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Changes in connectivity after visual cortical brain damage underlie altered visual function

The full extent of the brains ability to compensate for damage or changed experience is yet to be established. One question particularly important for evaluating and understanding rehabilitation following brain damage is whether recovery involves new and aberrant neural connections or whether any change in function is due to the functional recruitment of existing pathways, or both. Blindsight, a condition in which subjects with complete destruction of part of striate cortex (V1) retain extensive visual capacities within the clinically blind field, is an excellent example of altered visual function. Since the main pathway to the visual cortex is destroyed, the spared or recovered visual ability must arise from either an existing alternative pathway, or the formation of a new pathway. Using diffusion-weighted MRI, we show that both controls and blindsight subject GY, whose left V1 is destroyed, show an ipsilateral pathway between LGN (lateral geniculate nucleus) and human motion area MT+/V5 (bypassing V1). However, in addition, GY shows two major features absent in controls: (i) a contralateral pathway from right LGN to left MT+/V5, (ii) a substantial cortico-cortical connection between MT+/V5 bilaterally. Both observations are consistent with previous functional MRI data from GY showing enhanced ipsilateral activation in MT+/V5. There is also evidence for a pathway in GY from left LGN to right MT+/V5, although the lesion makes its quantification difficult. This suggests that employing alternative brain regions for processing of information following cortical damage in childhood may strengthen or establish specific connections.

Independent anatomical and functional measures of the V1/V2 boundary in human visual cortex

The cerebral cortex has both anatomical and functional specialization, but the level of correspondence between the two in the human brain has remained largely elusive. Recent successes in high-resolution magnetic resonance imaging of myeloarchitecture patterns in the cortex suggest that it may now be possible to compare directly human anatomy and function in vivo. We independently investigated the anatomical and functional borders between primary and secondary human visual areas (V1 and V2) in vivo. Functional borders were mapped with functional magnetic resonance imaging (fMRI) using a narrow, vertical black and white contrast-reversing wedge. In three separate scanning sessions, anatomical images were collected at three different slice orientations (300 microm x 300 microm, slice thickness, 1.5 mm). The anatomical signature of V1 was determined by the presence of a hypointense band in the middle of the cortical gray matter. The band was identified in between 81% and 33% (mean 57%) of V1 defined using fMRI, and less than 5% of the identified band was in cortex outside V1. Intensity profiles taken through the gray matter on the V1 and V2 sides of the functional border indicate a measurable difference in the size of the hypointense band for all subjects. This is the first demonstration that the definition of V1 by fMRI closely matches the anatomically defined striate cortex in the human brain. The development of very high-resolution structural MRI may permit the definition of cortical areas based on myeloarchitecture when functional definition is not possible.

Receptive field size in V1 neurons limits acuity for perceiving disparity modulation

Disparity selectivity in the striate cortex has generally been studied with uniform disparity fields covering the receptive field (RF). In four awake behaving monkeys, we quantitatively characterized the spatial three-dimensional structure of 55 V1 RFs using random dot stereograms in which disparity varied as a sinusoidal function of vertical position (“corrugations”). At low spatial frequencies, this produced a modulation in neuronal firing at the temporal frequency of the stimulus. As the spatial frequency increased, the modulation reduced. The mean response rate changed little and was close to that produced by a uniform stimulus at the mean disparity of the corrugation. In 48 of 55 (91%) neurons, the modulation strength was a lowpass function of spatial frequency. These results are compatible with a response determined only by the weighted mean of the disparities of the dots (the weights being set by the RF envelope) and suggest that there is no disparity-based surround inhibition or selectivity for disparity gradients. This simple weighting scheme predicts a relationship between RF size and the high-frequency cutoff. Comparison with independent measurements of RF size was compatible with this. All of this behavior closely matches the binocular energy model. The mean cutoff frequency, 0.5 cycles per degree, is similar to equivalent measures of decline in human psychophysical sensitivity for such depth corrugations as a function of frequency (Tyler, 1974; Prince and Rogers, 1998; Banks et al., 2004). This suggests that human cyclopean acuity for disparity modulations is limited by the selectivity of V1 neurons. This in turn is primarily limited by the RF size, because we find no sensitivity for disparity gradients or other disparity differences within the RFs.

