the cortically-blinded field

Unilateral V1 damage leads to micro-offsets of monocular fixation towards the cortically-blinded field

A deep neural network model of the primate superior colliculus for emotion recognition.

Although sensory processing is pivotal to nearly every theory of emotion, the evaluation of the visual input as ‘emotional’ (e.g. a smile as signalling happiness) has been traditionally assumed to take place in supramodal ‘limbic’ brain regions. Accordingly, subcortical structures of ancient evolutionary origin that receive direct input from the retina, such as the superior colliculus (SC), are traditionally conceptualized as passive relay centres. However, mounting evidence suggests that the SC is endowed with the necessary infrastructure and computational capabilities for the innate recognition and initial categorization of emotionally salient features from retinal information. Here, we built a neurobiologically inspired convolutional deep neural network (DNN) model that approximates physiological, anatomical and connectional properties of the retino-collicular circuit. This enabled us to characterize and isolate the initial computations and discriminations that the DNN model of the SC can perform on facial expressions, based uniquely on the information it directly receives from the virtual retina. Trained to discriminate facial expressions of basic emotions, our model matches human error patterns and above chance, yet suboptimal, classification accuracy analogous to that reported in patients with V1 damage, who rely on retino-collicular pathways for non-conscious vision of emotional attributes. When presented with gratings of different spatial frequencies and orientations never ‘seen’ before, the SC model exhibits spontaneous tuning to low spatial frequencies and reduced orientation discrimination, as can be expected from the prevalence of the magnocellular (M) over parvocellular (P) projections. Likewise, face manipulation that biases processing towards the M or P pathway affects expression recognition in the SC model accordingly, an effect that dovetails with variations of activity in the human SC purposely measured with ultra-high field functional magnetic resonance imaging. Lastly, the DNN generates saliency maps and extracts visual features, demonstrating that certain face parts, like the mouth or the eyes, provide higher discriminative information than other parts as a function of emotional expressions like happiness and sadness. The present findings support the contention that the SC possesses the necessary infrastructure to analyse the visual features that define facial emotional stimuli also without additional processing stages in the visual cortex or in ‘limbic’ areas.This article is part of the theme issue ‘Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience’.

Perceptual restoration fails to recover unconscious processing for smooth eye movements after occipital stroke.

The visual pathways that guide actions do not necessarily mediate conscious perception. Patients with primary visual cortex (V1) damage lose conscious perception but often retain unconscious abilities (e.g. blindsight). Here, we asked if saccade accuracy and post-saccadic following responses (PFRs) that automatically track target motion upon saccade landing are retained when conscious perception is lost. We contrasted these behaviors in the blind and intact fields of 11 chronic V1-stroke patients, and in 8 visually intact controls. Saccade accuracy was relatively normal in all cases. Stroke patients also had normal PFR in their intact fields, but no PFR in their blind fields. Thus, V1 damage did not spare the unconscious visual processing necessary for automatic, post-saccadic smooth eye movements. Importantly, visual training that recovered motion perception in the blind field did not restore the PFR, suggesting a clear dissociation between pathways mediating perceptual restoration and automatic actions in the V1-damaged visual system.

Morphological evidence for multiple distinct channels of corticogeniculate feedback originating in mid-level extrastriate visual areas of the ferret.

Complementary reciprocal feedforward and feedback circuits connecting the visual thalamus with the visual cortex are essential for visual perception. These circuits predominantly connect primary and secondary visual cortex with the dorsal lateral geniculate nucleus (LGN). Although there are direct geniculocortical inputs to extrastriate visual cortex, whether reciprocal corticogeniculate neurons exist in extrastriate cortex is not known. Here we utilized virus-mediated retrograde tracing to reveal the presence of corticogeniculate neurons in three mid-level extrastriate visual cortical areas in ferrets: PMLS, PLLS, and 21a. We observed corticogeniculate neurons in all three extrastriate areas, although the density of virus-labeled corticogeniculate neurons in extrastriate cortex was an order of magnitude less than that in areas 17 and 18. A cluster analysis of morphological metrics quantified following reconstructions of the full dendritic arborizations of virus-labeled corticogeniculate neurons revealed six distinct cell types. Similar corticogeniculate cell types to those observed in areas 17 and 18 were also observed in PMLS, PLLS, and 21a. However, these unique cell types were not equally distributed across the three extrastriate areas. The majority of corticogeniculate neurons per cluster originated in a single area, suggesting unique parallel organizations for corticogeniculate feedback from each extrastriate area to the LGN. Together, our findings demonstrate direct feedback connections from mid-level extrastriate visual cortex to the LGN, supporting complementary reciprocal circuits at multiple processing stages along the visual hierarchy. Importantly, direct reciprocal connections between the LGN and extrastriate cortex, that bypass V1, could provide a substrate for residual vision following V1 damage.

The Superior Colliculus and Amygdala Support Evaluation of Face Trait in Blindsight.

