Serotonergic modulation of odor input to the mammalian olfactory bulb

Petzold, Gabor C.; Hagiwara, Akari; Murthy, Venkatesh N.

doi:10.1038/nn.2335

Cited by 205 publications

(206 citation statements)

References 46 publications

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“…Although the effect of anesthesia on the peripheral inputs is negligible (42), it is more significant for the central processes (1,19). The OB receives modulatory inputs from several nuclei (16)(17)(18)43) and heavy feedback inputs from many cortices (11,43,44). Because multiple receptor types of these pathways spread over the OB, the effect of anesthesia on modulatory inputs is difficult to predict.…”

Section: Discussionmentioning

confidence: 99%

“…The information is mainly processed in the external plexiform layer that contains a dense dendrodendritic network formed between the secondary dendrites of the mitral/tufted (M/T) cells, whose somas are located in the MCL, and the dendrites of granular cells, whose somas are located in the GCL, then sent to higher olfactory centers by M/T cells (11,14,15). Under given conditions, the representation and process of the olfactory information in the OB and the regulation of OB activity by the other brain regions have been extensively studied, and have greatly advanced our understanding of the olfactory system (6,(16)(17)(18). However, how the OB processes, represents, and transmits information of the same olfactory stimulus in different brain states has not been systematically investigated (19)(20)(21).…”

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confidence: 99%

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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: Discussionmentioning

confidence: 99%

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confidence: 99%

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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“…Ultimately, these results imply that stronger and/or more synchronous inputs from cortex and thalamus are necessary to initiate action potentials in MSNs during periods of histaminergic activity. Such negative modulation of excitatory inputs is reminiscent of gain control used by sensory systems (Petzold et al, 2009) to keep the postsynaptic response within a normal dynamic range and preventing input saturation.…”

Section: Histaminergic Modulation Of Excitatory Inputsmentioning

confidence: 99%

Differential Modulation of Excitatory and Inhibitory Striatal Synaptic Transmission by Histamine

Ellender¹,

Huerta-Ocampo²,

Deisseroth³

et al. 2011

J. Neurosci.

112

134

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Information processing in the striatum is critical for basal ganglia function and strongly influenced by neuromodulators (e.g., dopamine). The striatum also receives modulatory afferents from the histaminergic neurons in the hypothalamus which exhibit a distinct diurnal rhythm with high activity during wakefulness, and little or no activity during sleep. In view of the fact that the striatum also expresses a high density of histamine receptors, we hypothesized that released histamine will affect striatal function. We studied the role of histamine on striatal microcircuit function by performing whole-cell patch-clamp recordings of neurochemically identified striatal neurons combined with electrical and optogenetic stimulation of striatal afferents in mouse brain slices. Bath applied histamine had many effects on striatal microcircuits. Histamine, acting at H 2 receptors, depolarized both the direct and indirect pathway medium spiny projection neurons (MSNs). Excitatory, glutamatergic input to both classes of MSNs from both the cortex and thalamus was negatively modulated by histamine acting at presynaptic H 3 receptors. The dynamics of thalamostriatal, but not corticostriatal, synapses were modulated by histamine leading to a facilitation of thalamic input. Furthermore, local inhibitory input to both classes of MSNs was negatively modulated by histamine. Subsequent dual whole-cell patch-clamp recordings of connected pairs of striatal neurons revealed that only lateral inhibition between MSNs is negatively modulated, whereas feedforward inhibition from fast-spiking GABAergic interneurons onto MSNs is unaffected by histamine. These findings suggest that the diurnal rhythm of histamine release entrains striatal function which, during wakefulness, is dominated by feedforward inhibition and a suppression of excitatory drive.

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“…Injection of a specific serotonergic neurotoxin in adult rats results in reduced olfactory discrimination, and depletion of 5-HT fibres in rat pups causes a failure in the development of odour preference (Moriizumi et al, 1994;McLean et al, 1993). Petzold et al (2009) suggested that the serotonergic system regulates odour input in the OB. Glomerular activation after odour stimulation is attenuated by 5-HT 2C receptor activation and amplified by 5-HT 2C receptor inhibition (Petzold et al, 2009), indicating a prominent role of serotonin in the initial steps of olfactory processing.…”

Section: Monoamines: Noradrenaline Serotoninmentioning

confidence: 99%

“…Petzold et al (2009) suggested that the serotonergic system regulates odour input in the OB. Glomerular activation after odour stimulation is attenuated by 5-HT 2C receptor activation and amplified by 5-HT 2C receptor inhibition (Petzold et al, 2009), indicating a prominent role of serotonin in the initial steps of olfactory processing. Whether serotonin-mediated effects involve also regulation of newborn olfactory interneurons seems to be unlikely.…”

Section: Monoamines: Noradrenaline Serotoninmentioning

confidence: 99%

From progenitors to integrated neurons: Role of neurotransmitters in adult olfactory neurogenesis

Bovetti

Gribaudo

Puché

et al. 2011

Journal of Chemical Neuroanatomy

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Adult neurogenesis is due to the persistence of pools of constitutive stem cells able to give rise to a progeny of proliferating progenitors. In rodents, adult neurogenic niches have been found in the subventricular zone (SVZ) along the lateral ventricles and in the subgranular zone of the dentate gyrus in the hippocampus. SVZ progenitors undergo a unique process of tangential migration from the lateral ventricle to the olfactory bulb (OB) where they differentiate mainly into GABAergic interneurons in the granule and glomerular layers. SVZ progenitor proliferation, migration and differentiation into fully integrated neurons, are strictly related processes regulated by complex interactions between cell intrinsic and extrinsic influences. Numerous observations demonstrate that neurotrasmitters are involved in all steps of the adult neurogenic process, but the understanding of their role is hampered by their intricate mechanism of action and by the highly complex network in which neurotransmitters work. By considering the three main steps of olfactory adult neurogenesis (proliferation, migration and integration), this review will discuss recent advances in the study of neurotransmitters, highlighting the regulatory mechanisms upstream and downstream their action.

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Serotonergic modulation of odor input to the mammalian olfactory bulb

Cited by 205 publications

References 46 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 Modulation of Excitatory and Inhibitory Striatal Synaptic Transmission by Histamine

From progenitors to integrated neurons: Role of neurotransmitters in adult olfactory neurogenesis

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