Behavioral studies have reported reduced spatial attention in amblyopia, a developmental disorder of spatial vision. However, the neural populations in the visual cortex linked with these behavioral spatial attention deficits have not been identified. Here, we use functional MRI–informed electroencephalography source imaging to measure the effect of attention on neural population activity in the visual cortex of human adult strabismic amblyopes who were stereoblind. We show that compared with controls, the modulatory effects of selective visual attention on the input from the amblyopic eye are substantially reduced in the primary visual cortex (V1) as well as in extrastriate visual areas hV4 and hMT+. Degraded attentional modulation is also found in the normal-acuity fellow eye in areas hV4 and hMT+ but not in V1. These results provide electrophysiological evidence that abnormal binocular input during a developmental critical period may impact cortical connections between the visual cortex and higher level cortices beyond the known amblyopic losses in V1 and V2, suggesting that a deficit of attentional modulation in the visual cortex is an important component of the functional impairment in amblyopia. Furthermore, we find that degraded attentional modulation in V1 is correlated with the magnitude of interocular suppression and the depth of amblyopia. These results support the view that the visual suppression often seen in strabismic amblyopia might be a form of attentional neglect of the visual input to the amblyopic eye.
Frequency-following and frequency-doubling neurons are ubiquitous in both striate and extrastriate visual areas. However, responses from these two types of neural populations have not been effectively compared in humans because previous EEG studies have not successfully dissociated responses from these populations. We devised a light–dark flicker stimulus that unambiguously distinguished these responses as reflected in the first and second harmonics in the steady-state visual evoked potentials. These harmonics revealed the spatial and functional segregation of frequency-following (the first harmonic) and frequency-doubling (the second harmonic) neural populations. Spatially, the first and second harmonics in steady-state visual evoked potentials exhibited divergent posterior scalp topographies for a broad range of EEG frequencies. The scalp maximum was medial for the first harmonic and contralateral for the second harmonic, a divergence not attributable to absolute response frequency. Functionally, voluntary visual–spatial attention strongly modulated the second harmonic but had negligible effects on the simultaneously elicited first harmonic. These dissociations suggest an intriguing possibility that frequency-following and frequency-doubling neural populations may contribute complementary functions to resolve the conflicting demands of attentional enhancement and signal fidelity—the frequency-doubling population may mediate substantial top–down signal modulation for attentional selection, whereas the frequency-following population may simultaneously preserve relatively undistorted sensory qualities regardless of the observer’s cognitive state.
In a neural population driven by a simple grating stimulus, different sub-populations are maximally informative about changes to the grating’s orientation and contrast. In theory, observers should attend to the optimal subpopulation when switching between orientation and contrast discrimination tasks. Here we used source-imaged, steady-state visual evoked potentials (SSVEPs) and visual psychophysics, to determine whether this is the case. Observers fixated centrally while static targets were presented bilaterally along with a cue indicating task type (contrast or orientation modulation detection) and task location (left or right). Changes in neuronal activity were measured by quantifying frequency-tagged responses from flickering ‘reporter’ gratings surrounding the targets. To determine the orientating tuning of attentionally-modulated neurons, we measured responses for three different probe-reporter angles: 0, 20 and 45°. We estimated frequency-tagged cortical activity using a minimum norm inverse procedure combined with realistic MR-derived head models and retinotopically-mapped visual areas. Estimates of neural activity from regions of interest centered on V1 showed that attention to a spatial location clearly increased the amplitude of the neural response in that location. More importantly, the pattern of modulation depended on the task. For orientation discrimination, attentional modulation showed a sharp peak in the population tuned 20° from the target orientation, whereas for contrast discrimination the enhancement was more broadly tuned. Similar tuning functions for orientation and contrast discrimination were obtained from psychophysical adaptation studies. These findings indicate that humans attend selectively to the most informative neural population and that these populations change depending on the nature of the task.
Attention is thought to operate by enhancing the target of interest and suppressing the surroundings. We hypothesized that the spatial profile of attention depends on the surround's relationship to the target. Using high-density electroencephalographic measurements, we examined the spatial profile of attention to a grating target surrounded by an annular grating that was either coextensive with the target (unsegmented) or appeared segmented from it due to a gap or phase offset. We directly probed the spread of attention from the central target into the surround by flickering the surround and monitoring frequency-tagged steady-state visual-evoked potentials. Observers were required to detect a contrast increment that occurred only on the target. Successful detection of the increment required selecting the target and suppressing the surround, particularly when the target did not readily segment from the surround. The profile of attention was investigated in five visual regions of interest (ROIs) (V1, V4, V3A, lateral occipital complex, and human middle temporal area), mapped in a separate anatomical magnetic resonance imaging scan. We found that in most ROIs, attention to the target generated smaller responses from the surrounding annulus when it was contiguous compared with when it was clearly segmented. This result shows that the profile of attention depends on task demands and on surrounding context; attention is tightly focused when the target region needs to be isolated but loosely focused when the target region is clearly segmented.
Selective attention is known to interact with perceptual organization. In visual scenes, individual objects that are distinct and discriminable may occur on their own, or in groups such as a stack of books. The main objective of this study is to probe the neural interaction that occurs between individual objects when attention is directed toward one or more objects. Here we record steady-state visual evoked potentials via electrocorticography to directly assess the responses to individual stimuli and to their interaction. When human participants attend to two adjacent stimuli, prefrontal and parietal cortex shows a selective enhancement of only the neural interaction between stimuli, but not the responses to individual stimuli. When only one stimulus is attended, the neural response to that stimulus is selectively enhanced in prefrontal and parietal cortex. In contrast, early visual areas generally manifest responses to individual stimuli and to their interaction regardless of attentional task, although a subset of the responses is modulated similarly to prefrontal and parietal cortex. Thus, the neural representation of the visual scene as one progresses up the cortical hierarchy becomes more highly task-specific and represents either individual stimuli or their interaction, depending on the behavioral goal. Attention to multiple objects facilitates an integration of objects akin to perceptual grouping. Individual objects in a visual scene are seen as distinct entities or as parts of a whole. Here we examine how attention to multiple objects affects their neural representation. Previous studies measured single-cell or fMRI responses and obtained only aggregate measures that combined the activity to individual stimuli as well as their potential interaction. Here, we directly measure electrocorticographic steady-state responses corresponding to individual objects and to their interaction using a frequency-tagging technique. Attention to two stimuli increases the interaction component that is a hallmark for perceptual integration of stimuli. Furthermore, this stimulus-specific interaction is represented in prefrontal and parietal cortex in a task-dependent manner.
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