Humans can respond rapidly to viewed expressions of fear, even in the absence of conscious awareness. This is demonstrated using visual masking paradigms in healthy individuals and in patients with cortical blindness due to damage to the primary visual cortex (V1) - so called affective blindsight. Humans have also been shown to implicitly process facial expressions representing important social dimensions. Two major axes, dominance and trustworthiness, are proposed to characterize the social dimensions of face evaluation. The processing of both types of implicit stimuli is believed to occur via similar subcortical pathways involving the amygdala. However, we do not know whether unconscious processing of more subtle expressions of facial traits can occur in blindsight, and if so, how. To test this, we studied 13 patients with unilateral V1 damage and visual field loss. We assessed their ability to detect and discriminate faces that had been manipulated along two orthogonal axes of trustworthiness and dominance to generate five trait levels inside the blind visual field: dominant, submissive, trustworthy, untrustworthy, and neutral. We compared neural activity and functional connectivity in patients classified as blindsight positive or negative for these stimuli. We found that dominant faces were most likely to be detected above chance, with individuals demonstrating unique interactions between performance and face trait. Only patients with blindsight (n = 8) showed significant preference in the superior colliculus and amygdala for face traits in the blind visual field, and a critical functional connection between the amygdala and superior colliculus in the damaged hemisphere. We also found a significant correlation between behavioral performance and fMRI activity in the amygdala and lateral geniculate nucleus across all participants. Our findings confirm that affective blindsight involving the superior colliculus and amygdala extends to the processing of socially salient but emotionally neutral facial expressions when V1 is damaged. This pathway is distinct from that which supports motion blindsight, as both types of blindsight can exist in the absence of the other with corresponding patterns of residual connectivity.

Functional preservation and enhanced capacity for visual restoration in subacute occipital stroke.

Stroke damage to the primary visual cortex (V1) causes a loss of vision known as hemianopia or cortically-induced blindness. While perimetric visual field improvements can occur spontaneously in the first few months post-stroke, by 6 months post-stroke, the deficit is considered chronic and permanent. Despite evidence from sensorimotor stroke showing that early injury responses heighten neuroplastic potential, to date, visual rehabilitation research has focused on patients with chronic cortically-induced blindness. Consequently, little is known about the functional properties of the post-stroke visual system in the subacute period, nor do we know if these properties can be harnessed to enhance visual recovery. Here, for the first time, we show that 'conscious' visual discrimination abilities are often preserved inside subacute, perimetrically-defined blind fields, but they disappear by ∼6 months post-stroke. Complementing this discovery, we now show that training initiated subacutely can recover global motion discrimination and integration, as well as luminance detection perimetry, just as it does in chronic cortically-induced blindness. However, subacute recovery was attained six times faster; it also generalized to deeper, untrained regions of the blind field, and to other (untrained) aspects of motion perception, preventing their degradation upon reaching the chronic period. In contrast, untrained subacutes exhibited spontaneous improvements in luminance detection perimetry, but spontaneous recovery of motion discriminations was never observed. Thus, in cortically-induced blindness, the early post-stroke period appears characterized by gradual-rather than sudden-loss of visual processing. Subacute training stops this degradation, and is far more efficient at eliciting recovery than identical training in the chronic period. Finally, spontaneous visual improvements in subacutes were restricted to luminance detection; discrimination abilities only recovered following deliberate training. Our findings suggest that after V1 damage, rather than waiting for vision to stabilize, early training interventions may be key to maximize the system's potential for recovery.

Dissociation between perception and predictive oculomotor behavior in retrained cortically blind fields

When saccading to a moving peripheral target, smooth pursuit can track the target immediately upon saccade landing, reflecting pre-saccadic motion integration (Gardner and Lisberger, 2001). Similarly, saccades to peripheral, static apertures containing global motion stimuli drive predictive smooth eye movements, called “post-saccadic following responses” (PFR), along the target motion direction immediately following saccade landing (Kwon et al., 2019). PFR persists even when motion disappears in-saccade-flight, indicating that pre-saccadic motion selection initiated the subsequent following response. Here, we asked if this automatic processing persists in 7 cortically blind (CB) patients who sustained V1 damage in adulthood. Patients exhibited normal PFR gain in intact portions of their visual field (0.15±0.08), and the magnitude of PFR gain was negatively correlated with direction integration thresholds (r=−0.54, p=0.01). However, at blind field locations where patients failed to discriminate global motion direction, they exhibited no significant PFR (gain=0.004±0.019). We then asked whether visual training that recovers global motion perception in CB fields (Huxlin et al., 2009), can restore this automatic pre-saccadic processing. The resulting PFR gain was only 0.03±0.09 (t-test: p=0.6104 relative to untrained locations), well below normal (t-test: p=0.03). In summary, peripheral visual discrimination training, which recovers global motion perception in the blind field, does not restore a normal PFR. Such poor automatic pre-processing of motion in retrained CB fields suggests that after V1 damage, neural circuits engaged in the PFR may differ from those mediating conscious motion perception at the same visual field locations.

Altered Sensitivity to Motion of Area MT Neurons Following Long-Term V1 Lesions.

