Upstream γ-synchronization enhances odor processing in downstream neurons

Dalal, Tal; Haddad, Rafi

doi:10.1016/j.celrep.2022.110693

Cited by 7 publications

(10 citation statements)

References 57 publications

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“…Nevertheless, the summated IPSP can delay spiking and thus possibly infer synchronization of MCs, as also pointed out earlier (e.g., Schoppa, 2006;McTavish et al, 2012;McIntyre and Cleland, 2016). Such synchronization in the gammabeta range in turn is likely to promote the binding of odor representations across the olfactory bulb and/or to enable transmission of stimulus features other than identity to the piriform cortex (e.g., Kashiwadani et al, 1999;Doucette et al, 2011;Dalal and Haddad, 2022).…”

Section: Functional Implications For Inhibition Originating From Gran...mentioning

confidence: 62%

Anatomical and Functional Connectivity at the Dendrodendritic Reciprocal Mitral Cell–Granule Cell Synapse: Impact on Recurrent and Lateral Inhibition

Aghvami

Kubota²,

Egger³

2022

Front. Neural Circuits

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In the vertebrate olfactory bulb, reciprocal dendrodendritic interactions between its principal neurons, the mitral and tufted cells, and inhibitory interneurons in the external plexiform layer mediate both recurrent and lateral inhibition, with the most numerous of these interneurons being granule cells. Here, we used recently established anatomical parameters and functional data on unitary synaptic transmission to simulate the strength of recurrent inhibition of mitral cells specifically from the reciprocal spines of rat olfactory bulb granule cells in a quantitative manner. Our functional data allowed us to derive a unitary synaptic conductance on the order of 0.2 nS. The simulations predicted that somatic voltage deflections by even proximal individual granule cell inputs are below the detection threshold and that attenuation with distance is roughly linear, with a passive length constant of 650 μm. However, since recurrent inhibition in the wake of a mitral cell action potential will originate from hundreds of reciprocal spines, the summated recurrent IPSP will be much larger, even though there will be substantial mutual shunting across the many inputs. Next, we updated and refined a preexisting model of connectivity within the entire rat olfactory bulb, first between pairs of mitral and granule cells, to estimate the likelihood and impact of recurrent inhibition depending on the distance between cells. Moreover, to characterize the substrate of lateral inhibition, we estimated the connectivity via granule cells between any two mitral cells or all the mitral cells that belong to a functional glomerular ensemble (i.e., which receive their input from the same glomerulus), again as a function of the distance between mitral cells and/or entire glomerular mitral cell ensembles. Our results predict the extent of the three regimes of anatomical connectivity between glomerular ensembles: high connectivity within a glomerular ensemble and across the first four rings of adjacent glomeruli, substantial connectivity to up to eleven glomeruli away, and negligible connectivity beyond. Finally, in a first attempt to estimate the functional strength of granule-cell mediated lateral inhibition, we combined this anatomical estimate with our above simulation results on attenuation with distance, resulting in slightly narrowed regimes of a functional impact compared to the anatomical connectivity.

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Section: Functional Implications For Inhibition Originating From Gran...mentioning

confidence: 62%

Anatomical and Functional Connectivity at the Dendrodendritic Reciprocal Mitral Cell–Granule Cell Synapse: Impact on Recurrent and Lateral Inhibition

Aghvami

Kubota²,

Egger³

2022

Front. Neural Circuits

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“…One mechanism by which spatially distributed neurons form an ensemble is by synchronizing their spiking activity in response to a sensory event (Buzsáki, 2010). This synchronization is thought to enhance the transmission of information to downstream targets (Dalal and Haddad, 2022; Macleod et al, 1998; Pritchett et al, 2015; Sohal, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…These MTCs interact with each other via a dense network of inhibitory neurons stratified throughout all six OB layers. Several studies have shown that odorants evoke strong spike gamma-entrainment in MTCs (Beshel et al, 2007; Dalal and Haddad, 2022; Fukunaga et al, 2014; Lepousez and Lledo, 2013), as well as synchronous firing of MTCs (Kashiwadani et al, 1999). This synchronization is mediated by granule cells (Schoppa, 2006)(GCs) and has recently been shown to enhance odor-information transmission to the Piriform cortex (Dalal and Haddad, 2022).…”

Section: Introductionmentioning

confidence: 99%

Activity-dependent lateral inhibition enables the synchronization of olfactory bulb projection neurons

