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Two distinct olfactory bulb sublaminar networks involved in gamma and beta oscillation generation: a CSD study in the anesthetized rat.

Fourcaud-Trocmé N, Courtiol E, Buonviso N - Front Neural Circuits (2014)

Bottom Line: In contrast, the generation of beta oscillation involves the lower part of the EPL and deep granule cells.This differential involvement of sublaminar networks is neither dependent on odor quality nor on the precise frequency of the fast oscillation under study.Overall, this study demonstrates a functional sublaminar organization of the rat OB, which is supported by previous anatomical findings.

View Article: PubMed Central - PubMed

Affiliation: Team Olfaction from Coding to Memory, Center for Research in Neuroscience of Lyon, CNRS UMR5292 - INSERM U1028 Lyon, France ; Team Olfaction from Coding to Memory, Center for Research in Neuroscience of Lyon, Université Claude Bernard Lyon 1 Lyon, France.

ABSTRACT
A prominent feature of olfactory bulb (OB) dynamics is the expression of characteristic local field potential (LFP) rhythms, including a slow respiration-related rhythm and two fast alternating oscillatory rhythms, beta (15-30 Hz) and gamma (40-90 Hz). All of these rhythms are implicated in olfactory coding. Fast oscillatory rhythms are known to involve the mitral-granule cell loop. Although the underlying mechanisms of gamma oscillation have been studied, the origin of beta oscillation remains poorly understood. Whether these two different rhythms share the same underlying mechanism is unknown. This study uses a quantitative and detailed current-source density (CSD) analysis combined with multi-unit activity (MUA) recordings to shed light on this question in freely breathing anesthetized rats. In particular, we show that gamma oscillation generation involves mainly the upper half of the external plexiform layer (EPL) and superficial areas of granule cell layer (GRL). In contrast, the generation of beta oscillation involves the lower part of the EPL and deep granule cells. This differential involvement of sublaminar networks is neither dependent on odor quality nor on the precise frequency of the fast oscillation under study. Overall, this study demonstrates a functional sublaminar organization of the rat OB, which is supported by previous anatomical findings.

Show MeSH
CSD analyses of fast rhythms revealed that different sub-layers of the OB network are involved in beta and gamma oscillation generation. (A) Time evolution of the CSD for a single multielectrode recording filtered in three different frequency bands (from top to bottom: 10–100 Hz, 40–90 Hz, and 15–30 Hz). The plotted time represents a single respiratory cycle. Below is the raw signal recorded from the deepest electrode in the GRL, on which are superimposed the detected gamma and beta oscillations. Visual comparison of the different CSD maps (use the black dashed lines as a guide) shows that the major current sources and sinks during beta and gamma oscillations appear at different layers, spaced by one to two electrodes, i.e., 50–100 μm. (B) Time evolution of the group average CSD maps across the gamma (left) and beta (right) cycles. Statistical significances are given as an electrode-by-electrode CSD amplitude comparison (range of recording sites averaged per electrode: N = 9–18). The current sink in the EPL was present in more superficial layers during the gamma oscillation. (C) Average amplitude of sink/source oscillation at each electrode during gamma (black) and beta (red) oscillations (error bars indicate the standard deviations). These data were obtained with electrodes spaced at 100-μm intervals. The results confirm the spatial shift between gamma and beta current sources/sinks observed in (A and B) and additionally show that the beta oscillation is involved in a larger zone of the GRL. Statistical significances are assessed as in (B). Note that the solid line corresponds to the amplitude of the group CSD modulation and the dashed line is the average of individual CSD amplitude modulation, on which statistical testing was performed.
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Figure 2: CSD analyses of fast rhythms revealed that different sub-layers of the OB network are involved in beta and gamma oscillation generation. (A) Time evolution of the CSD for a single multielectrode recording filtered in three different frequency bands (from top to bottom: 10–100 Hz, 40–90 Hz, and 15–30 Hz). The plotted time represents a single respiratory cycle. Below is the raw signal recorded from the deepest electrode in the GRL, on which are superimposed the detected gamma and beta oscillations. Visual comparison of the different CSD maps (use the black dashed lines as a guide) shows that the major current sources and sinks during beta and gamma oscillations appear at different layers, spaced by one to two electrodes, i.e., 50–100 μm. (B) Time evolution of the group average CSD maps across the gamma (left) and beta (right) cycles. Statistical significances are given as an electrode-by-electrode CSD amplitude comparison (range of recording sites averaged per electrode: N = 9–18). The current sink in the EPL was present in more superficial layers during the gamma oscillation. (C) Average amplitude of sink/source oscillation at each electrode during gamma (black) and beta (red) oscillations (error bars indicate the standard deviations). These data were obtained with electrodes spaced at 100-μm intervals. The results confirm the spatial shift between gamma and beta current sources/sinks observed in (A and B) and additionally show that the beta oscillation is involved in a larger zone of the GRL. Statistical significances are assessed as in (B). Note that the solid line corresponds to the amplitude of the group CSD modulation and the dashed line is the average of individual CSD amplitude modulation, on which statistical testing was performed.

