Publications

Face adaptation does not improve performance on search or discrimination tasks

The Representation of Behavioral Choice for Motion in Human Visual Cortex

Spatial and Cross-Modal Attention Alter Responses to Unattended Sensory Information in Early Visual and Auditory Human Cortex

Feature-Based Attentional Modulations in the Absence of Direct Visual Stimulation

Tactile Hyperacuity Thresholds Correlate with Finger Maps in Primary Somatosensory Cortex (S1)

The Effect of Spatial Attention on Contrast Response Functions in Human Visual Cortex

Abstract: Previous electrophysiology data suggests that the modulation of neuronal firing by spatial attention depends on stimulus contrast, which has been described using either a multiplicative gain or a contrast-gain model. Herewemeasured the effect of spatial attention on contrast responses in humans using functional MRI. To our surprise, we found that the modulation of blood oxygenation level-dependent (BOLD) responses by spatial attention does not greatly depend on stimulus contrast in visual cortical areas tested [V1, V2, V3, andMT
(middle temporal area)]. An additive model, rather than a multiplicative or contrast-gain model best describes the attentional modulations in V1. This inconsistency with previous single-unit electrophysiological data has implications for the population-based neuronal source of the BOLD signal.

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Selectivity for the Configural Cues that Identify the Gender, Ethnicity, and Identity of Faces in Human Cortex

Abstract: We used psychophysical and functional MRI (fMRI) adaptation to examine how and where the visual configural cues underlying identification of facial ethnicity, gender, and identity are processed. We found that the cortical regions showing selectivity to these cues are distributed widely across the inferior occipital cortex, fusiform areas, and the cingulate gyrus. These regions were not colocalized with areas activated by traditional face area localizer scans. Traditional face area localizer scans isolate regions defined by stronger fMRI responses to a random series of face images than to a series of non-face images. Because these scans present a random assortment of face images, they presumably produce the strongest responses within regions containing neurons that are face-sensitive but not highly tuned for face type. These areas might be expected to show only weak selective adaptation effects. In contrast, the largest responses to our selective adaptation paradigm would be expected within areas containing more selectively tuned neurons that might be expected to show only a sparse collective response to a series of random faces. Many aspects of face processing (e.g., prosopagnosia, recognition, and configural vs. featural processing) are likely to rely heavily on regions containing high proportions of neurons that show selective tuning for faces.

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Effects Of Feature-Based Attention On The Motion Aftereffect At Remote Locations

Abstract: Previous studies have shown that attention to a particular stimulus feature, such as direction of motion or color, enhances neuronal responses to unattended stimuli sharing that feature. We studied this effect psychophysically by measuring the strength of the motion aftereffect (MAE) induced by an unattended stimulus when attention was directed to one of two overlapping fields of moving dots in a different spatial location. When attention was directed to the same direction of motion as the unattended stimulus, the unattended stimulus induced a stronger MAE than when attention was directed to the opposite direction. Also, when the unattended location contained either uncorrelated motion or had no stimulus at all an MAE was induced in the opposite direction to the attended direction of motion. The strength of the MAE was similar regardless of whether subjects attended to the speed or luminance of the attended dots. These results provide further support for a global feature-based mechanism of attention, and show that the effect spreads across all features of an attended object, and to all locations of visual space.

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Adaptation: from single cells to BOLD signals

Abstract: Functional magnetic resonance imaging adaptation (fMRIa) is an increasingly popular method that aims to provide insight into the functional properties of subpopulations of neurons within an imaging voxel. The technique relies on the assumption that neural adaptation reduces activity when two successive stimuli activate the same subpopulation but not when they stimulate different subpopulations. Here, we assess the validity of fMRIa by comparing single-cell recordings with functional imaging of orientation, motion and face processing. We find that fMRIa provides novel insight into neural representations in the human brain. However, network responses in general and adaptation in particular are more complex than is often assumed, and an unequivocal interpretation of fMRIa results can be achieved only with great care.

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Comentary by S. Treue and J.C. Martin

Contrast gain in the brain

Abstract:Human sensory systems have the remarkable ability of adjusting sensitivity to the surrounding environment. In this issue of Neuron, Gardner and colleagues used fMRI to show how the visual system shifts its sensitivity to contrast. This process may be helpful for keeping the appearance of contrast constant across a range of spatial frequencies.