Primates with primary visual cortex (V1) damage often retain residual motion sensitivity, which is hypothesized to be mediated by middle temporal area (MT). MT neurons continue to respond to stimuli shortly after V1 lesions; however, experimental and clinical studies of lesion-induced plasticity have shown that lesion effects can take several months to stabilize. It is unknown what physiological changes occur in MT and whether neural responses persist long after V1 damage. We recorded neuronal responses in MT to moving dot patterns in adult marmoset monkeys 6-12months after unilateral V1 lesions. In contrast to results obtained shortly after V1 lesions, we found that fewer MT neurons were direction selective, including neurons expected to still receive projections from remaining parts of V1. The firing rates of most cells increased with increases in motion strength, regardless of stimulus direction. Furthermore, firing rates were higher and more variable than in control MT cells. To test whether these observations could be mechanistically explained by underlying changes in neural circuitry, we created a network model of MT. We found that a local imbalance of inhibition and excitation explained the observed firing rate changes. These results provide the first insights into functional implications of long-term plasticity in MT following V1 lesions.

Blindsight relies on a functional connection between hMT+ and the lateral geniculate nucleus, not the pulvinar.

When the primary visual cortex (V1) is damaged, the principal visual pathway is lost, causing a loss of vision in the opposite visual field. While conscious vision is impaired, patients can still respond to certain images; this is known as ‘blindsight’. Recently, a direct anatomical connection between the lateral geniculate nucleus (LGN) and human motion area hMT+ has been implicated in blindsight. However, a functional connection between these structures has not been demonstrated. We quantified functional MRI responses to motion in 14 patients with unilateral V1 damage (with and without blindsight). Patients with blindsight showed significant activity and a preserved sensitivity to speed in motion area hMT+, which was absent in patients without blindsight. We then compared functional connectivity between motion area hMT+ and a number of structures implicated in blindsight, including the ventral pulvinar. Only patients with blindsight showed an intact functional connection with the LGN but not the other structures, supporting a specific functional role for the LGN in blindsight.

Action blindsight and antipointing in a hemianopic patient

Blindsight refers to the observation of residual visual abilities in the hemianopic field of patients without a functional V1. Given the within- and between-subject variability in the preserved abilities and the phenomenal experience of blindsight patients, the fine-grained description of the phenomenon is still debated. Here we tested a patient with established “perceptual” and “attentional” blindsight (c.f. Danckert and Rossetti, 2005). Using a pointing paradigm patient MS, who suffers from a complete left homonymous hemianopia, showed clear above chance manual localisation of ‘unseen’ targets. In addition, target presentations in his blind field led MS, on occasion, to spontaneous responses towards his sighted field. Structural and functional magnetic resonance imaging was conducted to evaluate the magnitude of V1 damage. Results revealed the presence of a calcarine sulcus in both hemispheres, yet his right V1 is reduced, structurally disconnected and shows no fMRI response to visual stimuli. Thus, visual stimulation of his blind field can lead to “action blindsight” and spontaneous antipointing, in absence of a functional right V1. With respect to the antipointing, we suggest that MS may have registered the stimulation and subsequently presumes it must have been in his intact half field.

Feature-based attention potentiates recovery of fine direction discrimination in cortically blind patients

Training chronic, cortically-blind (CB) patients on a coarse [left-right] direction discrimination and integration (CDDI) task recovers performance on this task at trained, blind field locations. However, fine direction difference (FDD) thresholds remain elevated at these locations, limiting the usefulness of recovered vision in daily life. Here, we asked if this FDD impairment can be overcome by training CB subjects with endogenous, feature-based attention (FBA) cues. Ten CB subjects were recruited and trained on CDDI and FDD with an FBA cue or FDD with a neutral cue. After completion of each training protocol, FDD thresholds were re-measured with both neutral and FBA cues at trained, blind-field locations and at corresponding, intact-field locations. In intact portions of the visual field, FDD thresholds were lower when tested with FBA than neutral cues. Training subjects in the blind field on the CDDI task improved FDD performance to the point that a threshold could be measured, but these locations remained impaired relative to the intact field. FDD training with neutral cues resulted in better blind field FDD thresholds than CDDI training, but thresholds remained impaired relative to intact field levels, regardless of testing cue condition. Importantly, training FDD in the blind field with FBA lowered FDD thresholds relative to CDDI training, and allowed the blind field to reach thresholds similar to the intact field, even when FBA trained subjects were tested with a neutral rather than FBA cue. Finally, FDD training appeared to also recover normal integration thresholds at trained, blind-field locations, providing an interesting double dissociation with respect to CDDI training. In summary, mechanisms governing FBA appear to function normally in both intact and impaired regions of the visual field following V1 damage. Our results mark the first time that FDD thresholds in CB fields have been seen to reach intact field levels of performance. Moreover, FBA can be leveraged during visual training to recover normal, fine direction discrimination and integration performance at trained, blind-field locations, potentiating visual recovery of more complex and precise aspects of motion perception in cortically-blinded fields.

Pre-training cortical activity preserved after V1 damage predicts sites of training-induced visual recovery

Pre-training cortical activity preserved after V1 damage predicts sites of training-induced visual recovery