Lesion Of Primary Visual Cortex Research Articles

A clinico-anatomical dissection of the magnocellular and parvocellular pathways in a patient with the Riddoch syndrome

Key messageThe Riddoch syndrome is thought to be caused by damage to the primary visual cortex (V1), usually following a vascular event. This study shows that damage to the anatomical input to V1, i.e., the optic radiations, can result in selective visual deficits that mimic the Riddoch syndrome. The results also highlight the differential susceptibility of the magnocellular and parvocellular visual systems to injury. Overall, this study offers new insights that will improve our understanding of the impact of brain injury and neurosurgery on the visual pathways.The Riddoch syndrome, characterised by the ability to perceive, consciously, moving visual stimuli but not static ones, has been associated with lesions of primary visual cortex (V1). We present here the case of patient YL who, after a tumour resection surgery that spared his V1, nevertheless showed symptoms of the Riddoch syndrome. Based on our testing, we postulated that the magnocellular (M) and parvocellular (P) inputs to his V1 may be differentially affected. In a first experiment, YL was presented with static and moving checkerboards in his blind field while undergoing multimodal magnetic resonance imaging (MRI), including structural, functional, and diffusion, acquired at 3 T. In a second experiment, we assessed YL’s neural responses to M and P visual stimuli using psychophysics and high-resolution fMRI acquired at 7 T. YL’s optic radiations were partially damaged but not severed. We found extensive activity in his visual cortex for moving, but not static, visual stimuli, while our psychophysical tests revealed that only low-spatial frequency moving checkerboards were perceived. High-resolution fMRI revealed strong responses in YL's V1 to M stimuli and very weak ones to P stimuli, indicating a functional P lesion affecting V1. In addition, YL frequently reported seeing moving stimuli and discriminating their direction of motion in the absence of visual stimulation, suggesting that he was experiencing visual hallucinations. Overall, this study highlights the possibility of a selective loss of P inputs to V1 resulting in the Riddoch syndrome and in hallucinations of visual motion.

Vision: A Product of a Society of Independent Experts

A lesion of primary visual cortex, V1, can result in the perceived size of objects varying with the size of their retinal image. A new study shows that the pregrasp span of the hand of an individual with such a lesion remains tuned to the object's true size, providing evidence for separate representations mediating perceptual appearance and motor interactions.

Preserved extrastriate visual network in a monkey with substantial, naturally occurring damage to primary visual cortex.

Lesions of primary visual cortex (V1) lead to loss of conscious visual perception with significant impact on human patients. Understanding the neural consequences of such damage may aid the development of rehabilitation methods. In this rare case of a Rhesus macaque (monkey S), likely born without V1, the animal's in-group behaviour was unremarkable, but visual task training was impaired. With multi-modal magnetic resonance imaging, visual structures outside of the lesion appeared normal. Visual stimulation under anaesthesia with checkerboards activated lateral geniculate nucleus of monkey S, while full-field moving dots activated pulvinar. Visual cortical activation was sparse but included face patches. Consistently across lesion and control monkeys, functional connectivity analysis revealed an intact network of bilateral dorsal visual areas temporally correlated with V5/MT activation, even without V1. Despite robust subcortical responses to visual stimulation, we found little evidence for strengthened subcortical input to V5/MT supporting residual visual function or blindsight-like phenomena.

Unexplained Progressive Visual Field Loss in the Presence of Normal Retinotopic Maps.