This Preview commentary on the article: Gardner, J. L., Sun, P., Waggoner, R. A., Ueno, K., Tanaka, K., and Cheng, K. (2005). "Contrast adaptation and representation in human early visual cortex." Neuron;47 607-620.

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Click here to download Matlab code to generate the figure on the right.

Attention and visual perception

Abstract: Somewhere between the retina and our conscious visual experience, the majority of the information impinging on the eye is lost. We are typically aware of only either the most salient parts of a visual scene or the parts that we are actively paying attention to. Recent research on visual neurons in monkeys is beginning to show how the brain both selects and discards incoming visual information. For example, what happens to the responses of visual neurons when attention is directed to one element, such as an oriented colored bar, embedded among an array of other oriented bars? Some of this research shows that attention to the oriented bar restricts the receptive field of visual neurons down to this single element. However, other research shows that attention to this single element affects the responses of neurons with receptive fields throughout the visual field. In this review, these two seemingly contradictory results are shown to actually be mutually consistent. A simple computational model is described that explains these results, and also provides a framework for predicting a variety of additional neurophysiological, neuroimaging and behavioral studies of attention.

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Imaging orientation selectivity: decoding conscious perception in V1

Abstract: In V1, neurons preferring similar orientations are grouped in columns too small to be resolved by conventional fMRI. Two studies circumvent this limitation by using algorithms to recognize patterns of activation across a large area. This new trick allows the authors to distinguish responses to different orientations in human V1, and to study its contribution to conscious perception.

This is a News and Views commentary on two articles:

(1) Kamitani, Y. and Tong, F. (2005) "Decoding the visual ans subjective contents of the human brain" Nature Neuroscience;8 679-685.

(2) Haynes, J. and Rees, G. (2005) "Predicting the orientation of invisible stimuli from activity in human primary visual cortex" Nature Neuroscience;8 686-691.

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Click here to download Matlab code to generate the figure on the right.

The Relationship between Task Performance and Functional Magnetic Resonance Imaging Response

Abstract: We compared psychophysical and functional magnetic resonance imaging (fMRI) responses within areas V1–V3 and MT
during both a speed and a contrast discrimination task. We found that fMRI responses did not depend significantly on task in any of these areas. Moreover, responses in V1–V3 were larger than those in MT
for both the speed and the contrast discrimination tasks across a wide range of contrasts. This pattern of results demonstrates that localizing function based on finding those regions of cortex that show greater activity to a given task-stimulus combination than to other tasks and stimuli may, under certain conditions, be misleading. However, a simple ideal observer model assuming that perceptual thresholds are dependent on neuronal population responses does successfully show that V1 has neuronal properties consistent with our subjects’ contrast discrimination performance, and that MT
has neuronal properties consistent with subjects’ performance on a speed discrimination task.

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Individual Differences among Grapheme-Color Synesthetes: Brain-Behavior Correlations

Abstract: Grapheme-color synesthetes experience specific colors associated with specific number or letter characters. To determine the neural locus of this condition, we compared behavioral and fMRI responses in six grapheme-color synesthetes to control subjects. In our behavioral experiments, we found that a subject's synesthetic experience can aid in texture segregation (Experiment 1) and to reduce the effects of crowding (Experiment 2). For synesthetes, graphemes produced larger fMRI responses in color selective area human V4 than for control subjects (Experiment 3). Importantly, we found a correlation within subjects between the behavioral and fMRI results; subjects with better performance on the behavioral experiments showed larger fMRI responses in early retinotopic visual areas (V1, V2, V3 and hV4). These results suggest that grapheme-color synesthesia is the result of cross activation between grapheme-selective and color-selective brain areas. The correlation between the behavioral and fMRI results suggests that grapheme-color synesthesia may constitute a heterogeneous group.

