Figure 3.

Robust Enhancement of Theta-Gamma Coupling in the Dentate Gyrus during Rearing Events

(A) Anatomical sketch that depicts the main inputs of CA1 pyramidal and dentate granule cells. Sch, Schaffer; TA, temporoammonic; LPP, lateral perforant; MPP, medial perforant pathways.

(B) CSD wavelet spectrograms indicate the characteristic gamma bands and their theta phase along the hippocampal formation. Pr, pyramidal layer; Rd, radiatum; LM, lacunosum-moleculare; DG, dentate gyrus.

(C) Independent-component analysis (ICA) of hippocampal LFPs resulted in five main components (ICs), three restricted to the CA1 area and two to the dentate gyrus. Top row: voltage loadings of the five identified LFP generators in the hippocampal formation (from left to right: CA1pyr, CA1 pyramidal layer; rad, radiatum; LM, lacunosum-moleculare; LPP, lateral perforant path; MPP, medial performant path generators; from top to bottom: Pr, pyramidal layer; LM, lacunosum-moleculare; GCL, granule cell layer). Bottom row: CSD loadings of the same generators. In the dentate gyrus one component had maximal negative amplitude in the outer molecular layer (LPP) and the other (MPP) in the middle of it and both had positive polarity through the granular layer and the hilus.

(D) Average cross-frequency-amplitude comodulograms for the five ICs during running (averages of n = 5 animals).

(E) Average theta phase-gamma amplitude coupling matrices for the five ICs during running (averages of n = 5 animals). Two theta cycles are shown for visualization purposes. Top dashed trace indicates theta oscillation in the CA1 pyramidal layer. Note the opposite theta-phase preference of LM and MPP gamma oscillations, matching the phase distribution of entorhinal layer II and III spiking and local gamma oscillations (Fernández-Ruiz et al., 2017). (D) and (E) were calculated from IC segments during which the animal movement speed was above 0.04 m/s for at least 2 s.

(F) Fast gamma in the dentate gyrus. First row: filtered (5–12 Hz) CA1 pyramidal layer LFP; second row: 120–150 Hz filtered lacunosum-moleculare LFP; third row: 120–150 Hz filtered dentate gyrus LFP; bottom row: wavelet spectrogram of the dentate gyrus LFP. Red arrows highlight fast gamma transients on the dentate gyrus recordings and corresponding wavelet spectrogram. Vertical dashed lines indicate the pyramidal layer theta troughs. Fast gamma components were not detected in the lacunosum-moleculare LFP.

(G) Average comodulograms of the five ICs for different time intervals around rearing peak (averages of n = 5 animals). Plots were constructed by averaging individual comodulograms from five animals followed by the subtraction of baseline (−10 to −5 s to rearing peak) comodulograms. Red rectangle highlights comodulograms at rearing peak (0 s). Note the robust enhancement of the theta coupling of the medial perforant path generator (MPP).

(H) Average perievent modulation index values of the five ICs (rows) in three different gamma frequency bands (columns; averages of n = 5 animals, brown traces indicate the shuffled control, shaded area represents the 99% band of the shuffled control). Vertical dashed lines at zero indicates rearing peak. The dentate fast gamma (MPP generator) has broad frequency range appearing in both 50–100 Hz and 120–150 Hz frequency bands.

(I) The coupling of LM mid gamma and MPP dentate fast gamma to theta oscillation increases with running speed. However, rearing-coupled MPP theta-gamma coupling is about two times larger than that is observed during running (^∗p < 0.05, paired t test; n = 5 animals; values are mean ± SEM).

See also Figure S3.