Lesions of primary visual cortex or its primary inputs typically result in retinotopically localized scotomas. Here we present an individual with unexplained visual field loss and deficits in visual perception in the absence of structural damage to the early visual pathway or lesions in visual cortex. The subject, monocular from an early age, underwent repeated perimetry tests over 8 years demonstrating severe anopia of the lower hemifield, and a clockwise progression of the loss through her upper left visual field. Her visual impairment was evident in a number of standardized tests and psychophysics, especially in tasks assessing spatial integration using illusory contours. However, her intellectual ability was intact and her performance in some other tasks assessing color vision or object detection in scenes was normal. We employed functional magnetic resonance imaging (fMRI), electroretinography and visually evoked potentials. Surprisingly, in contrast to the participant’s severe anopia, we found no evidence of abnormal function of her early visual pathways. Specifically, we performed retinotopic mapping using population receptive field (pRF) analysis to map the functional organization of visual cortex in the anopic participant and three control participants on two occasions three and a half years apart. Despite the behavioral visual field loss, her retinotopic maps and pRF parameters in visual areas V1–V3 were qualitatively normal. Further behavioral experiments confirmed that this discrepancy was not trivially explained by the difference between stimuli used for retinotopic mapping and perimetry. Structural T1 scans were normal at both time points, and volumetric analysis of white and gray matter tissue on the segmented T1 volumes did not reveal any abnormalities or deterioration over time. Our findings suggest that normal functional organization of early visual cortex without evident structural damage to the early visual pathway as disclosed by the techniques employed in this study does not necessarily guarantee conscious perception across the visual field.

Unseen fearful faces facilitate visual discrimination in the intact field

Implicit visual processing of emotional stimuli has been widely investigated since the classical studies on affective blindsight, in which patients with primary visual cortex lesions showed discriminatory abilities for unseen emotional stimuli in the absence of awareness. In addition, more recent evidence from hemianopic patients showed response facilitation and enhanced early visual encoding of seen faces, only when fearful faces were presented concurrently in the blind field. However, it is still unclear whether unseen fearful faces specifically facilitate visual processing of facial stimuli, or whether the facilitatory effect constitutes an adaptive mechanism prioritizing the visual analysis of any stimulus. To test this question, we tested a group of hemianopic patients who perform at chance in forced-choice discrimination tasks of stimuli in the blind field. Patients performed a go/no-go task in which they were asked to discriminate simple visual stimuli (Gabor patches) presented in their intact field, while fearful, happy and neutral faces were concurrently presented in the blind field. The results showed a reduction in response times to the Gabor patches presented in the intact field, when fearful faces were concurrently presented in the blind field, but only in patients with left hemispheric lesions. No facilitatory effect was observed in patients with right hemispheric lesions. These results suggest that unseen fearful faces are implicitly processed and can facilitate the visual analysis of simple visual stimuli presented in the intact field. This effect might be subserved by activity in the spared colliculo-amygdala-extrastriate pathway that promotes efficient visual analysis of the environment and rapid execution of defensive responses. Such a facilitation is observed only in patients with left lesions, favouring the hypothesis that the right hemisphere mediates implicit visual processing of fear signals.

Neuronal degeneration in the dorsal lateral geniculate nucleus following lesions of primary visual cortex: comparison of young adult and geriatric marmoset monkeys.

Neuronal loss in the lateral geniculate nucleus (LGN) is a consequence of lesions of the primary visual cortex (V1). Despite the importance of this phenomenon in understanding the residual capacities of the primate visual system following V1 damage, few quantitative studies are available, and the effect of age at the time of lesion remains unknown. We compared the volume, neuronal number, and neuronal density in the LGN, 6-21months after unilateral V1 lesions in marmoset monkeys. Stereological sampling techniques and neuronal nuclei (NeuN) staining were used to assess the effects of similar-sized lesions in adult (2-4years) and geriatric (10-14years) animals. We found that lesions involving the opercular and caudal calcarine parts of V1 caused robust loss of neurons in topographically corresponding regions of the ipsilateral LGN (lesion projection zones), concomitant with a substantial reduction in the volume of this nucleus. Neuronal density was markedly reduced in the lesion projection zones, relative to the corresponding regions of the contralateral LGN, or the LGN in non-lesioned animals. Moreover, the percentage decrease in neuronal density within the lesion projection zones was significantly greater in the geriatric group, compared with the adult groups. The volume and neuronal density in the contralateral LGN of lesioned adult and geriatric marmosets were similar to those in non-lesioned animals. These results show that the primate LGN becomes more vulnerable to degeneration with advancing age. However, even in geriatric primates there is a population of LGN neurons which survives degeneration, and which could play a role in blindsight.

