Collinear stimuli induce local and cross-areal coherence in the visual cortex of behaving monkeys.

BACKGROUND: Collinear patterns of local visual stimuli are used to study contextual effects in the visual system. Previous studies have shown that proximal collinear flankers, unlike orthogonal, can enhance the detection of a low contrast central element. However, the direct neural interactions between cortical populations processing the individual flanker elements and the central element are largely unknown. METHODOLOGY/PRINCIPAL FINDINGS: Using voltage-sensitive dye imaging (VSDI) we imaged neural population responses in V1 and V2 areas in fixating monkeys while they were presented with collinear or orthogonal arrays of Gabor patches. We then studied the spatio-temporal interactions between neuronal populations processing individual Gabor patches in the two conditions. Time-frequency analysis of the stimulus-evoked VSDI signal showed power increase mainly in low frequencies, i.e., the alpha band (α; 7-14 Hz). Power in the α-band was more discriminative at a single trial level than other neuronal population measures. Importantly, the collinear condition showed an increased intra-areal (V1-V1 and V2-V2) and inter-areal (V1-V2) α-coherence with shorter latencies than the orthogonal condition, both before and after the removal of the stimulus contribution. α-coherence appeared between discrete neural populations processing the individual Gabor patches: the central element and the flankers. CONCLUSIONS/SIGNIFICANCE: Our findings suggest that collinear effects are mediated by synchronization in a distributed network of proximal and distant neuronal populations within and across V1 and V2

α-coherence between different ROIs in V1 and V2.

<p><i>A:</i> A schematic illustration of the 4 ROIs used in this study: V1-CE, V1-flanker, V2-CE and V2-flanker. Superimposed are 4 different interactions each representing a pair of ROIs: V1-CE and V1-flanker (blue), V1-CE and V2-CE (red), V1-flanker and V2-flanker (green), V2-CE and V2-flanker (purple). <i>B:</i> The α-coherence as a function of time for the collinear (solid lines) and orthogonal (dashed lines) conditions calculated between each of the four pairs in A. <i>C:</i> α-coherence difference (collinear – orthogonal) between each of the four pairs in A. α-coherence was average 40–60 ms after stimulus onset (shaded bar in B). Error bars indicate SEM over recording sessions (n = 8 recording session from 2 monkeys). Asterisks denote significant α-coherence compared to 0 or between pairs. * p<0.05; ** p<0.01.</p

α-coherence dynamics in collinear and orthogonal conditions.

<p><i>A</i>: α-coherence as a function of time between V1-CE and other ROIs for the collinear (blue), orthogonal (red) and fixation alone (green) conditions averaged over pixels within each of the 4 ROIs (from left to right): V1-CE (n = 555 pixels), V1-flanker (n = 444 pixels), V2-CE (n = 523 pixels) and V2-Flanker (n = 545 pixels). Dashed lines indicate mean±3×SEM. Black horizontal lines indicate upper and lower limits of the α-coherence (mean±3×SEM) in the fixation alone condition. A change in α-coherence is defined by exceeding these limits. There was significantly higher stimulus-induced α-coherence in both collinear and orthogonal conditions compared to the fixation alone condition (Mann-Whitney U-test; p<0.01; averaged 0–100 ms). The inset depicts the pair of ROIs (blue arrow) from which α-coherence was calculated (see Fig. 1E). <i>B</i>: Scatter plots of the average α-coherence (AAC) averaged 0–100 ms after stimulus onset (shaded bar in A) in the collinear (y-axis) vs. the orthogonal (x-axis) conditions for each pixel in the different ROIs as in A. Each point reflects the average α-coherence of all pixel pairs between this specific pixel (in a specific ROI) and the V1-CE ROI pixels (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0049391#pone.0049391.e012" target="_blank">equation 8</a>). Almost all pixels are above the diagonal meaning there is higher AAC in the collinear than the orthogonal condition. <i>C</i>: Histograms of time-to-peak (TTP) differences (orthogonal - collinear) of the α-coherence for the all pixels in the four ROIs as in B. Time = 0 indicates that peak α-coherence was reached at the same time window in both conditions. There is significantly lower TTP in the collinear than the orthogonal condition in each ROI (p<0.001). Data is from 8 recording session and 2 monkeys.</p

α-coherence maps in collinear and orthogonal conditions.

