Profound Context-Dependent Plasticity of Mitral Cell Responses in Olfactory Bulb

Doucette, Wilder; Restrepo, Diego

doi:10.1371/journal.pbio.0060258

Cited by 138 publications

(152 citation statements)

References 77 publications

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“…It has been reported that in the aspects of LFP signals and spiking rates, task-related learning processes can modify the neural representation (40,41). However, the objective modulation does not contradict the results in this study, because the task-related modified representations are also stable after the animals learned the task (40).…”

Section: Discussioncontrasting

confidence: 75%

“…However, the objective modulation does not contradict the results in this study, because the task-related modified representations are also stable after the animals learned the task (40). Therefore, the modification just redefines the stimulus to generate a new representation and perception accordingly, conferring the system with higher efficiency for complex olfactory functions.…”

Section: Discussionmentioning

confidence: 46%

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Brain-state–independent neural representation of peripheral stimulation in rat olfactory bulb

Gong

2011

Proc. Natl. Acad. Sci. U.S.A.

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It is critical for normal brains to perceive the external world precisely and accurately under ever-changing operational conditions, yet the mechanisms underlying this fundamental brain function in the sensory systems are poorly understood. To address this issue in the olfactory system, we investigated the responses of olfactory bulbs to odor stimulations under different brain states manipulated by anesthesia levels. Our results revealed that in two brain states, where the spontaneous baseline activities differed about twofold based on the local field potential (LFP) signals, the levels of neural activities reached after the same odor stimulation had no significant difference. This phenomenon was independent of anesthetics (pentobarbital or chloral hydrate), stimulating odorants (ethyl propionate, ethyl butyrate, ethyl valerate, amyl acetate, n-heptanal, or 2-heptanone), odor concentrations, and recording sites (the mitral or granular cell layers) for LFPs in three frequency bands and for multiunit activities. Furthermore, the activity patterns of the same stimulation under these two brain states were highly similar at both LFP and multiunit levels. These converging results argue the existence of mechanisms in the olfactory bulbs that ensure the delivery of peripheral olfactory information to higher olfactory centers with high fidelity under different brain states.T he ability to perceive the ever-changing external world accurately and precisely is a basic brain function. It is critical for daily life, survival, and higher brain functions, such as making decisions, plans, and judgments. However, the brain itself operates in ever-changing states (1, 2) or baselines (3) that are constantly modulated by external and internal factors, such as physical, physiological, psychological, clinical, and metabolic conditions. Therefore, elucidation of how sensory systems represent the same sensory information to the brain under different operational states is fundamental to understanding the related brain functions (1, 4-6).The olfactory system, as the most direct and intrinsic sensory module (1,7,8), provides a unique model to study the principles and functional mechanisms of the brain. The peripheral olfactory information takes just one synapse to enter the olfactory bulb (OB) in the brain. The OB outputs directly to the olfactory cortices that mostly belong to the limbic system. As a center to code and process the peripheral olfactory inputs and a hub to distribute the processed information to the olfactory cortices (9-11), the OB consists of laminar structures, from the outer surface to the inner core: the olfactory nerve, glomerular, external plexiform, mitral cell layer (MCL), and granular cell (GCL) layer. All peripheral olfactory input is received by a few thousand glomeruli, which generate an odor-specific spatiotemporal activity pattern across the glomerular layer (10, 12, 13). The information is mainly processed in the external plexiform layer that contains a dense dendrodendritic network formed between the secon...

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Section: Discussioncontrasting

confidence: 75%

Section: Discussionmentioning

confidence: 46%

Brain-state–independent neural representation of peripheral stimulation in rat olfactory bulb

Gong

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…Olfactory learning also induces changes in encoding of the learned odor in the olfactory bulb (OB) (Freeman and Schneider 1982;Wilson and Sullivan 1994;Mandairon et al 2006;Doucette and Restrepo 2008) and the orbitofrontal cortex (OFC; Schoenbaum et al 1998Schoenbaum et al , 1999Schoenbaum et al , 2003. In particular, we have reported (Cohen et al 2008) an enhancement of reciprocal connectivity between the PC and its ascending input from the OB and descending input from the OFC 3 days after learning.…”