Probing Human Visual Deficits with Functional Magnetic Resonance Imaging.

Much remains to be understood about visual system malfunction following injury. The resulting deficits range from dense, visual field scotomas to mild dysfunction of visual perception. Despite the predictive value of anatomical localization studies, much patient-to-patient variability remains regarding (a) perceptual abilities following injury and (b) the capacity of individual patients for visual rehabilitation. Visual field perimetry is used to characterize the visual field deficits that result from visual system injury. However, standard perimetry mapping does not always precisely correspond to underlying anatomical or functional deficits. Functional magnetic resonance imaging can be used to probe the function of surviving visual circuits, allowing us to classify better how the pattern of injury relates to residual visual perception. Identifying pathways that are potentially modifiable by training may guide the development of improved strategies for visual rehabilitation. This review discusses primary visual cortex lesions, which cause dense contralateral scotomas.

Correlated activity of cortical neurons survives extensive removal of feedforward sensory input.

A fundamental property of brain function is that the spiking activity of cortical neurons is variable and that some of this variability is correlated between neurons. Correlated activity not due to the stimulus arises from shared input but the neuronal circuit mechanisms that result in these noise correlations are not fully understood. Here we tested in the visual system if correlated variability in mid-level area V4 of visual cortex is altered following extensive lesions of primary visual cortex (V1). To this end we recorded longitudinally the neuronal correlations in area V4 of two behaving macaque monkeys before and after a V1 lesion while the monkeys fixated a grey screen. We found that the correlations of neuronal activity survived the lesions in both monkeys. In one monkey, the correlation of multi-unit spiking signals was strongly increased in the first week post-lesion, while in the second monkey, correlated activity was slightly increased, but not greater than some week-by-week fluctuations observed. The typical drop-off of inter-neuronal correlations with cortical distance was preserved after the lesion. Therefore, as V4 noise correlations remain without feedforward input from V1, these results suggest instead that local and/or feedback input seem to be necessary for correlated activity.

Preservation of Vision by the Pulvinar following Early-Life Primary Visual Cortex Lesions

Conscious vision is believed to depend upon an intact primary visual cortex (V1), although injury in early life is often accompanied by the preservation of visual capacity, unlike in adulthood. The middle temporal area (MT) receives input from the retinorecipient koniocellular layers of the lateral geniculate nucleus (LGN) and the more recently described medial subdivision of the inferior pulvinar (PIm) of the thalamus, pathways that potentially contribute to preservation of vision after early damage to V1. We examined the potential of these pathways to the long-term preservation of vision after permanent lesions of primate V1 in early and adult life by using a combination of neural tracing and diffusion MRI. We show that early-life V1 lesions lead to less pruning of the retina-pulvinar-MT pathway than is observed in control or adult lesion animals. These findings suggest that sustained visual input through the pulvinar to MT following a lesion of V1 in early life has the capacity to afford improved visual outcomes.

Lesion of Primary Visual Cortex in Monkey Impairs the Inhibitory but Not the Facilitatory Cueing Effect on Saccade

Prior visual stimulus presentation induces immediate facilitation and subsequent inhibition of orienting to an ensuing target at the same location. Recent studies revealed that the superior colliculus (SC) is involved in these facilitatory and inhibitory cueing effects on saccade; however, as the SC receives inputs both directly from the retina (retino-tectal pathway) and indirectly from visual cortices (geniculostriate pathway), it is unclear which visual pathway contributes to the effects. We investigated this issue using monkeys with lesions in the primary visual cortex (V1), thus depriving the SC of the geniculostriate pathway and leaving the retino-tectal pathway intact. We found that the inhibitory cueing effect was selectively impaired and the facilitatory cueing effect was spared after V1 lesions. The results suggest that the geniculostriate and the retino-tectal pathways are differentially involved in the generation of cueing effects on saccade: The former is critically involved in the inhibitory effect whereas the latter alone can induce the facilitatory effect. The results provide the first direct evidence for the involvement of the geniculostriate pathway in the inhibitory cueing effect and further imply that the more recent evolution of the geniculostriate pathway in higher mammals improves the efficiency of visual search by inhibiting orienting to a previously attended location.