<p><i>A</i>: Average α-coherence (AAC; averaged over 0–100 ms after stimulus onset) maps in the collinear (left) and orthogonal (right) conditions in one recording session. Each pixel in the map reflects the average AAC of that pixel with the ROI of V1-CE in the collinear (left) and orthogonal (right) conditions. Color denotes coherence values. The ROI of V1-CE (solid black ellipse) and the ROI of V1-flanker (dashed black ellipse) are superimposed on all maps. Inset indicates the 4 ROIs: V1-CE (yellow), V1-flanker (green), V2-CE (red) and V2-flanker (purple) for this recording session. <i>B</i>: AAC maps as in A, but for a different recording session with changed positions of CE and flanker.</p

Retinotopic mapping of the central element and the flanker.

<p><i>A</i>: Schematic illustration of the Gabor stimuli used for retinotopic mapping: the central element (CE, top) and the two flankers, vertically (middle) or horizontally (bottom) oriented were presented in separate trials. Fixation point is marked with a yellow dot. <i>B</i>: Average population response (VSDI amplitude) maps evoked by the stimuli in A. Maps and stimuli in A are presented in a corresponding order (from top to bottom). Color denotes fluorescence change (ΔF/F). The maps show activation patches in V1 for the central element (V1-CE activated area) and the lower flanker (V1-flanker activated area; the upper, more foveal flanker evoked neuronal activation outside the imaged area). In V1, a 2D Gaussian fit of the neuronal activation at the V1-CE activated area (top) and V1-flanker activated area (middle and bottom) are superimposed on the corresponding maps. Inner to outer contours represent the top 10%, 20% and 40% outlines of the Gaussian, respectively. Pixels within the top 10% fitted Gaussian area were defined as the ROIs in V1. In V2 we defined V2-CE and V2-flanker ROIs as pixels exceeding an SNR threshold. <i>C</i>: Blood vessel pattern of the imaged area. Black lines mark the border between V1/V2 and the lunate sulcus (LUS) located between V2 and V4. <i>D</i>: The four ROIs taken for analysis in this specific recording session: V1-CE (yellow), V1-flanker (green) and V2-CE (red) and V2-flanker (purple). <i>E:</i> A schematic illustration of the four ROIs in D in a more general outline. The schematic illustrations in E and D will be used throughout the following Figs.</p

Spectrograms and α-power analysis of the VSDI signal.

<p>Data are from a representative recording session except for F, lower panel. <i>A</i>: Schematic illustration of the visual stimuli conditions: collinear (top) and orthogonal (bottom) conditions in which a central Gabor element (CE) was displayed at 16% contrast and the flanker Gabors were displayed at 64% contrast. The distance between Gabors was set at 0.75° (3λ). Fixation point is marked with a yellow dot. <i>B</i>: Population response (VSDI amplitude) maps evoked by the stimuli in A. Maps and stimuli in A are presented in a corresponding order (from top to bottom). The maps were averaged at 100–200 ms after stimulus onset. Color denotes normalized fluorescence change (ΔF/F). The ROIs of the V1-CE and V1-flanker are superimposed on the maps (solid and dashed black lines, respectively). The inset shows the 4 analyzed ROIs: V1-CE (yellow), V1-flanker (green) and V2-CE (red), V2-flanker (purple). <i>C</i>: VSDI spectrogram for the collinear (top) and orthogonal (bottom) conditions averaged over pixels in V1-CE. Color denotes power in dB. Time 0 is stimulus onset. Frequency range is 6–50 Hz (see <i>Materials and Methods</i>). The α-band is confined between two horizontal dashed lines. <i>D</i>: Average α-power maps (averaged 0–100 ms time window) for the collinear (top) and orthogonal (bottom) conditions. Color denotes α-power in dB. The spatial patterns of the α-power are corresponding to the population response maps depicted in B. <i>E</i>: <i>Top row</i>: VSDI population response for the collinear (blue), orthogonal (red) and fixation alone (green) conditions for the 4 ROIs (from left to right): V1-CE, V1-flanker, V2-CE and V2-flanker. Error bars indicate mean±SEM over trials (n = 27, 29 and 28 trials for the collinear, orthogonal and fixation alone conditions respectively). <i>Bottom row</i>: The same as the top row but for the VSDI α-power. <i>F:</i> A receiver-operating characteristic (ROC) analysis on collinear vs. orthogonal single trials for different neural population measures: average α-power (0–100 ms); average β-power (0–100 ms), average γ-power (0–100 ms), maximal population response, maximal derivative of the population response and time-to-peak of the population response. Top panel: the ROC curves of most population measures for a typical recording session. Bottom panel: the AUC for each neuronal population measure was calculated in each recording session separately and then averaged across all recording sessions. Error bars indicate mean±SEM over recording sessions (n = 8 recording sessions).</p