Plasticity, and Its Limits, in Adult Human Primary Visual Cortex

There is an ongoing debate about whether adult human primary visual cortex (V1) is capable of large-scale cortical reorganization in response to bilateral retinal lesions. Animal models suggest that the visual neural circuitry maintains some plasticity through adulthood, and there are also a few human imaging studies in support this notion. However, the interpretation of these data has been brought into question, because there are factors besides cortical reorganization, such as the presence of sampling bias and/or the unmasking of task-dependent feedback signals from higher level visual areas, that could also explain the results. How reasonable would it be to accept that adult human V1 does not reorganize itself in the face of disease? Here, we discuss new evidence for the hypothesis that adult human V1 is not as capable of reorganization as in animals and juveniles, because in adult humans, cortical reorganization would come with costs that outweigh its benefits. These costs are likely functional and visible in recent experiments on adaptation — a rapid, short-term form of neural plasticity — where they prevent reorganization from being sustained over the long term

Preserved retinotopic brain connectivity in macular degeneration

PURPOSE: The eye disease macular degeneration (MD) is a leading cause of blindness worldwide. There is no cure for MD, but several promising treatments aimed at restoring vision at the level of the retina are currently under investigation. These treatments assume that the patient's brain can still process appropriately the retinal input once it is restored, but whether this assumption is correct has yet to be determined. METHODS: We used functional magnetic resonance imaging (fMRI) and connective field modelling to determine whether the functional connectivity between the input-deprived portions of primary visual cortex (V1) and early extrastriate areas (V2/3) is still retinotopically organised. Specifically, in both patients with juvenile macular degeneration and age-matched controls with simulated retinal lesions, we assessed the extent to which the V1-referred connective fields of extrastriate voxels, as estimated on the basis of spontaneous fMRI signal fluctuations, adhered to retinotopic organisation. RESULTS: We found that functional connectivity between the input-deprived portions of visual areas V1 and extrastriate cortex is still largely retinotopically organised in MD, although on average less so than in controls. Patients with stable fixation exhibited normal retinotopic connectivity, however, suggesting that for the patients with unstable fixation, eye-movements resulted in spurious, homogeneous signal modulations across the entire input-deprived cortex, which would have hampered our ability to assess their spatial structure of connectivity. CONCLUSIONS: Despite the prolonged loss of visual input due to MD, the cortico-cortical connections of input-deprived visual cortex remain largely intact. This suggests that the restoration of sight in macular degeneration can rely on a largely unchanged retinotopic representation in early visual cortex following loss of central retinal function

Human colour perception changes between seasons

Humans identify four 'unique hues' - blue, green, yellow and red - that do not appear to contain mixtures of other colours. Unique yellow (UY) is particularly interesting because it is stable across large populations: participants reliably set a monochromatic light to a stereotypical wavelength. Individual variability in the ratio of L- and M-cones in the retina, and effects of ageing, both impact unique green (UG) settings [1,2], but cannot predict the relatively small inter-individual differences in UY [2,3]. The stability of UY may arise because it is set by the environment rather than retinal physiology. Support for this idea comes from studies of long-term, artificial chromatic adaptation [4,5], but there is no evidence for this process in natural settings. Here, we measured 67 participants in York (UK) in both the winter and summer, and found a significant seasonal change in UY settings. In comparison, Rayleigh colour matches that would not be expected to exhibit environmentally driven changes were found to be constant. The seasonal shift in UY settings is consistent with a model that reweights L- and M-cone inputs into a perceptual opponent colour channel after a small, seasonally-driven change in mean L:M cone activity

An enhanced role for right hV5/MT+ in the analysis of motion in the contra- and ipsi-lateral visual hemi-fields