The primary visual cortex, and feedback to it, are not necessary for conscious vision

A compelling single case report of visual awareness (visual qualia) without primary visual cortex would be sufficient to refute the hypothesis that the primary visual cortex and the back-projections to it are necessary for conscious visual experience. In a previous study, we emphasized the presence of crude visual awareness in Patient G.Y., with a lesion of the primary visual cortex, who is aware of, and able to discriminate, fast-moving visual stimuli presented to his blind field. The visual nature of Patient G.Y.'s blind field experience has since been questioned and it has been suggested that the special circumstances of repeated testing over decades may have altered Patient G.Y.'s visual pathways. We therefore sought new evidence of visual awareness without primary visual cortex in patients for whom such considerations do not apply. Three patients with hemianopic field defects (Patient G.N. and Patient F.B. with MRI confirmed primary visual cortex lesions, Patient C.G. with an inferred lesion) underwent detailed psychophysical testing in their blind fields. Visual stimuli were presented at different velocities and contrasts in two- and four-direction discrimination experiments and the direction of motion and awareness reported using a forced-choice paradigm. Detailed verbal reports were also obtained of the nature of the blind field experience with comparison of the drawings of the stimulus presented in the blind and intact fields, where possible. All three patients reported visual awareness in their blind fields. Visual awareness was significantly more likely when a moving stimulus was present compared to no stimulus catch trials (P < 0.01 for each subject). Psychophysical performance in Patient F.B. and Patient G.N. was consistent with the Riddoch syndrome, with higher levels of visual awareness for moving compared to static stimuli (P < 0.001) and intact direction discrimination (P < 0.0001 for two- and four-direction experiments). Although the blind field experience of all three subjects was degraded, it was clearly visual in nature. We conclude that the primary visual cortex or back-projections to it are not necessary for visual awareness.

Guidance of gaze based on color saliency in monkeys with unilateral lesion of primary visual cortex

Guidance of gaze based on color saliency in monkeys with unilateral lesion of primary visual cortex

Role of different salient features in guiding gaze of monkeys with unilateral lesion of primary visual cortex

Role of different salient features in guiding gaze of monkeys with unilateral lesion of primary visual cortex

Reflections on blindsight: Neuroimaging and behavioural explorations clarify a case of reversed localisation in the blind field of a patient with hemianopia.

Blindsight refers to residual visual abilities of patients with primary visual cortex lesions. Most of this research uses single case studies, most famously patient GY. We examined a patient (DC) after surgical resection of V1 who demonstrated robust but reversed blind field target localisation, mislocalising midline blind field targets to the periphery and vice versa. This pattern was reliable across multiple sessions and was not because of extraocular light scatter. We then used functional magnetic resonance imaging to examine neural responses to blind field motion stimuli with no evidence of motion-selective activation in DC's extrastriate cortex in the damaged hemisphere, in stark contrast to GY who showed robust bilateral activation in response to blind field stimuli. This suggests that DC's blind field performance may not represent true blindsight. Follow-up testing with the target--background contrast reversed (i.e., black targets/white background), eliminated DC's reversed localisation, strongly suggesting that she was employing an unusual decision criterion based on intraocular light scatter. DC's failure to demonstrate true blindsight may be related to the age at which she acquired her lesion--much later in life than GY.

