scholarly journals Cell and circuit origins of fast network oscillations in the mammalian main olfactory bulb

2021 ◽  
Author(s):  
Shawn D Burton ◽  
Nathan N Urban

Neural synchrony generates fast network oscillations throughout the brain, including the main olfactory bulb (MOB), the first processing station of the olfactory system. Identifying the mechanisms synchronizing neurons in the MOB will be key to understanding how network oscillations support the coding of a high-dimensional sensory space. Here, using paired recordings and optogenetic activation of glomerular sensory inputs in MOB slices, we uncovered profound differences in principal mitral cell (MC) vs. tufted cell (TC) spike-time synchrony: TCs robustly synchronized across fast- and slow-gamma frequencies, while MC synchrony was weaker and concentrated in slow-gamma frequencies. Synchrony among both cell types was enhanced by shared glomerular input but was independent of intraglomerular lateral excitation. Cell-type differences in synchrony could also not be traced to any difference in the synchronization of synaptic inhibition. Instead, greater TC than MC synchrony paralleled the more periodic firing among resonant TCs than MCs and emerged in patterns consistent with densely synchronous network oscillations. Collectively, our results thus reveal a mechanism for parallel processing of sensory information in the MOB via differential TC vs. MC synchrony, and further contrast mechanisms driving fast network oscillations in the MOB from those driving the sparse synchronization of irregularly-firing principal cells throughout cortex.

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Shawn D Burton ◽  
Nathan N Urban

Neural synchrony generates fast network oscillations throughout the brain, including the main olfactory bulb (MOB), the first processing station of the olfactory system. Identifying the mechanisms synchronizing neurons in the MOB will be key to understanding how network oscillations support the coding of a high-dimensional sensory space. Here, using paired recordings and optogenetic activation of glomerular sensory inputs in MOB slices, we uncovered profound differences in principal mitral cell (MC) vs. tufted cell (TC) spike-time synchrony: TCs robustly synchronized across fast- and slow-gamma frequencies, while MC synchrony was weaker and concentrated in slow-gamma frequencies. Synchrony among both cell types was enhanced by shared glomerular input but was independent of intraglomerular lateral excitation. Cell-type differences in synchrony could also not be traced to any difference in the synchronization of synaptic inhibition. Instead, greater TC than MC synchrony paralleled the more periodic firing among resonant TCs than MCs and emerged in patterns consistent with densely synchronous network oscillations. Collectively, our results thus reveal a mechanism for parallel processing of sensory information in the MOB via differential TC vs. MC synchrony, and further contrast mechanisms driving fast network oscillations in the MOB from those driving the sparse synchronization of irregularly-firing principal cells throughout cortex.


2007 ◽  
Vol 85 (11) ◽  
pp. 2407-2421 ◽  
Author(s):  
Javier S. Recio ◽  
Eduardo Weruaga ◽  
Carmela Gómez ◽  
Jorge Valero ◽  
Jesús G. Briñón ◽  
...  

2008 ◽  
Vol 27 (7) ◽  
pp. 1686-1699 ◽  
Author(s):  
Mihaly Kollo ◽  
Noémi Holderith ◽  
Miklós Antal ◽  
Zoltan Nusser

2021 ◽  
Vol 17 (9) ◽  
pp. e1009169
Author(s):  
Michelle F. Craft ◽  
Andrea K. Barreiro ◽  
Shree Hari Gautam ◽  
Woodrow L. Shew ◽  
Cheng Ly

The majority of olfaction studies focus on orthonasal stimulation where odors enter via the front nasal cavity, while retronasal olfaction, where odors enter the rear of the nasal cavity during feeding, is understudied. The coding of retronasal odors via coordinated spiking of neurons in the olfactory bulb (OB) is largely unknown despite evidence that higher level processing is different than orthonasal. To this end, we use multi-electrode array in vivo recordings of rat OB mitral cells (MC) in response to a food odor with both modes of stimulation, and find significant differences in evoked firing rates and spike count covariances (i.e., noise correlations). Differences in spiking activity often have implications for sensory coding, thus we develop a single-compartment biophysical OB model that is able to reproduce key properties of important OB cell types. Prior experiments in olfactory receptor neurons (ORN) showed retro stimulation yields slower and spatially smaller ORN inputs than with ortho, yet whether this is consequential for OB activity remains unknown. Indeed with these specifications for ORN inputs, our OB model captures the salient trends in our OB data. We also analyze how first and second order ORN input statistics dynamically transfer to MC spiking statistics with a phenomenological linear-nonlinear filter model, and find that retro inputs result in larger linear filters than ortho inputs. Finally, our models show that the temporal profile of ORN is crucial for capturing our data and is thus a distinguishing feature between ortho and retro stimulation, even at the OB. Using data-driven modeling, we detail how ORN inputs result in differences in OB dynamics and MC spiking statistics. These differences may ultimately shape how ortho and retro odors are coded.