Previous experiments have demonstrated that transcranial magnetic stimulation (TMS) of human V5/MT+, in either the left or right cerebral hemisphere, can induce deficits in visual motion perception in their respective contra- and ipsi-lateral visual hemi-fields. However, motion deficits in the ipsi-lateral hemi-field are greater when TMS is applied to V5/MT + in the right hemisphere relative to the left hemisphere. One possible explanation for this asymmetry might lie in differential stimulation of sub-divisions within V5/MT + across the two hemispheres. V5/MT + has two major sub-divisions; MT/TO-1 and MST/TO-2, the latter area contains neurons with large receptive fields (RFs) that extend up to 15° further into the ipsi-lateral hemi-field than the former. We wanted to examine whether applying TMS to MT/TO-1 and MST/TO-2 separately could explain the previously reported functional asymmetries for ipsi-lateral motion processing in V5/MT + across right and left cerebral hemispheres. MT/TO-1 and MST/TO-2 were identified in seven subjects using fMRI localisers. In psychophysical experiments subjects identified the translational direction (up/down) of coherently moving dots presented in either the left or right visual field whilst repetitive TMS (25 Hz; 70%) was applied synchronously with stimulus presentation. Application of TMS to MT/TO-1 and MST/TO-2 in the right hemisphere affected translational direction discrimination in both contra-lateral and ipsi-lateral visual fields. In contrast, deficits of motion perception following application of TMS to MT/TO-1 and MST/TO-2 in the left hemisphere were restricted to the contra-lateral visual field. This result suggests an enhanced role for the right hemisphere in processing translational motion across the full visual field

A Direct Demonstration of Functional Differences between Subdivisions of Human V5/MT

Two subdivisions of human V5/MT+: one located posteriorly (MT/TO-1) and the other more anteriorly (MST/TO-2) were identified in human participants using functional magnetic resonance imaging on the basis of their representations of the ipsilateral versus contralateral visual field. These subdivisions were then targeted for disruption by the application of repetitive transcranial magnetic stimulation (rTMS). The rTMS was delivered to cortical areas while participants performed direction discrimination tasks involving 3 different types of moving stimuli defined by the translational, radial, or rotational motion of dot patterns. For translational motion, performance was significantly reduced relative to baseline when rTMS was applied to both MT/TO-1 and MST/TO-2. For radial motion, there was a differential effect between MT/TO-1 and MST/TO-2, with only disruption of the latter area affecting performance. The rTMS failed to reveal a complete dissociation between MT/TO-1 and MST/TO-2 in terms of their contribution to the perception of rotational motion. On the basis of these results, MT/TO-1 and MST/TO-2 appear to be functionally distinct subdivisions of hV5/MT+. While both areas appear to be implicated in the processing of translational motion, only the anterior region (MST/TO-2) makes a causal contribution to the perception of radial motion

An Orientation Dependent Size Illusion Is Underpinned by Processing in the Extrastriate Visual Area, LO1

We use the simple, but prominent Helmholtz’s squares illusion in which a vertically striped square appears wider than a horizontally striped square of identical physical dimensions to determine whether functional magnetic resonance imaging (fMRI) BOLD responses in V1 underpin illusions of size. We report that these simple stimuli which differ in only one parameter, orientation, to which V1 neurons are highly selective elicited activity in V1 that followed their physical, not perceived size. To further probe the role of V1 in the illusion and investigate plausible extrastriate visual areas responsible for eliciting the Helmholtz squares illusion, we performed a follow-up transcranial magnetic stimulation (TMS) experiment in which we compared perceptual judgments about the aspect ratio of perceptually identical Helmholtz squares when no TMS was applied against selective stimulation of V1, LO1, or LO2. In agreement with fMRI results, we report that TMS of area V1 does not compromise the strength of the illusion. Only stimulation of area LO1, and not LO2, compromised significantly the strength of the illusion, consistent with previous research that LO1 plays a role in the processing of orientation information. These results demonstrate the involvement of a specific extrastriate area in an illusory percept of size

Morphometric analyses of the visual pathways in macular degeneration

Introduction. Macular degeneration (MD) causes central visual field loss. When field defects occur in both eyes and overlap, parts of the visual pathways are no longer stimulated. Previous reports have shown that this affects the grey matter of the primary visual cortex, but possible effects on the preceding visual pathway structures have not been fully established. Method. In this multicentre study, we used high-resolution anatomical magnetic resonance imaging and voxel-based morphometry to investigate the visual pathway structures up to the primary visual cortex of patients with age-related macular degeneration (AMD) and juvenile macular degeneration (JMD). Results. Compared to age-matched healthy controls, in patients with JMD we found volumetric reductions in the optic nerves, the chiasm, the lateral geniculate bodies, the optic radiations and the visual cortex. In patients with AMD we found volumetric reductions in the lateral geniculate bodies, the optic radiations and the visual cortex. An unexpected finding was that AMD, but not JMD, was associated with a reduction in frontal white matter volume. Conclusion. MD is associated with degeneration of structures along the visual pathways. A reduction in frontal white matter volume only present in the AMD patients may constitute a neural correlate of previously reported association between AMD and mild cognitive impairment. Keywords: macular degeneration - visual pathway - visual field - voxel-based morphometryComment: appears in Cortex (2013