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Comentary by M.J. Dixon and D. Smilek

The time course and specificity of perceptual deterioration

Abstract: Repeated within-day testing on a texture discrimination task leads to retinotopically specific decreases in performance. Although perceptual learning has been shown to be highly specific to the retinotopic location and characteristics of the trained stimulus, the specificity of perceptual deterioration has not been studied. We investigated the similarities between learning and deterioration by examining whether deterioration transfers to new distractor or target orientations or to the untrained eye. Participants performed a texture discrimination task in three one-hour sessions. We tested the specificity of deterioration in the final session by switching either the orientation of the background or the target elements by 90°. We found that performance deteriorated steadily both within and across the first two sessions and was specific to the target but not the distractor orientation. In a separate experiment, we found that deterioration transferred to the untrained eye. Changes in performance were independent of reported sleepiness and awareness of stimulus changes, arguing against the possibility that perceptual deterioration is due to general fatigue. Rather, we hypothesize that perceptual deterioration may be caused by changes in the ability for attention to selectively enhance the responses of relatively low-level orientation-selective sensory neurons, possibly within the primary visual cortex. Further, the differences in specificity profiles between learning and deterioration suggest separate underlying mechanisms that occur within the same cortical area.

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Visual Cortex: The Continuing Puzzle of Area V2

Abstract: Surprisingly little is known about the role of V2 in visual processing. A recent study found that the responses of V2 neurons to pairs of angled lines could be predicted from their responses to the individual line components. A simple analysis shows how these neurons may simply sum the responses from one or more orientation selective V1 neurons.

This is a dispatch written in reponse to Ito, M. and H. Komatsu (2004). "Representation of angles embedded within contour stimuli in area V2 of macaque monkeys." J Neurosci 24(13): 3313-24. Reprint

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The invariance of directional tuning with contrast and coherence

Abstract: The responses of motion mechanisms depend not only on the direction of a stimulus, but also on its contrast, coherence and speed. We examined how contrast, coherence and directional selectivity interact by measuring directional tuning psychophysically across a wide range of coherence and contrast levels. We fit data with a simple model that estimated directional tuning bandwidth using contrast and coherence gain parameters that were based on neurophysiological estimates. This model estimated a bandwidth of ~90° for directionally selective mechanisms. Bandwidth was invariant across a wide range of contrasts and coherences, as predicted by models of contrast normalization.

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Adaptation and Attention Selection

G.M. Boynton
Nature Neuroscience 2004;7 8-10.

Abstract: Attention improves perception, presumably by influencing neural responses. In this issue, an fMRI study shows that paying attention to an object might enhance perception by increasing the selectivity of neuronal subpopulations in higher visual areas.

This is a News and Views commentary on Murray and Wojciulik "Attention increases neural selectivity in the human lateral occipital complex" Nature Neuroscience 2004;70-74. , and Supplementary Information

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Orientation-specific Adaptation in Human Visual Cortex

Abstract: Nearly all methods for analyzing and interpreting fMRI data assume that the fMRI signal behaves roughly a in a linear fashion. However, it has been shown that the mean fMRI response to a pair of briefly presented visual stimuli is significantly smaller than would be expected from the response to a single stimulus. This smaller response could be the result of either a nonlinearity in the fMRI signal or to neuronal adaptation. We tested the neuronal adaptation hypothesis by measuring the fMRI response to sequential pairs of sinusoidal gratings that had either the same or orthogonal orientation. The adaptation hypothesis predicts that brain areas with orientation selective neurons should show a more linear response when the stimulus pair is orthogonal than when the pair is identical. Our results show no orientation-specific adaptation effects in primary visual cortex (V1), but increasing effects along the hierarchy of visual areas (V2, V3 and V4V). A psychophysical contrast detection experiment, using similar oriented gratings as adapters, shows evidence of orientation-specific adaptation in the visual system. These results have implications for the interpretation of rapid event-related fMRI experiments, as well as for recently developed methods that use adaptation as a tool to measure the response properties of underlying neuronal subpopulations.

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The Effects of Long-Term Deprivation on Visual Perception and Visual Cortex

Abstract: Suppose a man born blind, and now adult, and taught by his touch to distinguish between a cube and a sphere Suppose then the cube and the sphere placed on the table, and the blind man made to see Query: whether by his sight, before he touched them, he could distinguish and tell which is the globe, which is the cube?" Despite the philosophical and psychological interest of Molyneaux's question, cases of adult sight restoration are so rare that even now little is known about perceptual experience after long-term visual deprivation. To address this question, we used psychophysics and functional magnetic resonance imaging to characterize visual processing in a subject who had been blind from the age of 3 to 43. We found several consequences of long-term visual deprivation, including a shift in the tuning of neurons towards very low spatial frequencies, impairments in form processing, object agnosia, and prosopagnosia. Using fMRI we demonstrated that these deficiencies were consequent upon neural changes in visual striate and extrastriate cortex. In contrast to these difficulties with form perception, motion processing was relatively undisturbed by deprivation. Consistent with this dissociation, cortical areas responsible for motion processing (MT complex) showed stronger and more organized fMRI activation than form processing areas (V1-V4).

