Sparse Odor Coding in Awake Behaving Mice

Rinberg, Dmitry; Koulakov, Alex; Gelperin, Alan

doi:10.1523/jneurosci.0884-06.2006

Cited by 252 publications

(289 citation statements)

References 58 publications

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“…6). The change in the synchronized oscillatory activity of mitral cells may play a key role in the statedependent gating in the olfactory cortex (Murakami et al, 2005), and in the different mitral cell responses to odorants in anesthetized mice and awake mice (Rinberg et al, 2006).…”

Section: Discussionmentioning

confidence: 99%

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Tsuno¹,

Kashiwadani²,

Mori³

2008

J. Neurosci.

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Behavioral states regulate how information is processed in local neuronal circuits. Here, we asked whether dendrodendritic synaptic interactions in the olfactory bulb vary with brain and behavioral states. To examine the state-dependent change of the dendrodendritic synaptic transmission, we monitored changes in field potential responses in the olfactory bulb of urethane-anesthetized and freely behaving rats. In urethane-anesthetized rats, granule-to-mitral dendrodendritic synaptic inhibition was larger and longer when slow waves were present in the electroencephalogram (slow-wave state) than during the fast-wave state. The state-dependent alternating change in the granule-to-mitral inhibition was regulated by the cholinergic system. In addition, the frequency of the spontaneous oscillatory activity of local field potentials and periodic discharges of mitral cells in the olfactory bulb shifted in synchrony with shifts in the neocortical brain state. Freely behaving rats showed multilevel changes in dendrodendritic synaptic inhibition that corresponded to diverse behavioral states; the inhibition was the largest during slow-wave sleep state, and successively smaller during light sleep, awake immobility, and awake moving states. These results provide evidence that behavioral state-dependent global changes in cholinergic tone modulate dendrodendritic synaptic inhibition and the information processing mode in the olfactory bulb.

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Section: Discussionmentioning

confidence: 99%

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Tsuno¹,

Kashiwadani²,

Mori³

2008

J. Neurosci.

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“…Urethane results in different olfactory response intensities when animals undergo spontaneous shift between fast-wave and slow-wave states (Murakami et al, 2005;Wilson, 2010). Ketamine leads to higher response intensities and lower selectivity in the olfactory bulb and induces slow oscillations in the olfactory cortex (Fontanini et al, 2003;Rinberg et al, 2006). In addition to the potential artifacts caused by anesthesia, it had also been difficult to identify cell types in vivo.…”

Section: Odor Representation By Functionally Heterogeneous Populationmentioning

confidence: 99%

“…The interpretation of previous observations is limited by two key technical concerns. First, recordings and imaging are typically performed in anesthetized animals, and anesthetics can exert side effects on neuronal dynamics and olfactory responses in both the MOB and the PCX (Friedberg et al, 1999;Murakami et al, 2005;Rinberg et al, 2006;Wilson, 2010). Second, neurons of diverse morphological features are present in the PCX, and different types of neurons can exhibit highly distinct olfactory tunings (Poo and Isaacson, 2009).…”

Section: Introductionmentioning

confidence: 99%

Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice

Zhan¹,

Luo²

2010

J. Neurosci.

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The mammalian piriform cortex receives direct synaptic input from the olfactory bulb and is likely the locus for the formation of odor percept. It remains unclear how individual cortical neurons encode olfactory information in unanesthetized animals. By single-cell recordings from head-restrained awake mice, we studied the odor response profiles of individual neurons in the anterior piriform cortex (aPCX). Neurons were juxtacellularly labeled, and their cell types were determined by their morphology and neurotransmitter phenotypes. We found a considerable level of variability in selectivity patterns among pyramidal neurons (PNs). Approximately one-quarter of PNs were broadly activated by structurally dissimilar odorants, whereas the excitations to the rest of PNs were highly selective. Broad inhibition was only observed from a subpopulation of PNs. GABAergic neurons displayed nonselective excitatory responses to test odorants and rarely exhibited inhibition. In contrast, non-GABAergic nonpyramidal neurons in the deep layer tended to be strongly inhibited by multiple different odorants. Our findings suggest that odor representation is accomplished by both broadly tuned and narrow-tuned PNs in the aPCX of awake animals. In addition, various types of interneurons may play different roles in the intracortical processing of olfactory information.

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“…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).In this study, we examined the OB activities at rest and after stimulation in different brain states. We found that in two resting states with rather different baseline activities, the levels of peak activities of the same stimulation had no significant difference.…”

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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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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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Sparse Odor Coding in Awake Behaving Mice

Cited by 252 publications

References 58 publications

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Behavioral State Regulation of Dendrodendritic Synaptic Inhibition in the Olfactory Bulb

Diverse Patterns of Odor Representation by Neurons in the Anterior Piriform Cortex of Awake Mice

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

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