Saliency-based guidance of gaze in monkeys with unilateral lesion of primary visual cortex

Saliency-based guidance of gaze in monkeys with unilateral lesion of primary visual cortex

Investigation of spontaneous saccades based on the saliency model in monkeys with unilateral lesion of primary visual cortex

Investigation of spontaneous saccades based on the saliency model in monkeys with unilateral lesion of primary visual cortex

Visually guided eye movements based on color saliency in monkeys with unilateral lesion of primary visual cortex

Visually guided eye movements based on color saliency in monkeys with unilateral lesion of primary visual cortex

The role of retinotectal pathway for saccade control after the lesion of primary visual cortex

The standard approach to brain stimulation in stroke is based on the premise that ipsilesional M1 (iM1) is important for motor function of the paretic upper limb, while contralesional cortices compete with iM1. Therefore, the approach typically advocates facilitating iM1 and/or inhibiting contralesional M1 (cM1). But, this approach fails to elicit much improvement in severely affected patients, who on account of extensive damage to ipsilesional pathways, cannot rely on iM1. These patients are believed to instead rely on the undamaged cortices, especially the contralesional dorsal premotor cortex (cPMd), for support of function of the paretic limb. Here, we tested for the first time whether facilitation of cPMd could improve paretic limb function in severely affected patients, and if a cut-off could be identified to separate responders to cPMd from responders to the standard approach to stimulation.In a randomized, sham-controlled crossover study, fifteen patients received the standard approach of stimulation involving inhibition of cM1 and a new approach involving facilitation of cPMd using repetitive transcranial magnetic stimulation (rTMS). Patients also received rTMS to control areas. At baseline, impairment [Upper Extremity Fugl-Meyer (UEFMPROXIMAL, max = 36)] and damage to pathways [fractional anisotropy (FA)] was measured. We measured changes in time to perform proximal paretic limb reaching, and neurophysiology using TMS.Facilitation of cPMd generated more improvement in severely affected patients, who had experienced greater damage and impairment than a cut-off value of FA (0.5) and UEFMPROXIMAL (26–28). The standard approach instead generated more improvement in mildly affected patients. Responders to cPMd showed alleviation of interhemispheric competition imposed on iM1, while responders to the standard approach showed gains in ipsilesional excitability in association with improvement.A preliminary cut-off level of severity separated responders for standard approach vs. facilitation of cPMd.Cut-offs identified here could help select candidates for tailored stimulation in future studies so patients in all ranges of severity could potentially achieve maximum benefit in function of the paretic upper limb.

Visually Driven Activation in Macaque Areas V2 and V3 without Input from the Primary Visual Cortex

Creating focal lesions in primary visual cortex (V1) provides an opportunity to study the role of extra-geniculo-striate pathways for activating extrastriate visual cortex. Previous studies have shown that more than 95% of neurons in macaque area V2 and V3 stop firing after reversibly cooling V1 [1], [2], [3]. However, no studies on long term recovery in areas V2, V3 following permanent V1 lesions have been reported in the macaque. Here we use macaque fMRI to study area V2, V3 activity patterns from 1 to 22 months after lesioning area V1. We find that visually driven BOLD responses persist inside the V1-lesion projection zones (LPZ) of areas V2 and V3, but are reduced in strength by ∼70%, on average, compared to pre-lesion levels. Monitoring the LPZ activity over time starting one month following the V1 lesion did not reveal systematic changes in BOLD signal amplitude. Surprisingly, the retinotopic organization inside the LPZ of areas V2, V3 remained similar to that of the non-lesioned hemisphere, suggesting that LPZ activation in V2, V3 is not the result of input arising from nearby (non-lesioned) V1 cortex. Electrophysiology recordings of multi-unit activity corroborated the BOLD observations: visually driven multi-unit responses could be elicited inside the V2 LPZ, even when the visual stimulus was entirely contained within the scotoma induced by the V1 lesion. Restricting the stimulus to the intact visual hemi-field produced no significant BOLD modulation inside the V2, V3 LPZs. We conclude that the observed activity patterns are largely mediated by parallel, V1-bypassing, subcortical pathways that can activate areas V2 and V3 in the absence of V1 input. Such pathways may contribute to the behavioral phenomenon of blindsight.

Saliency-based guidance of eye movements in monkeys with unilateral lesion of primary visual cortex

Saliency-based guidance of eye movements in monkeys with unilateral lesion of primary visual cortex