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Supplementary note
Comentary by Gregory, R. L. (2003). "Seeing after blindness." Nat Neurosci 6(9): 909-10.

Surface Segmentation Based on the Luminance and Color Statistics of Natural Scenes

Abstract: The luminance and color of surfaces in natural scenes are relatively independent under certain linear transformations,with the luminance of a surface providing little information about the color of that surface, and vice versa. However, differences in luminance between two locations in a natural scene remain strongly associated with differences in color. We used the statistics of the spatiochromatic structure of natural scenes as the priors for a Bayesian model that decides whether or not two points within an image fall on the same surface. This model provides a biologically plausible algorithm for surface segmentation that models observer segmentations well.

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Cortical Magnification Within Human Primary Visual Cortex Correlates with Acuity Thresholds

Abstract: We measured linear cortical magnification factors in V1 with fMRI and visual acuity (Vernier and grating) in the same observers. The cortical representation of both Vernier and grating acuity thresholds in V1 was found to be roughly constant across all eccentricities. We also found a within-observer correlation between cortical magnification and Vernier acuity, further supporting claims that Vernier acuity is limited by cortical magnification in V1.

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Global Feature-Based Attention for Motion and Color

Abstract: We used a divided attention psychophysical task to test the hypothesis that visual attention to a stimulus feature facilitates the processing of other stimuli sharing the same feature. Performance on a dual task was significantly better when human observers divided attention across two spatially separate stimuli sharing a common feature (same direction of motion or same color) compared to opposing features. This attentional effect was dependent upon the presence of competing stimuli. These results are consistent with a spatially global feature-based mechanism of attention that increases the response of cortical neurons tuned to an attended feature throughout the visual field.
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Global Effects of Feature-based Attention in Human Visual Cortex

Abstract: The content of visual experience depends on how selective attention is distributed in the visual field. We used functional magnetic resonance imaging (fMRI) in humans to test whether feature-based attention can globally influence visual cortical responses to stimuli outside the attended location. Attention to a stimulus feature (color or direction of motion) increased the response of cortical visual areas to a spatially distance, ignored stimulus that shared the same feature.

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Supplementary methods

Color Vision: How the Cortex Represents Color

Abstract: Our understanding of how we see color has benefited from the long tradition of visual psychophysics. More recently, models and methods from psychophysics are helping to guide modern neuroimaging experiments on color vision. Combining the two techniques can lead to discoveries that neither can make alone.

This is a dispatch written in reponse to Wade, A.R. and B.A. Wandell, Chromatic light adaptation measured using functional magnetic resonance imaging. J Neurosci, 2002. 22(18): p. 8148-57.

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Efficient Design of Event-Related fMRI Experiments Using M-Sequences

Abstract: Rapid event-related fMRI (erfMRI) allows estimation of the shape of hemodynamic responses (HDR) associated with transient brain activation evoked by various sensory, motor, and cognitive events. Choosing a sequence of events that maximizes efficiency of estimating the HDR is essential for conducting event-related brain imaging experiments, since increasing efficiency is essentially equivalent to reducing scanning time or increasing the strength of the principal magnetic field. The efficiency of an erfMRI design depends critically on the temporal arrangement of the sequence of events and the noise in the fMRI signal. We introduce to erfMRI a simple method for generating efficient event sequences based on maximum-length shift register sequences, or m-sequences. We show that under the assumption of white uncorrelated MRI noise, efficiency of erfMRI experimental designs that employ m-sequences exceeds efficiency of the best randomly generated sequences. This is true for single and multiple event type experiments, which allow either parallel events (overlapping events design) or designs in which only one event occurs at a time (non-overlapping events design). HDR estimation efficiency afforded by m-sequences grows with the number of event types, and is greatest when event sequences are relatively short, albeit within commonly used scan times (i.e. 63-255 total events per scan).