Imaging reveals optic tract degeneration in hemianopia.

PURPOSE To investigate whether there is transsynaptic degeneration in the human optic tract in hemianopia. To consider how the degeneration varies with duration of hemianopia and location of insult. METHODS Seven patients with damage to the primary visual cortex (V1), the lateral geniculate nucleus (LGN), or the optic tract were scanned with structural MRI. The volume and cross-sectional area of the left and right optic tracts were computed based on the intensity values of the T1-weighted image. High values correspond to voxels with high white matter content, and the values decrease as the white matter content drops (indicating degeneration). A laterality index to compare the tract size in the two hemispheres was calculated at different intensity values. RESULTS The three hemianopic patients with longstanding damage to either V1 or LGN showed laterality indices greater than 0.5 at the highest intensity values, indicating significant optic tract degeneration. Those with recent damage to the optic tract had even higher laterality indices due to direct degeneration. Even 18 months after V1 lesion, there was a significant correlation between the cross-section and volume indices at different intensity thresholds, whereas no control subject showed any correlation. CONCLUSIONS Transsynaptic degeneration had already begun 18 months after lesion. Although there was no visible decrease in volume at this stage, the white matter integrity was compromised. Significant decrease in volume could be visualized at longer durations of hemianopia. This method of objectively assessing structural images provides an effective, noninvasive approach to monitor the timescale of optic tract degeneration.

Human blindsight is mediated by an intact geniculo-extrastriate pathway.

Although damage to the primary visual cortex (V1) causes hemianopia, many patients retain some residual vision; known as blindsight. We show that blindsight may be facilitated by an intact white-matter pathway between the lateral geniculate nucleus and motion area hMT+. Visual psychophysics, diffusion-weighted magnetic resonance imaging and fibre tractography were applied in 17 patients with V1 damage acquired during adulthood and 9 age-matched controls. Individuals with V1 damage were subdivided into blindsight positive (preserved residual vision) and negative (no residual vision) according to psychophysical performance. All blindsight positive individuals showed intact geniculo-hMT+ pathways, while this pathway was significantly impaired or not measurable in blindsight negative individuals. Two white matter pathways previously implicated in blindsight: (i) superior colliculus to hMT+ and (ii) between hMT+ in each hemisphere were not consistently present in blindsight positive cases. Understanding the visual pathways crucial for residual vision may direct future rehabilitation strategies for hemianopia patients. DOI: http://dx.doi.org/10.7554/eLife.08935.001

Structural and Functional Changes across the Visual Cortex of a Patient with Visual Form Agnosia

Loss of shape recognition in visual-form agnosia occurs without equivalent losses in the use of vision to guide actions, providing support for the hypothesis of two visual systems (for “perception” and “action”). The human individual DF received a toxic exposure to carbon monoxide some years ago, which resulted in a persisting visual-form agnosia that has been extensively characterized at the behavioral level. We conducted a detailed high-resolution MRI study of DFs cortex, combining structural and functional measurements. We present the first accurate quantification of the changes in thickness across DFs occipital cortex, finding the most substantial loss in the lateral occipital cortex (LOC). There are reduced white matter connections between LOC and other areas. Functional measures show pockets of activity that survive within structurally damaged areas. The topographic mapping of visual areas showed that ordered retinotopic maps were evident for DF in the ventral portions of visual cortical areas V1, V2, V3, and hV4. Although V1 shows evidence of topographic order in its dorsal portion, such maps could not be found in the dorsal parts of V2 and V3. We conclude that it is not possible to understand fully the deficits in object perception in visual-form agnosia without the exploitation of both structural and functional measurements. Our results also highlight for DF the cortical routes through which visual information is able to pass to support her well-documented abilities to use visual information to guide actions.