2019 ◽  
Author(s):  
Satoshi Fujimoto ◽  
Marcus N. Leiwe ◽  
Richi Sakaguchi ◽  
Yuko Muroyama ◽  
Reiko Kobayakawa ◽  
...  

ABSTRACTIn the mouse olfactory bulb, sensory information detected by ∼1,000 types of olfactory sensory neurons (OSNs) is represented by the glomerular map. The second-order neurons, mitral and tufted cells, connect a single primary dendrite to one glomerulus. This forms discrete connectivity between the ∼1,000 types of input and output neurons. It has remained unknown how this discrete dendrite wiring is established during development. We found that genetically silencing neuronal activity in mitral cells, but not from OSNs, perturbs the dendrite pruning of mitral cells. In vivo calcium imaging of awake neonatal animals revealed two types of spontaneous neuronal activity in mitral/tufted cells, but not in OSNs. Pharmacological and knockout experiments revealed a role for glutamate and NMDARs. The genetic blockade of neurotransmission among mitral/tufted cells reduced spontaneous activity and perturbed dendrite wiring. Thus, spontaneous network activity generated within the olfactory bulb self-organizes the parallel discrete connections in the mouse olfactory system.


2005 ◽  
Vol 37 (4) ◽  
pp. 276-282 ◽  
Author(s):  
Zhao-Ping Qin ◽  
Shu-Ming Ye ◽  
Ji-Zeng Du ◽  
Gong-Yu Shen

Abstract The distribution of calbindin, calretinin and parvalbumin during the development of the mouse main olfactory bulb (MOB) was studied using immunohistochemistry techniques. The results are as follows: (1) calbindin-immunoreactive profiles were mainly located in the glomerular layer, and few large calbindin-immunoreactive cells were found in the subependymal layer of postnatal day 10 (P1 0) to postnatal day 40 (P40) mice; (2) no calbindin was detected in the mitral cell layer at any stage; (3) calretinin-immunoreactive profiles were present in all layers of the main olfactory bulb at all stages, especially in the olfactory nerve layer, glomerular layer and granule cell layer; (4) parvalbumin-immunoreactive profiles were mainly located in the external plexiform layer (except for P10 mice); (5) weakly stained parvalbumin-immunoreactive profiles were present in the glomerular layer at all stages; and (6) no parvalbumin was detected in the mitral cell layer at any stage.


2003 ◽  
Vol 89 (5) ◽  
pp. 2601-2610 ◽  
Author(s):  
Daniel Friedman ◽  
Ben W. Strowbridge

Odor perception depends on a constellation of molecular, cellular, and network interactions in olfactory brain areas. Recently, there has been better understanding of the cellular and molecular mechanisms underlying the odor responses of neurons in the olfactory epithelium, the first-order olfactory area. In higher order sensory areas, synchronized activity in networks of neurons is known to be a prominent feature of odor processing. The perception and discrimination of odorants is associated with fast (20–70 Hz) electroencephalographic oscillations. The cellular mechanisms underlying these fast network oscillations have not been defined. In this study, we show that synchronous fast oscillations can be evoked by brief electrical stimulation in the rat olfactory bulb in vitro, partially mimicking the natural response of this brain region to sensory input. Stimulation induces periodic inhibitory synaptic potentials in mitral cells and prolonged spiking in GABAergic granule cells. Repeated stimulation leads to the persistent enhancement in both granule cell activity and mitral cell inhibition. Prominent oscillations in field recordings indicate that stimulation induces high-frequency activity throughout networks of olfactory bulb neurons. Network synchronization results from chemical and electrical synaptic interactions since both glutamate-receptor antagonists and gap junction inhibitors block oscillatory intracellular and field responses. Our results demonstrate that the olfactory bulb can generate fast oscillations autonomously through the persistent activation of networks of inhibitory interneurons. These local circuit interactions may be critically involved in odor processing in vivo.


Author(s):  
John Harvey ◽  
Thomas Heinbockel

A major step in our understanding of brain function is to determine how neural circuits are altered in their function by signaling molecules or neuromodulators. Neuromodulation is the neurochemical process that modifies the computations performed by a neuron or network based on changing the functional needs or behavioral state of the subject. These modulations have the effect of altering the responsivity to synaptic inputs. Early sensory processing areas, such as the main olfactory bulb, provide an accessible window for investigating how neuromodulation regulates the functional states of neural networks and influences how we process sensory information. Olfaction is an attractive model system in this regard because of its relative simplicity and because it links primary olfactory sensory neurons to higher olfactory and associational networks. Likewise, centrifugal fibers from higher order brain centers target neurons in the main olfactory bulb to regulate synaptic processing. The neuromodulatory systems that provide regulatory inputs and play important roles in olfactory sensory processing and behaviors include the endocannabinoid system, the dopaminergic system, the cholinergic system, the noradrenergic system and the serotonergic system. Here, we present a brief survey of neuromodulation of olfactory signals in the main olfactory bulb with an emphasis on the endocannabinoid system.


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