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Download matlab code for generating M-sequences

Color Signals in Human Motion-Selective Cortex

Abstract: The neural basis for the effects of color and contrast on perceived speed was examined using functional magnetic resonance imaging (fMRI). Responses to S-cone (blue-yellow) and L-M cone (luminance) patterns were measured in area V1 and in the motion area MT+. The MT+ responses were quantitatively similar to perceptual speed judgments of color patterns but not to color detection measures. We also measured cortical motion responses in individuals lacking L and M cone function (S cone monochromats). The S cone monochromats have clear motion-response regions in the conventional MT+ position, and their contrast-response functions have twice the responsiviity of S cone contrast-response functions in normal controls. But, their responsivity is far lower than the normals' responsivity to luminance contrast. Thus, the powerful magnocellular input to MT+ is either weak or silend during photopic vision in S cone monochromats.

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Motion Opponency in Visual Cortex

Abstract: Perceptual studies suggest that visual motion perception is mediated by opponent mechanisms that correspond to mutually suppressive populations of neurons sensitive to motions in opposite directions.  We tested for a neuronal correlate of motion opponency using functional magnetic resonance imaging to measure brain activity in human visual cortex.  There was strong motion opponency in a secondary visual cortical area known as the human MT complex (MT+), but there was little evidence of motion opponency in primary visual cortex (V1).  To determine whether the level of opponency in human MT+ and monkey MT are comparable, a variant of these experiments was performed using multi-unit electrophysiological recording in areas MT and MST of the macaque monkey brain.  While there was substantial variability in the degree of opponency between recording sites, the monkey and human data were qualitatively similar on average.  These results provide further evidence that: 1) direction selective signals underlie human MT+ responses, 2) neuronal signals in human MT+ support visual motion perception, 3) human MT+ may be homologous to macaque monkey MT along with adjacent motion sensitive brain areas, and 4) that fMRI measurements are correlated with average spiking activity.

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Spatial Attention Affects Brain Activity in Human Primary Visual Cortex

Abstract: Functional magnetic resonance imaging (fMRI) was used to test if instructing subjects to attend to one or another location in a visual scene would affect neural activity in human primary visual cortex (V1). Stimuli were moving gratings restricted to a pair of peripheral, circular apertures, positioned to the right and to the left of a central fixation point. Subjects were trained to perform a motion discrimination task, attending (without moving their eyes) at any moment in time to one of the two stimulus apertures. FMRI responses were recorded while subjects were cued to alternate their attention between the two apertures. V1 responses in each hemisphere modulated with the alternation of the cue; responses were greater when the subject attended to the stimuli in the contralateral hemifield. The attentional modulation of the brain activity was about 25 percent of that evoked by alternating the stimulus with a uniform field.

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Neuronal Basis of Contrast Discrimination

Abstract: Psychophysical contrast increment thresholds were compared with neuronal responses, measured using functional magnetic resonance imaging (fMRI), to test the hypothesis that pattern discrimination judgments are limited by neuronal signals in early visual cortical areas. FMRI was used to measure human brain activity as a function of stimulus contrast, in each of several identifiable visual cortical areas. Contrast increment thresholds were measured for the same stimuli across a range of baseline contrasts. FMRI responses in visual areas V1, V2d, and V3d were found to be consistent with the psychophysical judgments, i.e., a contrast increment was detected when the fMRI responses in each of these brain areas increased by a criterion amount. Thus, the pooled activity of large numbers of neurons can reasonably well predict behavioral performance.

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Temporal Sensitivity of Human Luminance Pattern Mechanisms Determined by Masking with Temporally Modulated Stimuli

