How global are olfactory bulb oscillations?

Abstract

Previous studies in waking animals have shown that the frequency structure of olfactory bulb (OB) local field potential oscillations is very similar across the OB, but large low-impedance surface electrodes may have favored highly coherent events, averaging out local inhomogeneities. We tested the hypothesis that OB oscillations represent spatially homogeneous phenomena at all scales. We used pairs of concentric electrodes (200 μm outer shaft surrounding an inner 2-3 μm recording site) beginning on the dorsal OB at anterior and medial locations in urethane-anesthetized rats and measured local field potential responses at successive 200 μm depths before and during odor stimulation. Within locations (outer vs. inner lead on a single probe), on the time scale of 0.5 s, coherence in all frequency bands was significant, but on larger time scales (10 s), only respiratory (1-4 Hz) and beta (15-30 Hz) oscillations showed prominent peaks. Across locations, coherence in all frequency bands was significantly lower for both sizes of electrodes at all depths but the most superficial 600 μm. Near the pial surface, coherence across outer (larger) electrodes at different sites was equal to coherence across outer and inner (small) electrodes within a single site and larger than coherence across inner electrodes at different sites. Overall, the beta band showed the largest coherence across bulbar sites and electrodes. Therefore larger electrodes at the surface of the OB favor globally coherent events, and at all depths, coherence depends on the type of oscillation (beta or gamma) and duration of the analysis window.

Fig. 1.

Electrodes, recording sites, and sample data. A: left: concentric electrode—an outer insulated stainless steel cannula with the end ring exposed (200 μm diam, ∼100 KΩ impedance) surrounds an inner tungsten microelectrode with a 1–3 μm tip (∼1–4 MΩ impedance). Right: electrode positions relative to the olfactory bulb (OB) layers; both electrodes begin with the outer cannula on the surface of the OB and the inner probe at a depth of 200 μm. The probes are advanced in 200 μm increments to a depth of 2 mm. After the probes cross the mitral cell layer, the different depths of the OB at the anterior and medial locations causes the 2 probes to be in different parts of the cortex. Dashed lines indicate an example of the extent of travel for the probes. B: sample signals from 2 concentric electrodes (ant, anterior; med, medial; O, outer; I, inner; 5 s of data are shown). Top 4 traces are raw local field potentials (LFPs; 0.3–300 Hz). Note that the 2 anterior and 2 medial leads are more similar to each other than either is with the other location. Below the raw data are the gamma band–filtered (30–75 Hz) traces from anterior and medial inner electrodes. The trace labeled deep θ is the surrogate of the respiratory wave from an electrode that is placed in the granule cell layer in the deep posterior OB (low-pass filter at 4 Hz). Markers above the theta trace note automatically detected peaks.

Fig. 2.

Power and coherence spectra by depth. A: power spectra, 10 s windows. Power was computed from 6 10-s windows across the 10 rats at each depth for each recording site (ant, anterior; med, medial; O, outer; I, inner). Semilog plots for each depth are displayed with the depth in micrometers above each plot. Error bands around each power estimate represent the 95% confidence range from jackknife power estimates. Note the primary gamma peak at ∼50 Hz and the lower gamma or high beta peak at ∼35 Hz, particularly in the deep layers. B: Z-coherence, 10 s windows. Z-coherence was computed from the same 10 s time windows as in A, and the error bands are the 95% confidence estimates from jackknife z-coherence estimates. Note that the only prominent peaks from 10 s windows are in the lower frequency ranges: beta and theta. A weak 35 Hz peak also emerges in the deep layers. Z-coherence in the 1st 3 layers is as high for the outer cross-site pair of leads as it is for the outer-inner within-site pairs. By 1,000–1,200 μm in depth, the outer and inner cross-site pair coherence values are the same. The gray traces at the bottom of the top left panel are the coherence values from shuffled data.

Fig. 3.

Short time window coherence spectra by depth. A: 0.5 s windows, odor periods. Z-coherence was computed from 20 nonoverlapping 0.5 s windows during odor stimulation comprising the same 10 s windows as in Fig. 2, and gamma peaks are now evident at all depths but not on every pair of leads. The largest coherence values are from within-site (outer-inner) estimates. Prominent peaks are also present in the beta band and at ∼35 Hz as a shoulder to the beta peak. Error bands are the 95% confidence estimates from jackknife Z-coherence estimates. The gray traces at the bottom of the top left panel are the coherence values from shuffled data. B: 0.5 s windows, prestimulus periods. Z-coherence was computed from 20 nonoverlapping 0.5 s windows comprising the 10 s prestimulus periods just before each odor period. Note that gamma band peaks are less prominent when odors are absent.