Yee-Joon Kim

Attention Selects Informative Neural Populations in Human V1

In a neural population driven by a simple grating stimulus, different subpopulations are maximally informative about changes to the gratings 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 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 orientation 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.

The Selectivity of Task-Dependent Attention Varies with Surrounding Context

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 surrounds 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.

Degraded attentional modulation of cortical neural populations in strabismic amblyopia

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.

Cortical sources of Vernier acuity in the human visual system: An EEG-source imaging study

Vernier acuity determines the relative position of visual features with a precision better than the sampling resolution of cone receptors in the retina. Because Vernier displacement is thought to be mediated by orientation-tuned mechanisms, Vernier acuity is presumed to be processed in striate visual cortex (V1). However, there is considerable evidence suggesting that Vernier acuity is dependent not only on structures in V1 but also on processing in extrastriate cortical regions. Here we used functional magnetic resonance imaging–informed electroencephalogram source imaging to localize the cortical sources of Vernier acuity in observers with normal vision. We measured suprathreshold and near-threshold responses to Vernier onset/offset stimuli at different stages of the visual cortical hierarchy, including V1, hV4, lateral occipital cortex (LOC), and middle temporal cortex (hMT+). These responses were compared with responses to grating on/off stimuli, as well as to stimuli that control for lateral motion in the Vernier task. Our results show that all visual cortical regions of interest (ROIs) responded to both suprathreshold Vernier and grating stimuli. However, thresholds for Vernier displacement (Vernier acuity) were lowest in V1 and LOC compared with hV4 and hMT+, whereas all visual ROIs had identical thresholds for spatial frequency (grating acuity) and for relative motion. The cortical selectivity of sensitivity to Vernier displacement provides strong evidence that LOC, in addition to V1, is involved in Vernier acuity processing. The robust activation of LOC might be related to the sensitivity to the relative position of features, which is common to Vernier displacement and to some kinds of texture segmentation.

Attention to Multiple Objects Facilitates Their Integration in Prefrontal and Parietal Cortex

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. SIGNIFICANCE STATEMENT 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.

Cortical sources of vernier acuity: an EEG-source imaging study.

Vernier acuity determines the relative position of visual features with a precision better than the sampling resolution of the cone mosaic. Because the vernier offset is thought to be detected by orientation-tuned mechanisms, we expect cortical areas such as V1 to respond strongly to vernier stimuli. Here we use 128-channel EEG combined with cortical source imaging to identify multiple regions of visual cortex that underlie the detection of vernier offsets. Steady-state Visual Evoked Potentials (SSVEPs) were recorded from fifteen normal vision observers under two conditions. In the test condition, vernier offsets were periodically introduced and withdrawn at 3.75 Hz (alignment/misalignment) on a 2 cpd square-wave grating. In the control condition, the offsets were displaced symmetrically with respect to the reference (misalignment/misalignment), to produce the same displacement as in the test condition. In both conditions, the size of the offset was swept from 8 to 0.5 arcmin in 10-logarithm steps within a ten-second presentation interval. The vernier-offset (test condition) elicited robust odd harmonic responses in V1 and lateral occipital cortex (LOC). Thresholds for eliciting odd-harmonic responses were lowest in V1 and LOC, followed by V3a, with higher thresholds in middle temporal (hMT+) and hV4. Importantly, the control condition elicited very weak odd harmonic activity. Both the vernier test and the lateral-motion control condition elicited similar activity at even harmonics in all cortical regions of interest (ROI), related to the lateral-motion of the offsets. Our data indicate that V1, LOC and V3a are particularly sensitive to the detection of vernier offsets, while all visual ROIs are sensitive to lateral motion. Our results support a role for V1 in vernier acuity related to its exquisite sensitivity to orientation differences. The robust activation of LOC might be related to the texture characteristics of the extended vernier, or to its sensitivity to vernier offsets. Meeting abstract presented at VSS 2015.