Dalal,

Haddad

2024

Preprint

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Information in the brain is represented by the activity of neuronal ensembles. These ensembles are adaptive and dynamic, formed and truncated based on the animal’s experience. One mechanism by which spatially distributed neurons form an ensemble is synchronizing their spiking activity in response to a sensory event. In the olfactory bulb, odor stimulation evokes rhythmic gamma activity in spatially distributed mitral and tufted cells (MTCs). This rhythmic activity is thought to enhance the relay of odor information to the downstream olfactory targets. However, how only the odor-activated MTCs are synchronized is unknown. Here, we demonstrate that light activating one set of MTCs can gamma-entrain the spiking activity of another set. This lateral synchronization was particularly effective when both MTCs fired at the gamma rhythm, facilitating the synchronization of only the odor-activated MTCs. Furthermore, we show that lateral synchronization did not depend on the distance between the MTCs and is mediated by Granule cells. In contrast, lateral inhibition between MTCs that reduced their firing rates was spatially restricted to adjacent MTCs and was not mediated by Granule cells. Our findings reveal a simple yet robust mechanism by which spatially distributed neurons entrain each other’s spiking activity to form an ensemble.HighlightsMTC activation entrains the spike timing of other MTCs in an activity-dependent and spatially-independent manner.MTC to MTC suppression is activity- and distance-dependentSpatially distributed Granule cells control MTC’s spike timing, yet do not substantially affect their firing rate.

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“…Together, these oscillatory patterns reflect processes that may gate, bind, and multiplex information, as it is transmitted from the olfactory bulb to downstream regions. More specifically, activity of neurons with respect to each other, or with respect to the breathing cycle, can be informative about the stimulus (Uchida et al, 2014, Haddad et al, 2013, Gill et al, 2020, Chong and Rinberg, 2018, Wilson et al, 2017, Smear et al, 2013, Smear et al, 2011, Shusterman et al, 2011, Cleland, 2014, Dalal and Haddad, 2022). The ubiquity of such patterns in MOS oscillations strongly suggests that they play important functional roles in chemosensory information processing.…”

Section: Introductionmentioning

confidence: 99%

“…In contrast, VNS stimulus uptake is largely uncoupled from breathing, and instead relies on active suction by the vomeronasal organ (Meredith and O’Connell, 1979, Wysocki et al, 1980, Ben Shaul et al, 2010). Other differences between the two systems include the intrinsic properties of olfactory bulb neurons (Shpak et al, 2012, Zibman et al, 2011, Gao et al, 2017), their interactions with each other (Larriva-Sahd, 2008, Dulac and Wagner, 2006, Takami and Graziadei, 1991), and the properties of downstream regions that receive the information (Davison and Ehlers, 2011, Uchida et al, 2014, Haddad et al, 2013, Dalal and Haddad, 2022). Taken together, these observations imply that if, like the MOS, VNS information processing involves concerted patterns of population activity, they are likely to differ in their phenomenological expression and underlying mechanisms.…”

Section: Introductionmentioning

confidence: 99%

Stimulus-induced theta band LFP oscillations format neuronal representations of social chemosignals in the mouse accessory olfactory bulb

Cohen

Kahan

Steinberg

et al. 2023

Preprint

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The vomeronasal system (VNS) is dedicated to processing ethologically relevant chemosensory cues from other organisms. Its first central processing stage is the accessory olfactory bulb (AOB), which sends information to downstream brain regions via spiking activity of its principal neurons, AOB mitral cells (AOB-MCs). Recent studies provided important insights about the functional properties of AOB-MCs and the stimulus aspects that they encode. However, very little is known about the principles that govern their coordinated activity and the manner by which AOB outputs are relayed to downstream regions. In many brain regions, network oscillations play a key role in orchestrating the activity of output neurons, and thereby facilitate and enhance transmission of information. A widely used readout of network processes and oscillations is the local field potential (LFP), which has been extensively studied in the main olfactory system (MOS) and, specifically, in the main olfactory bulb (MOB). To reveal population-level processes in the AOB, we analyzed LFP signals while presenting natural stimuli to anesthetized adult male and female mice. Our recordings reveal prominent LFP theta band oscillatory episodes with a characteristic spatial pattern across the AOB. Using a template matching approach, we find that network dynamics show varying degrees of similarity to this pattern throughout an experiment. Notably, both the similarity to this pattern, and the intensity of the pattern, are modulated by stimulus features. Analysis of LFP signal polarity and its spatial relationship to single unit activity, indicate that oscillatory episodes are generated locally within the AOB, likely representing a reciprocal interaction between AOB-MCs and granule cells (GCs). Co-examination of single unit and LFP activity suggests that oscillations appear when sensory activation surpasses a certain threshold. Importantly, spike times of many AOB-MCs are constrained to the negative LFP oscillation phase, in a manner that can drastically effect integration by downstream processing stages. Based on these observations, we propose that these LFP oscillations can gate, bind, and potentially also multiplex outgoing signals from individual AOB neurons to downstream processing stages.

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Upstream γ-synchronization enhances odor processing in downstream neurons

Cited by 7 publications

References 57 publications

Anatomical and Functional Connectivity at the Dendrodendritic Reciprocal Mitral Cell–Granule Cell Synapse: Impact on Recurrent and Lateral Inhibition

Anatomical and Functional Connectivity at the Dendrodendritic Reciprocal Mitral Cell–Granule Cell Synapse: Impact on Recurrent and Lateral Inhibition

Activity-dependent lateral inhibition enables the synchronization of olfactory bulb projection neurons

Stimulus-induced theta band LFP oscillations format neuronal representations of social chemosignals in the mouse accessory olfactory bulb

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