Neuronal Computation of Disparity in V1 Limits Temporal Resolution for Detecting Disparity Modulation

The human ability to detect modulation of binocular disparity over time is poor compared with detection of luminance modulation. We examined the physiological origin of this limitation by analyzing neuronal responses to temporal modulation of binocular disparity in striate cortex of awake monkeys. When neurons were presented with random-dot stereograms in which disparity varied sinusoidally over time, their responses modulated at the stimulus temporal frequency, with little change in mean firing rate. We calculated modulation amplitude as a function of temporal frequency and compared this with the psychophysical performance of four human observers. Neuronal and psychophysical functions showed similar peak frequencies (2 Hz) and comparable high-cut frequencies (10 and 5.5 Hz, respectively). Thus, V1 (primary visual cortex) neurons appear to limit psychophysical performance. The temporal resolution of the same neurons for contrast modulation was ∼2.5 times greater, which parallels the superior psychophysical performance for contrast. There is a simple mathematical explanation for this difference: it results from calculating cross-correlation between temporally broadband monocular images that are bandpass filtered before measuring correlation. The limit on temporal resolution is a direct consequence of the binocular energy model that adds to the list of properties of human stereoscopic performance that are explained by this simple model of disparity encoding in V1: the same neurons can account for the performance of psychophysical tasks that result in either high (contrast) or low (disparity) temporal resolution. Because this principle holds whenever a broadband input is bandpass filtered before computing correlation, it may limit the resolution of other neuronal systems.

Human Cortical Activity Evoked by the Assignment of Authenticity when Viewing Works of Art

The expertise of others is a major social influence on our everyday decisions and actions. Many viewers of art, whether expert or naïve, are convinced that the full esthetic appreciation of an artwork depends upon the assurance that the work is genuine rather than fake. Rembrandt portraits provide an interesting image set for testing this idea, as there is a large number of them and recent scholarship has determined that quite a few fakes and copies exist. Use of this image set allowed us to separate the brain’s response to images of genuine and fake pictures from the brain’s response to external advice about the authenticity of the paintings. Using functional magnetic resonance imaging, viewing of artworks assigned as “copy,” rather than “authentic,” evoked stronger responses in frontopolar cortex (FPC), and right precuneus, regardless of whether the portrait was actually genuine. Advice about authenticity had no direct effect on the cortical visual areas responsive to the paintings, but there was a significant psycho-physiological interaction between the FPC and the lateral occipital area, which suggests that these visual areas may be modulated by FPC. We propose that the activation of brain networks rather than a single cortical area in this paradigm supports the art scholars’ view that esthetic judgments are multi-faceted and multi-dimensional in nature.

Visual activation of extra-striate cortex in the absence of V1 activation.

Research highlights ▶ Gray matter of V1 shows abnormal T1 characteristics and its perfusion is reduced. ▶ Damage is confined to gray matter with no adjacent white matter involvement. ▶ BOLD activation levels in the calcarine sulcus are drastically reduced. ▶ Activation of extrastriate regions to visual stimulation is preserved. ▶ Pathway between LGN and V1 shows degeneration; between LGN and V5/MT is intact.

Methodological issues relating to in vivo cortical myelography using MRI

The relationship between neocortical structure and function is a key area of research in neuroscience. Most studies of neural function, whether using neurophysiology or neuroimaging methods, are interpreted with relation to the underlying cortical myelo‐ and cytoarchitecture. For functional neuroimaging studies this often means using cytoarchitectonic maps based on the study of a limited number of brains, despite evidence for substantial interindividual variation. Improvements in MR technology, resulting in wider availability of high‐field MRI systems, have led to an increase in the achievable resolution in MR scans. Several groups have reported the in vivo detection of myelination patterns within the cortex, consistent with those observed in postmortem tissue. This leads to the possibility of predefining areas for fMRI analysis based on the cortical architecture. To do this it is essential to know, in a quantitative way, how reliably myeloarchitectonic areas and boundaries can be detected using MRI. Here we investigate the striate cortex, known to be coincident with V1, to assess the detectability of the stria of Gennari across V1 and across subjects. Under optimal conditions, 80% of the stria of Gennari was visualized using our methodology, although there was considerable variability in the level of detection across subjects. We discuss the limitations of the methodology and propose ways to improve the detection level of cortical myeloarchitecture more generally. Hum. Brain Mapping, 2005.