Endogenous fluctuations in cortical state selectively enhance different modes of sensory processing in human temporal lobe

The degree of synchronized fluctuations in neocortical network activity can vary widely during alertness. One influential idea that has emerged over the past few decades is that perceptual decisions are more accurate when the state of population activity is desynchronized. This suggests that optimal task performance may occur during a particular cortical state – the desynchronized state. Here we show that, contrary to this view, cortical state can both facilitate and suppress perceptual performance in a task-dependent manner. We performed electrical recordings from surface-implanted grid electrodes in the temporal lobe while human subjects completed two perceptual tasks. We found that when local population activity is in a synchronized state, network and perceptual performance are enhanced in a detection task and impaired in a discrimination task, but these modulatory effects are reversed when population activity is desynchronized. These findings indicate that the brain has adapted to take advantage of endogenous fluctuations in the state of neural populations in temporal cortex to selectively enhance different modes of sensory processing during perception in a state-dependent manner.


Figure S1 :
Figure S1: Power spectra for correct and incorrect trials.(a) Average power spectra of the IFP signal during the 400 ms pre-stimulus window depicting differences in average voltage-squared power between correct trials (blue) and incorrect trials (red) during detection task.(b) Same as (a) but for discrimination task.To improve the clarity of illustration, the total frequency band of interest (2.5-80 Hz) was divided into three distinct groups as follows: (delta + theta + alpha; 2.5-12 Hz; left), (beta; 12-30 Hz; middle), and (gamma; 30-80 Hz; right).Shaded regions represent standard error of mean.

Figure S2 .Figure S3 .
Figure S2.Average spectrograms: Average (n=97) spectrograms for both detection and discrimination tasks, highlighting the distinctions in ongoing IFP activity between correct and incorrect groups of trials.The magnitude values have been normalized between 0 and 1 for each frequency, and spectrograms from all electrodes across the four subjects have been pooled together.

Figure S7 :
FigureS7: Perceptual performance as a function of PR.Perceptual performance for both detection (blue) and discrimination (red) tasks using three equally sized bins of PR values.The bins were created using PR percentiles: the low bin corresponds to values between 0-33.33,medium bin between 33.33-66.67,and high bin between 66.67-100 percentiles.Vertical lines represent standard error of means (** p=0.0023, *** p=0.0019, bootstrapping with 1,000,000 iterations).

Figure S9 :
Figure S9: Relationship between pre-stimulus PR values and reaction times.Box plot summarizing the Pearson correlation coefficient between pre-stimulus PR values and the subsequent reaction times during correct trials in subjects performing detection (blue) and discrimination (red) tasks.We found a significant negative correlation between reaction time and PR values (r=-0.042,p=0.006, n=97 independent electrodes, one-sided Wilcoxon signed-rank test for negative median) in the detection task.In contrast, we found a significant positive correlation between reaction time and PR values (r=0.11,p=2.4e-5, n=97 independent electrodes, one-sided Wilcoxon signed-rank test for positive median) in the discrimination task.** p<0.01.The box plot's midline represents the median, the edges mark the quartiles, and the whiskers show the range.Notches indicate the 95% confidence interval of the median.

Figure S10 :
Figure S10: Comparison of evoked responses and electrode localization to sub-regions of the temporal lobe between low and high state-correlated electrodes.(a) Box plot comparing the evoked responses of low (blue) and high (red) state-correlated electrodes in the four subjects during the 200 ms test stimulus of the detection task (S1: n=8, S2: n=12, S3: n=7, S4: n=6).n.s.p>0.05, two-sided Wilcoxon rank sum test.(b) Same as (a) but for discrimination task.(c) Box plot illustrating the likelihood of an electrode, exhibiting low (blue) or high (red) state-correlation with the population, being positioned in various sub-regions of the temporal lobe in detection task.'p' values are computed using Kruskal-Wallis multiple comparison test by ranks.(Middle temporal gyrus: n=4, Superior temporal gyrus: n=4, Inferior temporal gyrus: n=4, Temporal pole: n=2, Fusiform gyrus: n=3, Parahippocampal gyrus: n=3 independent subjects) (d) Same as (c) but for discrimination task.The box plot's midline represents the median, the edges mark the quartiles, and the whiskers show the range.

Figure S11 :
Figure S11: Chance level same-state probability.Distribution of same-state probabilities calculated after shuffling PR values at each individual electrode across trials.The mean of this distribution provided the chance level same-state probability: 0.5000 ± 0.061 (mean ± standard deviation).