Abstract: Target contrast thresholds were measured using vertical spatial Gabor targets in the presence of full field maskers of the same spatial frequency and orientation. In the first experiment both target and masker were 2 cpd. The target was modulated at a frequency of 1 or 10 Hz and the maskers varied in temporal frequency from 1 to 30 Hz and in contrast from 0.03 to 0.50. In the second experiment both target and masker had a spatial frequency of 1, 5 or 8 cpd. The target was modulated at 7.5 Hz and the same set of maskers was used as in the first experiment. The results are not consistent with a widely used model that is based on mechanisms in which excitation is summed linearly and the sum is transformed by an S-shaped nonlinear excitation-response function. A new model of human pattern vision mechanisms, which has excitatory and divisive inhibitory inputs, describes the results well. Parameters from the best fit of the new model to the results of the first experiment show that the 1 Hz and 10 Hz targets were detected by mechanisms with temporal low-pass and band-pass excitatory sensitivity, respectively. Fits to the second experiment suggest that at 1 cpd, the excitatory tuning of the detecting mechanism is band-pass. At 5 and 8 cpd, the mechanisms are excited by a broad range of temporal frequencies. Mechanism sensitivity to divisive inhibition depends on temporal frequency in the same general way as sensitivity to excitation. Mechanisms are more broadly tuned to divisive inhibition than to excitation, except when the target temporal frequency is high.

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Functional Magnetic Resonance Imaging of Early Visual Pathways in Dyslexia

Abstract: We measured brain activity, perceptual thresholds and reading performance in a group of dyslexic and normal readers to test the hypothesis that dyslexia is associated with an abnormality in the magnocellular (M) pathway of the early visual system. Functional magnetic resonance imaging (fMRI) was used to measure brain activity in conditions designed to preferentially stimulate the M pathway. Speed discrimination thresholds, that measure the minimal increase in stimulus speed that is just noticeable, were acquired in a paradigm modeled after a previous study of M pathway lesioned monkeys. Dyslexics showed reduced brain activity compared to controls both in primary visual cortex (V1) and in several extrastriate areas, including area MT+ that is believed to receive a predominant M pathway input. There was a strong three-way correlation between brain activity, speed discrimination thresholds, and reading speed. Subjects with higher V1 and MT+ responses had lower perceptual thresholds (better performance) and were faster readers. These results support the hypothesis for an M pathway abnormality in dyslexia and imply strong relationships between the integrity of the M pathway, visual motion perception, and reading ability.

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Psychophysical evidence for a magnocellular pathway deficit in dyslexia

Abstract: The relationship between reading ability and psychophysical performance was examined to test the hypothesis that dyslexia is associated with a deficit in the magnocellular (M) pathway. Speed discrimination thresholds and contrast detection thresholds were measured under conditions (low mean luminance, low spatial frequency, high temporal frequency) for which psychophysical performance presumably depends on M pathway integrity. Dyslexic subjects had higher psychophysical thresholds than controls in both the speed discrimination and contrast detection tasks, but only the differences in speed thresholds were statistically significant. In addition, there was a strong correlation between individual differences in speed thresholds and reading rates. These results support the hypothesis for an M pathway abnormality in dyslexia, and suggest that motion discrimination may be a better indicator of dyslexia than is contrast sensitivity.

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Brain activity in visual cortex predicts individual differences in reading performance

Abstract: The relationship between brain activity and reading performance was examined to test the hypothesis that dyslexia involves a deficit in a specific visual pathway known as the magnocellular (M) pathway. Functional magnetic resonance imaging was used to measure brain activity in dyslexic and control subjects in conditions designed to preferentially stimulate the M pathway. Dyslexics showed reduced activity compared with controls both in the primary visual cortex and in a secondary cortical visual area (MT1) that is believed to receive a strong M pathway input. Most importantly, significant correlations were found between individual differences in reading rate and brain activity. These results support the hypothesis for an M pathway abnormality in dyslexia and imply a strong relationship between the integrity of the M pathway and reading ability.

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Linear Systems Analysis of fMRI in Human V1

Abstract: The linear transform model of functional magnetic resonance imaging (fMRI) hypothesizes that fMRI responses are proportional to local average neural activity, averaged over a period of time. This article reports results from three empirical tests that support this hypothesis. First, fMRI responses in human primary visual cortex (V1) depend separably on stimulus timing and stimulus contrast. Secondly, responses to long duration stimuli can be predicted from responses to shorter duration stimuli. Thirdly, the noise in the fMRI data is independent of stimulus contrast and temporal period. Although these tests can not prove the correctness of the linear transform model, they might have been used to reject the model. Since the linear transform model is consistent with our data, we proceeded to estimate the temporal fMRI impulse response function and the underlying (presumably neural) contrast-response function of human V1.

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