Prestimulus frontal-parietal coherence predicts auditory detection performance in rats

Abstract

Electrophysiology in primates has implicated long-range neural coherence as a potential mechanism for enhancing sensory detection. To test whether local synchronization and long-range neural coherence support detection performance in rats, we recorded local field potentials (LFPs) in frontal and parietal cortex while rats performed an auditory detection task. We observed significantly elevated power at multiple low frequencies (<15 Hz) preceding the target beep when the animal failed to respond to the signal (misses), in both frontal and parietal cortex. In terms of long-range coherence, we observed significantly more frontal-parietal coherence in the beta band (15-30 Hz) before the signal on misses compared with hits. This effect persisted after regressing away linear trends in the coherence values during a session, showing that the excess frontal-parietal beta coherence prior to misses cannot be explained by slow motivational changes during a session. In addition, a trend toward higher low-frequency (<15 Hz) coherence prior to miss trials compared with hits became highly significant when we rereferenced the LFPs to the mean voltage on each recording array, suggesting that the results are specific to our frontal and parietal areas. These results do not support a role for long-range frontal-parietal coherence or local synchronization in facilitating the detection of external stimuli. Rather, they extend to long-range frontal-parietal coherence previous findings that correlate local synchronization of low-frequency (<15 Hz) oscillations with inattention to external stimuli and synchronization of beta rhythms (15-30 Hz) with voluntary or involuntary prolongation of the current cognitive or motor state.

Keywords: attention; oscillation; synchrony.

Fig. 1.

Auditory detection task and evoked local field potentials (LFPs). A: response latency histogram (50-ms bins) combining all 25 behavioral recording sessions. Response latencies represent the time between the signal beep and the first subsequent lick. Peaked response latency distributions demonstrate nonrandom licking; rats generally responded within 1 s of unpredictably timed auditory cues during the detection task. B: fraction of hit trials in sliding 5-min windows, averaged over recorded detection sessions. Shading denotes SE over sessions; 5 sessions lasted until the 15th window (70–75 min) or longer. C and D: session-averaged frontal (C) and parietal (D) LFPs triggered on the target tone, for hit and miss trials separately.

Fig. 2.

Session-averaged evolution of frontal-parietal coherence on hit vs. miss trials. A and B: average coheregrams for hit (A) and miss (B) trials. Coherence spectra were calculated in 500-ms windows shifted in 50-ms steps, averaged across interarea electrode pairs and then across hit and miss trials separately. The hit and miss coheregrams from each session were then averaged (n = 25) to form the grand coheregrams shown. As the x-axis denotes the start of each half-second window, the last prestimulus window is at −0.5, marked by the arrowheads. C: hit-miss difference coheregram: the difference between the hit and miss coheregrams shown in A and B. D and E: statistical significance and sign of differences between the average hit and miss coheregrams is shown as the P value of a 1-tailed t-test asking whether hit coherence was significantly greater than miss coherence (D) or whether miss coherence was greater than hit coherence (E). Hotter colors indicate greater statistical significance (i.e., smaller P values). In each panel the arrowhead denotes the last prestimulus window.

Fig. 3.

Choice probability analysis of frontal-parietal coherence. To quantify the extent to which single-trial frontal-parietal coherences predict hit or miss trials, choice probabilities (CPs) were calculated based on coherence in each time-frequency bin (500-ms time windows, shifted by 50 ms), averaged over frontal-parietal electrode pairs. A and B: significant difference of CPs from 0.5, indicating that high coherence predicts hit or miss trials, was calculated with a permutation test (P < 0.05, see materials and methods). Color represents % of sessions in which high coherence at each time-frequency bin significantly predicted misses (A) or hits (B). Arrowheads denote the last completely prestimulus half-second window. C and D: distribution of CPs across sessions at 18 Hz for the last prestimulus window (C) and at 46 Hz for the penultimate prestimulus window (−0.45 to −0.05 s) (D), with CPs significantly different from 0.5 in black. A CP significantly greater than 0.5 means that greater coherence predicts hits, while a CP significantly less than 0.5 indicates that higher coherence predicts misses.

Fig. 4.

Prestimulus hit and miss coherence spectra for an example session and individual electrode pair analysis. A: the average coherence spectrum across all frontal-parietal electrode pairs for 1 detection session is plotted for hits and misses. Shading denotes SE based on the variability across trials. B: the P value for a 2-tailed unpaired t-test comparing hit and miss coherences (after tanh transformation, see materials and methods) is plotted as log(1/P) (darker curve) so that higher plotted values indicate more significant (smaller) P values. To account for potential changes in coherence associated with slow changes in rats' motivation, the lighter curve shows the analogous P values for a hit-miss comparison based on residuals of a linear regression on coherence values during each session (i.e., after slow changes have been subtracted out). Frequency bins where either curve exceeds the dotted line were significant at the 95% confidence level; similarly, bins where the curve exceeds 2 on the y-axis were significant at the 99% confidence level [since log(1/0.01) = 2]. C and D: total number (across 25 sessions) of individual frontal-parietal electrode pairs at each frequency bin that showed prestimulus hit coherence significantly greater than miss coherence (C) or vice versa (D), according to a stringent Bonferroni-corrected criterion (t-test, uncorrected α = 0.05).

Fig. 5.

Session-averaged prestimulus frontal-parietal coherence spectra. A: separate frontal-parietal coherence spectra for hit and miss trials were calculated for each session based on the 500 ms prior to each signal beep and then averaged over the 25 sessions. The variability of these average coherence spectra across sessions is indicated by the shading denoting SE calculated from variability of the hit and miss coherence spectra across sessions. B: the P value for a 2-tailed t-test comparing hit and miss coherences (see materials and methods) is plotted as log(1/P) (darker curve) so that higher plotted values indicate more significant (smaller) P values. To account for potential changes in coherence associated with slow changes in rats' motivation, the lighter curve shows the analogous P values for a hit-miss comparison based on residuals of a linear regression on coherence values during each session (i.e., after slow changes have been subtracted out). Frequency bins where either curve exceeds the dotted line were significant at the 95% confidence level; similarly, bins where the curve exceeds 2 on the y-axis were significant at the 99% confidence level [since log(1/0.01) = 2].

Fig. 6.

Session-averaged hit and miss spectrograms for frontal and parietal cortex. Power spectra were calculated in 500-ms windows shifted in 50-ms steps, averaged across frontal and parietal electrodes separately and then across hit and miss trials separately. A: average frontal hit spectrogram. B: parietal hit spectrogram. C: frontal miss spectrogram. D: parietal miss spectrogram. Arrowheads indicate the last prestimulus time-window. Color represents power in (nV)² × 10⁻⁴. E and F: difference between hit and miss spectrograms (hit − miss) for frontal (E) and parietal (F) electrodes. Color represents power in (nV)² × 10⁻⁵. G and H: statistical significance of differences between the average hit and miss spectrograms is shown as the P value of a 1-tailed t-test asking whether miss power was greater than hit power for frontal (G) and parietal (H) electrodes. Hotter colors indicate greater statistical significance (i.e., smaller P values). (There were no significant time-frequency bins for the converse question asking whether hit power was greater than miss power, so the results are not shown.) In each panel the arrowhead denotes the last prestimulus window.