Cortical functional topography of high-frequency gamma activity relates to perceptual decision: an Intracranial study

<div><p>High-frequency activity (HFA) is believed to subserve a functional role in cognition, but these patterns are often not accessible to scalp EEG recordings. Intracranial studies provide a unique opportunity to link the all-encompassing range of high-frequency patterns with holistic perception. We tested whether the functional topography of HFAs (up to 250Hz) is related to perceptual decision-making. Human intracortical data were recorded (6 subjects; >250channels) during an ambiguous object-recognition task. We found a spatial topography of HFAs reflecting processing anterior dorsal and ventral streams, linked to decision independently of the type of processed object/stimulus category. Three distinct regional fingerprints could be identified, with lower gamma frequency patterns (<45Hz) dominating in the anterior semantic ventral object processing and dorsoventral integrating networks and evolving later, during perceptual decision phases, than early sensory posterior patterns (60-250Hz). This suggests that accurate object recognition/perceptual decision-making is related to distinct spatiotemporal signatures in the low gamma frequency range.</p></div

Analysis of Power per electrode cluster and condition reveals a temporal pattern of differences in power, with anterior object recognition regions showing increased decision related low frequency activity patterns.

<p>Cluster averaged power is plotted with standard deviation. Notably lower frequency band activation emerges after stimulus offset (decision period) for the more anterior electrodes (“green” and “blue”). Color lines (horizontal panels) represent the three clusters of electrodes. The more posterior channels (“orange” labels) have the main pattern increase at high gamma in contrast to the other locations. Black bars in the plots indicate the significant differences between time-windows (p<0.0065; detailed statistical values are reported in Table A in S1 file). No difference was found across stimuli conditions, suggesting that the observed regional patterns reflect a general object recognition mechanism.</p

The topography of high frequency oscillations.

<p>We found distinct high frequency activity patterns during the ambiguous object recognition/perceptual decision task. The position of the electrodes per subject belonging to each of the clusters were marked as dots (in three distinct colors) in the coregistered brain. These patterns have distinct sources in the brain as represented by the correspondent dots. B) The example TF plots are a group average of all the represented electrodes of that cluster (N = 3 subjects for “blue” labels; N = 4 subjects for “orange” and “green” labels). Data (dB) are presented for the Mooney faces condition but these results could be generalized for the other conditions (see Figure A in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0186428#pone.0186428.s001" target="_blank">S1 File</a>). The black line segmented “blobs” in the plots depict the TF spectral–temporal patterns which are significant (blue z = -3.12, p<0.0017; orange, z = 3.11, p<0.0018; green, z = 3.09, p<0.0019). The dashed lines mark the start and end of stimulus.</p

Channel clustering analysis of evoked frequency responses to faces.

<p>A) Frequency response of the 0-600ms time window per channel. Black lines: individual channels over all five subjects from the left hemisphere. B) Channel clusters as computed by the semi-automatic iterative channel clustering procedure. The default Kmeans approach with squared Euclidean distance measure was computed (best sum of distances = 6796; cluster 1 blue = 2327; cluster 2 orange = 2274; cluster 3 green = 2195). Channels belonging to the same centroid (bold lines) are marked with the same line color. The locations of these channels are plotted in the results section.</p

Task timeline: Mooney stimuli (ambiguous black and white shapes) of faces/inverted faces, guitars and scrambled pictures were presented for 250ms.

<p>Subjects had to detect a face (or not) and respond (button press) during the inter-stimulus interval (1900-2150ms). Stimulus order was randomized and the experiment was divided in three runs (100 trials per run) to avoid subject fatigue.</p

Behavioral results.

<p>A) Percentage of responses per stimuli category. *difference between responses per category with p = 0.028. B) Reaction time per stimuli condition. ** p = 0.007. Bars show the group average ± SD (N = 6).</p