Multivariate Patterns in the Human Object-Processing Pathway Reveal a Shift from Retinotopic to Shape Curvature Representations in Lateral Occipital Areas, LO-1 and LO-2

Representations in early visual areas are organized on the basis of retinotopy, but this organizational principle appears to lose prominence in the extrastriate cortex. Nevertheless, an extrastriate region, such as the shape-selective lateral occipital cortex (LO), must still base its activation on the responses from earlier retinotopic visual areas, implying that a transition from retinotopic to “functional” organizations should exist. We hypothesized that such a transition may lie in LO-1 or LO-2, two visual areas lying between retinotopically defined V3d and functionally defined LO. Using a rapid event-related fMRI paradigm, we measured neural similarity in 12 human participants between pairs of stimuli differing along dimensions of shape exemplar and shape complexity within both retinotopically and functionally defined visual areas. These neural similarity measures were then compared with low-level and more abstract (curvature-based) measures of stimulus similarity. We found that low-level, but not abstract, stimulus measures predicted V1–V3 responses, whereas the converse was true for LO, a double dissociation. Critically, abstract stimulus measures were most predictive of responses within LO-2, akin to LO, whereas both low-level and abstract measures were predictive for responses within LO-1, perhaps indicating a transitional point between those two organizational principles. Similar transitions to abstract representations were not observed in the more ventral stream passing through V4 and VO-1/2. The transition we observed in LO-1 and LO-2 demonstrates that a more “abstracted” representation, typically considered the preserve of “category-selective” extrastriate cortex, can nevertheless emerge in retinotopic regions

Neural markers of suppression in impaired binocular vision

Even after conventional patching treatment, individuals with a history of amblyopia typically lack good stereo vision. This is often attributed to atypical suppression between the eyes, yet the specific mechanism is still unclear. Guided by computational models of binocular vision, we tested explicit predictions about how neural responses to contrast might differ in individuals with impaired binocular vision. Participants with a history of amblyopia (N = 25), and control participants with typical visual development (N = 19) took part in the study. Neural responses to different combinations of contrast in the left and right eyes, were measured using both electroencephalography (EEG) and functional magnetic resonance imaging (fMRI). Stimuli were sinusoidal gratings with a spatial frequency of 3c/deg, flickering at 4 Hz. In the fMRI experiment, we also ran population receptive field and retinotopic mapping sequences, and a phase-encoded localiser stimulus, to identify voxels in primary visual cortex (V1) sensitive to the main stimulus. Neural responses in both modalities increased monotonically with stimulus contrast. When measured with EEG, responses were attenuated in the weaker eye, consistent with a fixed tonic suppression of that eye. When measured with fMRI, a low contrast stimulus in the weaker eye substantially reduced the response to a high contrast stimulus in the stronger eye. This effect was stronger than when the stimulus-eye pairings were reversed, consistent with unbalanced dynamic suppression between the eyes. Measuring neural responses using different methods leads to different conclusions about visual differences in individuals with impaired binocular vision. Both of the atypical suppression effects may relate to binocular perceptual deficits, e.g. in stereopsis, and we anticipate that these measures could be informative for monitoring the progress of treatments aimed at recovering binocular vision

On the role of suppression in spatial attention : evidence from negative BOLD in human subcortical and cortical structures

There is clear evidence that spatial attention increases neural responses to attended stimuli in extrastriate visual areas and, to a lesser degree, in earlier visual areas. Other evidence shows that neurons representing unattended locations can also be suppressed. However, the extent to which enhancement and suppression is observed, their stimulus dependence, and the stages of the visual system at which they are expressed remains poorly understood. Using fMRI we set out to characterize both the task and stimulus dependence of neural responses in the lateral geniculate nucleus (LGN), primary visual cortex (V1), and visual motion area (V5) in humans to determine where suppressive and facilitatory effects of spatial attention are expressed. Subjects viewed a lateralized drifting grating stimulus, presented at multiple stimulus contrasts, and performed one of three tasks designed to alter the spatial location of their attention. In retinotopic representations of the stimulus location, we observed increasing attention-dependent facilitation and decreasing dependence on stimulus contrast moving up the visual hierarchy from the LGN to V5. However, in the representations of unattended locations of the LGN and V1, we observed suppression, which was not significantly dependent on the attended stimulus contrast. These suppressive effects were also found in the pulvinar, which has been frequently associated with attention. We provide evidence, therefore, for a spatially selective suppressive mechanism that acts at a subcortical level