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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.

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Sublaminar network organization of the OB as revealed by functional and anatomical studies. Combination of the different sublaminar networks involved in beta and gamma oscillations revealed by the present CSD study (color plot) and OB anatomical organization adapted from Orona et al. (1984). These data show that gamma oscillations involve mainly tufted and type II mitral cells (in black on the right panel) with more superficial secondary dendrite arborization in the external EPL. In contrast, beta oscillations involve more type I mitral cells (in black on the left panel) with secondary dendrites mainly in the internal EPL. There is a similar segregation in the GRL. Cell name abbreviations: MI: type I mitral cell; MII: type II mitral cell; Gs: superficial granule cell; Gd: deep granule cell; Te: external tufted cell; Tm: middle tufted cell.
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Figure 9: Sublaminar network organization of the OB as revealed by functional and anatomical studies. Combination of the different sublaminar networks involved in beta and gamma oscillations revealed by the present CSD study (color plot) and OB anatomical organization adapted from Orona et al. (1984). These data show that gamma oscillations involve mainly tufted and type II mitral cells (in black on the right panel) with more superficial secondary dendrite arborization in the external EPL. In contrast, beta oscillations involve more type I mitral cells (in black on the left panel) with secondary dendrites mainly in the internal EPL. There is a similar segregation in the GRL. Cell name abbreviations: MI: type I mitral cell; MII: type II mitral cell; Gs: superficial granule cell; Gd: deep granule cell; Te: external tufted cell; Tm: middle tufted cell.

Mentions: The CSD study is only a functional and indirect demonstration of these oscillatory laminar subnetworks. The next question is whether there are anatomical substrates for these networks. Interestingly, many anatomical studies show differences between the lower and upper parts of EPL and GRL. For example, individual cell reconstructions have revealed that mitral cells can be divided into two groups, with a type I or type II group with secondary dendrites that innervate only the lower or intermediate portion of the EPL, respectively (Orona et al., 1984). The same authors demonstrated that granule cell innervation of the EPL was also inhomogeneous, with more superficial cells of the GRL innervating the upper half of EPL, and with deeper cells of the GRL innervating the deeper EPL (Orona et al., 1983). Since then, other studies have shown that anatomic or metabolic markers can display differences between the lower and upper EPL in mice or rats, including cytochrome oxidase (Mouradian and Scott, 1988) and α3-GABA subunits (Panzanelli et al., 2005; Sassoè-Pognetto et al., 2009), or between the lower and upper GRL, including perisomatic targeting granule cells (Naritsuka et al., 2009) and the functional properties and spatial distribution of newborn cells (Carleton et al., 2003; Lemasson et al., 2005). Overall, these anatomical studies provide support for a sublaminar organization of the EPL and GRL, similar to the functional observations in the present CSD study (see Figure 9 for a parallel between the anatomical substrates and the CSD profiles).


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)

Sublaminar network organization of the OB as revealed by functional and anatomical studies. Combination of the different sublaminar networks involved in beta and gamma oscillations revealed by the present CSD study (color plot) and OB anatomical organization adapted from Orona et al. (1984). These data show that gamma oscillations involve mainly tufted and type II mitral cells (in black on the right panel) with more superficial secondary dendrite arborization in the external EPL. In contrast, beta oscillations involve more type I mitral cells (in black on the left panel) with secondary dendrites mainly in the internal EPL. There is a similar segregation in the GRL. Cell name abbreviations: MI: type I mitral cell; MII: type II mitral cell; Gs: superficial granule cell; Gd: deep granule cell; Te: external tufted cell; Tm: middle tufted cell.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4115636&req=5

Figure 9: Sublaminar network organization of the OB as revealed by functional and anatomical studies. Combination of the different sublaminar networks involved in beta and gamma oscillations revealed by the present CSD study (color plot) and OB anatomical organization adapted from Orona et al. (1984). These data show that gamma oscillations involve mainly tufted and type II mitral cells (in black on the right panel) with more superficial secondary dendrite arborization in the external EPL. In contrast, beta oscillations involve more type I mitral cells (in black on the left panel) with secondary dendrites mainly in the internal EPL. There is a similar segregation in the GRL. Cell name abbreviations: MI: type I mitral cell; MII: type II mitral cell; Gs: superficial granule cell; Gd: deep granule cell; Te: external tufted cell; Tm: middle tufted cell.
Mentions: The CSD study is only a functional and indirect demonstration of these oscillatory laminar subnetworks. The next question is whether there are anatomical substrates for these networks. Interestingly, many anatomical studies show differences between the lower and upper parts of EPL and GRL. For example, individual cell reconstructions have revealed that mitral cells can be divided into two groups, with a type I or type II group with secondary dendrites that innervate only the lower or intermediate portion of the EPL, respectively (Orona et al., 1984). The same authors demonstrated that granule cell innervation of the EPL was also inhomogeneous, with more superficial cells of the GRL innervating the upper half of EPL, and with deeper cells of the GRL innervating the deeper EPL (Orona et al., 1983). Since then, other studies have shown that anatomic or metabolic markers can display differences between the lower and upper EPL in mice or rats, including cytochrome oxidase (Mouradian and Scott, 1988) and α3-GABA subunits (Panzanelli et al., 2005; Sassoè-Pognetto et al., 2009), or between the lower and upper GRL, including perisomatic targeting granule cells (Naritsuka et al., 2009) and the functional properties and spatial distribution of newborn cells (Carleton et al., 2003; Lemasson et al., 2005). Overall, these anatomical studies provide support for a sublaminar organization of the EPL and GRL, similar to the functional observations in the present CSD study (see Figure 9 for a parallel between the anatomical substrates and the CSD profiles).

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
Related in: MedlinePlus