Directional coupling from the olfactory bulb to the hippocampus during a go/no-go odor discrimination task

Abstract

The hippocampus and olfactory regions are anatomically close, and both play a major role in memory formation. However, the way they interact during odor processing is still unclear. In both areas, strong oscillations of the local field potential (LFP) can be recorded, and are modulated by behavior. In particular, in the olfactory system, the beta rhythm (15-35 Hz) is associated with cognitive processing of an olfactory stimulus. Using LFP recordings in the olfactory bulb and dorsal and ventral hippocampus during performance of an olfactory go/no-go task in rats, we previously showed that beta oscillations are also present in the hippocampus, coherent with those in the olfactory bulb, during odor sampling. In this study, we provide further insight into information transfer in the olfacto-hippocampal network by using directional coherence (DCOH estimate), a method based on the temporal relation between two or more signals in the frequency domain. In the theta band (6-12 Hz), coherence between the olfactory bulb (OB) and the hippocampus (HPC) is weak and can be both in the feedback and feedforward directions. However, at this frequency, modulation of the coupling between the dorsal and ventral hippocampus is seen during stimulus expectation versus odor processing. In the beta frequency band (15-35 Hz), analysis showed a strong unidirectional coupling from the OB to dorsal and ventral HPC, indicating that, during odor processing, beta oscillations in the hippocampus are driven by the olfactory bulb.

Fig. 1.

Examples of local field potential (LFP) recordings during odor sampling of heptanol (CS+) and hexanol (CS−) (animal 31, day 2, criterion level). A and B: signals recorded in the olfactory bulb and the ventral and dorsal hippocampus filtered between 15 and 60 Hz (blue) and between 6 and 12 Hz (red). C–H: spectrotemporal histograms of significant power increase over 76 trials in the olfactory bulb (OB: C and F), ventral hippocampus (VH; D and G), and dorsal hippocampus (DH; E and H). For a given trial, the power spectral density (PSD) estimate is computed by classical spectrograms between −4 and 4 s around odor onset; for each frequency, 2.5 and 97.5% levels are estimated from all the points and the trials within the interval from −3 to −1 s. At a given time and frequency, each value of a spectrotemporal histogram of significant power increase is the percentage over trials of PSD values above the 97.5% level. (Decreases were not significant and are shown in Supplementary Fig. S1.)

Fig. 2.

Example of averaged directional coherence (DCOH) spectra for the flows between each pair of structures (OB, DH, VH) estimated for 2 time intervals: before odor onset (−3 to −1 s, dotted line) and during odor sampling (0–2 s, solid line) (animal 31, 2nd session). Top: CS+. Bottom: CS−. + indicates each frequency where the DCOH spectrum is significantly increased during odor sampling compared with the −3 to −1 s time interval. o indicates a significant decrease.

Fig. 3.

Averaged difference over trials between DCOH spectrum before and after odor onset for heptanol (CS+). Left: rat and session numbers. Structures and flow directions are on the top of plots. Dark lines indicate significant increase, and light lines decreases at the given frequency.

Fig. 4.

Summary of significant directional flow increases (coupling) and decreases (uncoupling) between available structures for (A) beta 15–35 Hz and (B) theta 6–12 Hz frequency bands for all rats. Significant relationships between 2 structures are counted over animals and sessions for each pair of structures (among OB, DH, VH), each odor pair [heptanol CS+/hexanol CS− (HH), geraniol CS+/citral CS− (GC), and citral CS+/geraniol CS− (GCrev)], and condition (CS+, CS−), and each flow direction (see legend at the bottom). For 1 animal and 1 session, a flow increase is counted in the direction structure 1 to 2 if, for at least 1 frequency within the frequency band, the Wilcoxon test comparing DCOH before/after odor onset was found significant in the upper tail of the test (see Fig. 3). A significant flow decrease corresponds to lower tails of the same Wilcoxon tests. Counted flows are reported in bars in darker gray in the direction structure 1 to 2 and in lighter gray for structure 2 to 1. The same pair of gray shades are used for CS+ and CS− conditions, with different pairs for coupling (black/light gray, increase/decrease) vs. uncoupling (medium gray/white, increase/decrease). Coupling and uncoupling in a given direction are symbolized by filled arrows and empty arrows with a line through, respectively, the arrow size being proportional to the number of corresponding significant flows for both conditions. For cases in which instances of both coupling and uncoupling were seen across subjects and sessions, the arrows represent the majority activity.

Fig. 5.

Correlation between oscillation power in OB and coupling strength (OB→VH top line and OB→DH bottom line) in the beta band. For the 3 odor pairs (HH, GC, and GCrev in columns), and both contingencies CS+ and CS− (o and x signs, respectively): x-axis is the mean time-frequency PSD during odor sampling (0–2 s); y-axis is the mean DCOH increase [preodor period (−3 to −1 s) subtracted from odor sampling period (0–2 s)]. Each value corresponds to 1 animal and 1 session (day of experiment). Lines are linear regression fitting (plain line for CS+ and dashed line for CS− condition); correlation coefficients are reported on each corresponding subplot.

Fig. 6.

Influence of the behavioral response (correct vs. incorrect) for the CS− odors. Beta band coupling over sessions (x-axis) for each animal (in columns), each odor pair (A) HH, (B) GC, and (C) GCrev, and flows OB toward VH and DH (top and middle horizontal panels, respectively). Vertical bars are SE. Sessions of the CS− condition where coupling is different between the 2 responses (correct or incorrect) are indicated by an asterisk (P < 0.05). In the bottom horizontal panel, the percentage of correct behavioral responses among each session is shown for CS+ and CS− (dark and light colors, respectively); c on the top of bars indicates sessions where criterion is attained, which was set at 90% correct in 2 successive 20 trial blocks.

Fig. 7.

Relation between behavioral level and coupling strength. Values for each behavioral level (beg, beginner; crit, criterion; post, postcriterion) represent the average across all trials and animals of beta frequency band (15–35 Hz) coupling strength from OB toward VH (top) and DH (bottom) for each odor set (HH, GC, and GCrev, in columns) and for both CS+ and CS− (plain and dashed lines, respectively). The coupling strength is the DCOH averaged over the beta band before the odor (−3 to −1 s) subtracted from that during the odor (0–2 s) in ordinate. Asterisks indicate significant difference in coupling between 2 behavioral levels (P < 0.05) for CS+; triangle indicates significant difference between CS+ and CS− in a given behavioral level (P < 0.05).