Theta oscillations and sensorimotor performance

Abstract

Performance and cognitive effort in humans have recently been related to amplitude and multisite coherence of alpha (7-12 Hz) and theta (4-7 Hz) band electroencephalogram oscillations. I examined this phenomenon in rats by using theta band oscillations of the local field potential to signify sniffing as a sensorimotor process. Olfactory bulb (OB) theta oscillations are coherent with those in the dorsal hippocampus (HPC) during odor sniffing in a two-odor olfactory discrimination task. Coherence is restricted to the high-frequency theta band (6-12 Hz) associated with directed sniffing in the OB and type 1 theta in the HPC. Coherence and performance fluctuate on a time scale of several minutes. Coherence magnitude is positively correlated with performance in the two-odor condition but not in extended runs of single odor conditional-stimulus-positive trials. Simultaneous with enhanced OB-HPC theta band coherence during odor sniffing is a significant decrease in lateral entorhinal cortex (EC)-HPC and OB-EC coherence, suggesting that linkage of the olfactory and hippocampal theta rhythms is not through the synaptic relay from OB to HPC in the lateral EC. OB-HPC coupling at the sniffing frequency is proposed as a mechanism underlying olfactory sensorimotor effort as a cognitive process.

Fig. 1.

Trial design and sample data. (a) Schematic of the fixed timing of trials showing successive CS⁺ odor (A), plain air (O) and CS^- odor (B) trials. P, no press period. (b) Examples of lever pressing performance showing that the rats can anticipate the arrival of the odor stimulus. Dark traces are correct CS⁺ trials, and dashed traces are incorrect CS⁺ trials. Vertical gray lines surround the no press period, and the vertical black line indicates the odor onset time. (c) Simultaneously recorded data from the four brain areas. Theta band data are 1-20 Hz. Raw data (1-300 Hz) are shown for the OB and HPC. Note the change in character of the theta rhythm beginning with the onset of the no press period and again with the odor onset, transitioning in the OB to low amplitude and high frequency, which is consistent with the transition to sniffing.

Fig. 2.

Dynamic power spectra show changes over the behavioral epochs. Averaged power spectra are shown for the four recording sites across a set of 25 nonconsecutive CS⁺ trials chosen for similarity in response time. Spectra are estimated for each 1,024-ms time window, stepped by 250 ms. Odor onset is indicated by the vertical white line at 3.5 s, and the average response time ± standard deviation is shown below each matrix (red horizontal bar). Color scale indicates log dimensionless power and is constant for the four plots. (a) OB frequencies occupy all parts of the theta band, with 7-10 Hz predominating during the sniffing period. (b) aPC theta is similar to that in the OB. (c)EC theta oscillations cover the lower end of the theta band, from 4 to 7 Hz, rarely showing peaks in the higher portion of the band. (d) HPC theta occupies two bands corresponding to the definitions of type 1 (7-12 Hz) and type 2 (4-6 Hz) theta. Very low-frequency power in all spectra is due to the 1/f nature of the power spectra in most cortical areas. The data have been log-transformed to attenuate this effect.

Fig. 3.

Dynamic coherence spectra show differences in functional connectivity across behavioral epochs. Pairwise coherence spectra are shown for the same data as in Fig. 2. (a) OB-aPC. (b) OB-EC. (c) OB-HPC. (d) EC-HPC. Note significant coherence after odor onset for the OB-HPC pair and the interruption of coherence for the OB-EC and EC-HPC pairs. The yellow square in c marks the time and frequency domain in which coherence occurs during odor sniffing. This segment of data is used for the coherence statistics represented in Figs. 5 and 11. OB-EC coherence can be strong or weak in the prestimulus period. Examples of strong OB-EC coherence, also interrupted with the onset of odor sniffing, are shown in Fig. 7. Scale is constant for the four plots, with dark blue representing the threshold for significance as compared with shuffled data. The overall performance for this experiment was 68.3%. (More OB-HPC coherence examples are shown in Fig. 8.)

Fig. 4.

Functional connectivity may vary during the course of a test session. Longitudinal coherence from the odor sniffing period (3.25-4.25 s) is shown for four electrode pairs. Each horizontal point is estimated from 15 consecutive CS⁺ trials ending with the trial number on the horizontal axis. Values of lighter hue than the dark blue background are significantly above the average coherence values for shuffled data. (a) OB-aPC. The dominant coherence band matches the sniffing frequency estimated from the OB theta frequency during odor sampling (7.8 Hz). (b) OB-EC. There is virtually no coherence between these two areas in the theta band during odor sniffing. (c) OB-HPC. The OB (lower solid white trace) and HPC (dashed white line) peak high theta frequencies (7-13 Hz) are shown overlaid, as are performance statistics (upper solid white trace; right axis). Note the long stretch of trials in which significant coherence is seen in the band spanned by the OB and HPC peak theta frequencies and that this corresponds to an extended period of higher performance values. The region indicated by the yellow line is a run of CS⁺ trials delivered at the end of the session. (d) EC-HPC. There is no coherence in this band during odor sniffing; although, during other periods, the coherence is high (see Fig. 3d).

Fig. 5.

Correlation between OB-HPC coherence and performance in the two-odor task is consistently positive. Coherence magnitude is the average coherence in the frequency band spanned by the peak OB and HPC high theta frequencies during odor sniffing. (a) Correlation plot for data from Fig. 4c. The crosses fit by the solid line show positive correlation in the two-odor condition (half-overlapping windows also show significant correlation; R = 0.60, P < 0.05). The open circles fit by the dashed line represent the CS⁺-only run at the end of the session. Note that the correlation in this period is insignificant, even though some time windows do show significant coherence. The dashed line marked “shuffle” in all plots shows the correlation for the same data with the coherence estimated from OB and HPC data in mismatched trials. (b) Correlation for a different session from the same rat. (c) Correlation for a session from another rat (more examples in Fig. 10). (d) Positive correlation during the two-odor portion of a session and negative correlation during a one-odor run at the end. The longitudinal coherence plots for b, c, and d are in Fig. 11.