Mentions: The layered and approximately spherical organization of the OB allows the computation of the CSD in one dimension (Rall and Shepherd, 1968). For each recording site, the CSD maps were computed with the inverse current-source density method (iCSD, Pettersen et al., 2006). Compared with standard methods, which require an estimate of the LFP spatial second derivative (Mitzdorf, 1985), the iCSD method computes a model of the LFP assuming an arbitrary distribution of sources or sinks across electrodes and then reverses the model to obtain the estimated sources and sinks from the actual data. This process accounts for the long-range influence of sinks and sources and enables the acquisition of a CSD estimation for every electrode, including electrodes at the ends of the silicon probe. To attenuate signal variability, sinks and sources were smoothed by computing the CSD and then spatially averaging over three electrodes, which produced very similar results to a standard CSD method that computes the spatial second derivative of the raw signal. Following standard assumptions (see Rall and Shepherd, 1968, for a discussion), we considered the tissue resistivity to be the same throughout and assumed that average extracellular currents flowed parallel to the probe. As the tissue resistivity was unknown, the CSD was expressed in arbitrary units (a.u.). Finally, the CSD was generally computed for a given frequency band only (except in Figure 8, left panels). This calculation was achieved by filtering the raw data prior to computing the CSD or performing any averaging (fast Fourier transform-filtering performed on the whole 15-s trial).


Two distinct olfactory bulb sublaminar networks involved in gamma and beta oscillation generation: a CSD study in the anesthetized rat.

Fourcaud-Trocmé N, Courtiol E, Buonviso N - Front Neural Circuits (2014)