Section: Introductionmentioning

confidence: 92%

Differential Modifications of Synaptic Weights During Odor Rule Learning: Dynamics of Interaction Between the Piriform Cortex with Lower and Higher Brain Areas

Cohen¹,

Wilson²,

Barkai³

2013

Cerebral Cortex

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Learning of a complex olfactory discrimination (OD) task results in acquisition of rule learning after prolonged training. Previously, we demonstrated enhanced synaptic connectivity between the piriform cortex (PC) and its ascending and descending inputs from the olfactory bulb (OB) and orbitofrontal cortex (OFC) following OD rule learning. Here, using recordings of evoked field postsynaptic potentials in behaving animals, we examined the dynamics by which these synaptic pathways are modified during rule acquisition. We show profound differences in synaptic connectivity modulation between the 2 input sources. During rule acquisition, the ascending synaptic connectivity from the OB to the anterior and posterior PC is simultaneously enhanced. Furthermore, post-training stimulation of the OB enhanced learning rate dramatically. In sharp contrast, the synaptic input in the descending pathway from the OFC was significantly reduced until training completion. Once rule learning was established, the strength of synaptic connectivity in the 2 pathways resumed its pretraining values. We suggest that acquisition of olfactory rule learning requires a transient enhancement of ascending inputs to the PC, synchronized with a parallel decrease in the descending inputs. This combined short-lived modulation enables the PC network to reorganize in a manner that enables it to first acquire and then maintain the rule.

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“…Indeed, when animals perform correctly a discrimination task, gamma oscillations are enhanced (Beshel et al, 2007), whereas mitral cell responses are hardly detectable by measuring single-cell firing rate (Kay and Laurent, 1999;Doucette and Restrepo, 2008). Although the dendrodendritic synapse is essential for gamma oscillation generation, the physiological mechanisms underlying these oscillations are not well understood.…”

Section: Delayed and Long-lasting Effects On Gamma Oscillations And Dmentioning

confidence: 99%

Somatostatin Contributes toIn VivoGamma Oscillation Modulation and Odor Discrimination in the Olfactory Bulb

Lepousez

Mouret²,

Loudes³

et al. 2010

J. Neurosci.

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Neuropeptides are systematically encountered in local interneurons, but their functional contribution in neural networks is poorly documented. In the mouse main olfactory bulb (MOB), somatostatin is mainly concentrated in local GABAergic interneurons restricted to the external plexiform layer (EPL). Immunohistochemical experiments revealed that the sst2 receptor, the major somatostatin receptor subtype in the telencephalon, is expressed by mitral cells, the MOB principal cells. As odor-activated mitral cells synchronize and generate gamma oscillations of the local field potentials, we investigated whether pharmacological manipulations of sst2 receptors could influence these oscillations in freely behaving mice. In wild-type, but not in sst2 knock-out mice, gamma oscillation power decreased lastingly after intrabulbar injection of an sst2-selective antagonist (BIM-23627), while sst2-selective agonists (octreotide and L-779976) durably increased it. Sst2-mediated oscillation changes were correlated with modifications of the dendrodendritic synaptic transmission between mitral and granule cells. Finally, bilateral injections of BIM-23627 and octreotide respectively decreased and increased odor discrimination performances. Together, these results suggest that endogenous somatostatin, presumably released from EPL interneurons, affects gamma oscillations through the dendrodendritic reciprocal synapse and contributes to olfactory processing. This provides the first direct correlation between synaptic, oscillatory, and perceptual effects induced by an intrinsic neuromodulator.

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Profound Context-Dependent Plasticity of Mitral Cell Responses in Olfactory Bulb

Cited by 138 publications

References 77 publications

Brain-state–independent neural representation of peripheral stimulation in rat olfactory bulb

Brain-state–independent neural representation of peripheral stimulation in rat olfactory bulb

Differential Modifications of Synaptic Weights During Odor Rule Learning: Dynamics of Interaction Between the Piriform Cortex with Lower and Higher Brain Areas

Somatostatin Contributes toIn VivoGamma Oscillation Modulation and Odor Discrimination in the Olfactory Bulb

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