Invariance of firing rate and field potential dynamics to stimulus modulation rate in human auditory cortex

Abstract

The effect of stimulus modulation rate on the underlying neural activity in human auditory cortex is not clear. Human studies (using both invasive and noninvasive techniques) have demonstrated that at the population level, auditory cortex follows stimulus envelope. Here we examined the effect of stimulus modulation rate by using a rare opportunity to record both spiking activity and local field potentials (LFP) in auditory cortex of patients during repeated presentations of an audio-visual movie clip presented at normal, double, and quadruple speeds. Mean firing rate during evoked activity remained the same across speeds and the temporal response profile of firing rate modulations at increased stimulus speeds was a linearly scaled version of the response during slower speeds. Additionally, stimulus induced power modulation of local field potentials in the high gamma band (64-128 Hz) exhibited similar temporal scaling as the neuronal firing rate modulations. Our data confirm and extend previous studies in humans and anesthetized animals, supporting a model in which both firing rate, and high-gamma LFP power modulations in auditory cortex follow the temporal envelope of the stimulus across different modulation rates.

Figure 1

Anatomical localization. Electrode location (green dots) displayed on coronal, saggital and axial MRI slices for Patient 1 (top) and Patient 2 (bottom). On the left hemisphere, Patient 1 had a single Heschl's gyrus and the electrode was in the border between the anterior part of Planum Temporale and posterior part of HG. On the right side, this patient had a bifurcated HG and the electrode was in the posterior medial portion of HG. For Patient 2, HG on the left was bifurcated and the electrode was on the posterior part somewhere in the middle on the medial/lateral axis. On the right hemisphere of this patient, HG is trifurcated and the electrode is on the most anterior portion, and somewhere in the middle on the medial/lateral axis. Blue—Superior Temporal Gyrus (STG), red—Heschl's gyrus (HG), and yellow—Planum Temporale.

Figure 2

(A) Correlation vs. smoothing—spikes. For each neuron we calculated the correlation between the two smoothed spike trains in each modulation rate (see Methods). The graph represents the average correlation values of 25 neurons and error bars denote standard error of the mean across all neurons. (B) LFP responses. Correlation between repeated runs was also evaluated for the LFPs at different frequencies (see Methods). Significant correlations were seen only in the high γ‐band. The bars represent the average correlation and standard deviation across 21 LFP channels. (C) Similar to A, we calculated the degree of inter‐run correlation as a function of smoothing level for the high gamma band LFPs.

Figure 3

Firing rate invariance. (A) Average spike count ratio. Average ratio between the number of spikes emitted during the different stimulus modulation rates and the number of spikes emitted during normal speed stimulation. For speed × 1 the value is 1 by definition. (B) Each dot represents the firing rate during a 20‐s segment (x‐axis) plotted against the firing rate of the same neuron during the corresponding 10 s of the double speed stimulation (y‐axis). The regression line and r values are in the top left corner. (C) Same as B, comparing the firing rate during 10‐s segments of double speed stimulation with the firing rate during the corresponding 5 s of the quadruple speed stimulation. (D) Same as B and C comparing 20 s of the normal speed with the corresponding 5 s of the quadruple speed. (E) Ratio of firing rate vs. correlation level. For each time segment, we calculated the ratio of firing rate between normal and double speed and plotted it against the correlation level between the two normal speed runs (see Methods). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 4

Effect of stimulus rate on spike train parameters. (A) For each neuron and each stimulus repetition we computed the distribution of inter‐spike intervals (ISIs) normalized by the total number of spikes. The graph represents the average distribution of ISIs across all cells. Note there is no significant difference in the ISI distribution across different stimulus presentation speeds even at very short ISIs (see inset). (B) Autocorrelation: the average population spike train for each stimulation speed was binned at 500 ms and the autocorrelation function was computed.

Figure 5

Stretch analysis. (A) Average temporal profile of spikes (N = 25 cells) during normal speed presentation (blue traces) superimposed with the temporal profile during double speed presentation stretched in time (red traces; see Stretch analysis in Methods). The figure depicts 2 min of the experiment [starting at 120 (60) s into the normal (double) speed stimulus presentations]. The full time courses for the entire duration of the experiment are provided in supplementary Figures 8 and 9. Correlation level and significance for each time window are in the top left corner. (B) Average correlation level of individual neurons (left) and the population (right) within and across presentation speeds. Error bars denote S.D. across the number of correlation values averaged. (C) Same as (A) for high γ‐band LFP power modulations (N = 21 electrodes).