CSD analyses of fast rhythms revealed that different sub-layers of the OB network are involved in beta and gamma oscillation generation. (A) Time evolution of the CSD for a single multielectrode recording filtered in three different frequency bands (from top to bottom: 10–100 Hz, 40–90 Hz, and 15–30 Hz). The plotted time represents a single respiratory cycle. Below is the raw signal recorded from the deepest electrode in the GRL, on which are superimposed the detected gamma and beta oscillations. Visual comparison of the different CSD maps (use the black dashed lines as a guide) shows that the major current sources and sinks during beta and gamma oscillations appear at different layers, spaced by one to two electrodes, i.e., 50–100 μm. (B) Time evolution of the group average CSD maps across the gamma (left) and beta (right) cycles. Statistical significances are given as an electrode-by-electrode CSD amplitude comparison (range of recording sites averaged per electrode: N = 9–18). The current sink in the EPL was present in more superficial layers during the gamma oscillation. (C) Average amplitude of sink/source oscillation at each electrode during gamma (black) and beta (red) oscillations (error bars indicate the standard deviations). These data were obtained with electrodes spaced at 100-μm intervals. The results confirm the spatial shift between gamma and beta current sources/sinks observed in (A and B) and additionally show that the beta oscillation is involved in a larger zone of the GRL. Statistical significances are assessed as in (B). Note that the solid line corresponds to the amplitude of the group CSD modulation and the dashed line is the average of individual CSD amplitude modulation, on which statistical testing was performed.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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Figure 2: CSD analyses of fast rhythms revealed that different sub-layers of the OB network are involved in beta and gamma oscillation generation. (A) Time evolution of the CSD for a single multielectrode recording filtered in three different frequency bands (from top to bottom: 10–100 Hz, 40–90 Hz, and 15–30 Hz). The plotted time represents a single respiratory cycle. Below is the raw signal recorded from the deepest electrode in the GRL, on which are superimposed the detected gamma and beta oscillations. Visual comparison of the different CSD maps (use the black dashed lines as a guide) shows that the major current sources and sinks during beta and gamma oscillations appear at different layers, spaced by one to two electrodes, i.e., 50–100 μm. (B) Time evolution of the group average CSD maps across the gamma (left) and beta (right) cycles. Statistical significances are given as an electrode-by-electrode CSD amplitude comparison (range of recording sites averaged per electrode: N = 9–18). The current sink in the EPL was present in more superficial layers during the gamma oscillation. (C) Average amplitude of sink/source oscillation at each electrode during gamma (black) and beta (red) oscillations (error bars indicate the standard deviations). These data were obtained with electrodes spaced at 100-μm intervals. The results confirm the spatial shift between gamma and beta current sources/sinks observed in (A and B) and additionally show that the beta oscillation is involved in a larger zone of the GRL. Statistical significances are assessed as in (B). Note that the solid line corresponds to the amplitude of the group CSD modulation and the dashed line is the average of individual CSD amplitude modulation, on which statistical testing was performed.
Mentions: The layered and approximately spherical organization of the OB allows the computation of the CSD in one dimension (Rall and Shepherd, 1968). For each recording site, the CSD maps were computed with the inverse current-source density method (iCSD, Pettersen et al., 2006). Compared with standard methods, which require an estimate of the LFP spatial second derivative (Mitzdorf, 1985), the iCSD method computes a model of the LFP assuming an arbitrary distribution of sources or sinks across electrodes and then reverses the model to obtain the estimated sources and sinks from the actual data. This process accounts for the long-range influence of sinks and sources and enables the acquisition of a CSD estimation for every electrode, including electrodes at the ends of the silicon probe. To attenuate signal variability, sinks and sources were smoothed by computing the CSD and then spatially averaging over three electrodes, which produced very similar results to a standard CSD method that computes the spatial second derivative of the raw signal. Following standard assumptions (see Rall and Shepherd, 1968, for a discussion), we considered the tissue resistivity to be the same throughout and assumed that average extracellular currents flowed parallel to the probe. As the tissue resistivity was unknown, the CSD was expressed in arbitrary units (a.u.). Finally, the CSD was generally computed for a given frequency band only (except in Figure 8, left panels). This calculation was achieved by filtering the raw data prior to computing the CSD or performing any averaging (fast Fourier transform-filtering performed on the whole 15-s trial).

Bottom Line: In contrast, the generation of beta oscillation involves the lower part of the EPL and deep granule cells.This differential involvement of sublaminar networks is neither dependent on odor quality nor on the precise frequency of the fast oscillation under study.Overall, this study demonstrates a functional sublaminar organization of the rat OB, which is supported by previous anatomical findings.

View Article: PubMed Central - PubMed

Affiliation: Team Olfaction from Coding to Memory, Center for Research in Neuroscience of Lyon, CNRS UMR5292 - INSERM U1028 Lyon, France ; Team Olfaction from Coding to Memory, Center for Research in Neuroscience of Lyon, Université Claude Bernard Lyon 1 Lyon, France.

ABSTRACT
A prominent feature of olfactory bulb (OB) dynamics is the expression of characteristic local field potential (LFP) rhythms, including a slow respiration-related rhythm and two fast alternating oscillatory rhythms, beta (15-30 Hz) and gamma (40-90 Hz). All of these rhythms are implicated in olfactory coding. Fast oscillatory rhythms are known to involve the mitral-granule cell loop. Although the underlying mechanisms of gamma oscillation have been studied, the origin of beta oscillation remains poorly understood. Whether these two different rhythms share the same underlying mechanism is unknown. This study uses a quantitative and detailed current-source density (CSD) analysis combined with multi-unit activity (MUA) recordings to shed light on this question in freely breathing anesthetized rats. In particular, we show that gamma oscillation generation involves mainly the upper half of the external plexiform layer (EPL) and superficial areas of granule cell layer (GRL). In contrast, the generation of beta oscillation involves the lower part of the EPL and deep granule cells. This differential involvement of sublaminar networks is neither dependent on odor quality nor on the precise frequency of the fast oscillation under study. Overall, this study demonstrates a functional sublaminar organization of the rat OB, which is supported by previous anatomical findings.

Show MeSH