Dynamic Sensory Representations in the Olfactory Bulb: Modulation by Wakefulness and Experience

Kato, Hiroyuki; Chu, Monica W.; Isaacson, Jeffry S.; Komiyama, Takaki

doi:10.1016/j.neuron.2012.09.037

Cited by 237 publications

(356 citation statements)

References 68 publications

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“…Two to four weeks post-injection, we implanted a cranial window over the dorsal OB and investigated the Ca 2+ responses of GCs in anesthetized mice under baseline conditions and following odor stimulation ( Figures 1A and 1B). In line with and extending previous reports [6,23], our in vivo Ca 2+ imaging revealed the presence of functionally distinct subtypes of GCs based on their spontaneous activity. Slightly more than half of the GCs did not show any change in their fluorescence intensity during the 2-min acquisition period (30-Hz sampling rate; blue arrowhead in Figure 1C; top trace in Figure 1D).…”

Section: Functionally Heterogeneous Populations Of Gcs In the Adult Obsupporting

confidence: 91%

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CaMKIIα Expression Defines Two Functionally Distinct Populations of Granule Cells Involved in Different Types of Odor Behavior

Malvaut¹,

Gribaudo

Hardy³

et al. 2017

Current Biology

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International audienceGranule cells (GCs) in the olfactory bulb (OB) play an important role in odor information processing. Although they have been classified into various neurochemical subtypes, the functional roles of these subtypes remain unknown. We used in vivo two-photon Ca2+ imaging combined with cell-type-specific identification of GCs in the mouse OB to examine whether functionally distinct GC subtypes exist in the bulbar network. We showed that half of GCs express Ca2+/calmodulin-dependent protein kinase IIα (CaMKIIα+) and that these neurons are preferentially activated by olfactory stimulation. The higher activity of CaMKIIα+ neurons is due to the weaker inhibitory input that they receive compared to their CaMKIIα-immunonegative (CaMKIIα−) counterparts. In line with these functional data, immunohistochemical analyses showed that 75%–90% of GCs expressing the immediate early gene cFos are CaMKIIα+ in naive animals and in mice that have been exposed to a novel odor and go/no-go operant conditioning, or that have been subjected to long-term associative memory and spontaneous habituation/dishabituation odor discrimination tasks. On the other hand, a perceptual learning task resulted in increased activation of CaMKIIα− cells

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Section: Functionally Heterogeneous Populations Of Gcs In the Adult Obsupporting

confidence: 91%

“…Furthermore, it has previously been shown that GC activity increases with wakefulness [23]. We thus determined the percentage of CaMKIIa + GCs among all activated cells throughout the GCL and whether their activation differed in awake animals.…”

Section: Functionally Heterogeneous Populations Of Gcs In the Adult Obmentioning

confidence: 99%

CaMKIIα Expression Defines Two Functionally Distinct Populations of Granule Cells Involved in Different Types of Odor Behavior

Malvaut¹,

Gribaudo

Hardy³

et al. 2017

Current Biology

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“…First, we observed that the olfactory afterimage is state-dependent for it is both stronger and longer in awake mice than anesthetized mice. Whether this difference is due to top-down processes like attention or anesthesia-induced changes in the network (28,32) is impossible to disambiguate. We also observed that the olfactory afterimage is stronger in anesthetized mice for familiar odors over naïve odors although this effect was weak.…”

Section: Discussionmentioning

confidence: 99%

“…All experiments performed so far were at a high odor concentration (5%), which evokes relatively dense activity patterns in glomeruli (28,32). To check whether olfactory afterimages are present at lower concentrations, and to see whether the afterimages contain concentration-specific information, we repeated our experiments using three lower odor concentrations (0.1%, 0.4%, and 2%).…”

Section: S2dmentioning

confidence: 99%

Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

Patterson

Lagier

Carleton

2013

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

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Rodents can discriminate odors in one breath, and mammalian olfaction research has thus focused on the first breath. However, sensory representations dynamically change during and after stimuli. To investigate these dynamics, we recorded spike trains from the olfactory bulb of awake, head-fixed mice and found that some mitral cells' odor representations changed following the first breath and others continued after odor cessation. Population analysis revealed that these postodor responses contained odor-and concentration-specific information-an odor afterimage. Using calcium imaging, we found that most olfactory glomerular activity was restricted to the odor presentation, implying that the afterimage is not primarily peripheral. The odor afterimage was not dependent on odorant physicochemical properties. To artificially induce aftereffects, we photostimulated mitral cells using channelrhodopsin and recorded centrally maintained persistent activity. The strength and persistence of the afterimage was dependent on the duration of both artificial and natural stimulation. In summary, we show that the odor representation evolves after the first breath and that there is a centrally maintained odor afterimage, similar to other sensory systems. These dynamics may help identify novel odorants in complex environments.multielectrode recording | network dynamics | optogenetics S ensory systems, even when presented with fixed stimuli, use dynamic neural representations that change over time. These changes range from simple potentiation or adaptation to more complex temporal patterns (1, 2). These dynamics can persist even after the cessation of stimulus, which can take the form of an off-response or prolonged aftereffect. Aftereffects have been intensely studied in vision (1, 3) and also observed in audition (4, 5), touch (6, 7), taste (here the afterimages may be due to persistent ligand binding) (8, 9), and insect olfaction (10, 11). In mammalian olfaction, the only reported aftereffect is a "persistent afterdischarge" following high concentration odors (12).Olfaction is an active process that is coordinated by breathing (2, 13). Odorants bind to odorant receptor neurons (ORNs) in the epithelium, which synapse onto mitral/tufted (M/T) cells in the olfactory bulb (OB) at precisely defined glomeruli. Direct recordings of ORNs in rats show that ORNs are excited by odors and that activity can last for seconds after odor cessation (14). Others have measured the output of ORNs, by imaging glomeruli, and found that the response is gated by each breath and that the amplitude decreases with time (13, 15). The importance of breath segmentation for M/T cells has recently been shown in awake subjects, where neurons respond with precise, phasic firing patterns (16-18). However, these recordings have focused on how information is represented during the first breath, as rodents can identify odors in a single breath (19)(20)(21). Activity in piriform cortex is also segmented by breaths, and neurons there respond sparsely (22,23), and with a...

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“…Unlike acute AOB slice experiments, which also expose circuit elements for electrophysiological and optical recordings, this preparation retains all sensory afferents and intra-AOB connections. Although this can also be said of anesthetized in vivo approaches, the presence of anesthetics necessarily alters neural function, namely excitatory/inhibitory balance, which is crucial for information processing in this and other olfactory circuits 18 . Because the preparation avoids the use of anesthetics, and because the AOB surface is completely exposed to the superfusate, it is amenable to pharmacological inquiries into local neural processing.…”

Section: Discussionmentioning

confidence: 99%

<em>Ex Vivo</em> Preparations of the Intact Vomeronasal Organ and Accessory Olfactory Bulb

Doyle

Hammen

Meeks

2014

JoVE

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The mouse accessory olfactory system (AOS) is a specialized sensory pathway for detecting nonvolatile social odors, pheromones, and kairomones. The first neural circuit in the AOS pathway, called the accessory olfactory bulb (AOB), plays an important role in establishing sextypical behaviors such as territorial aggression and mating. This small (<1 mm 3 ) circuit possesses the capacity to distinguish unique behavioral states, such as sex, strain, and stress from chemosensory cues in the secretions and excretions of conspecifics. While the compact organization of this system presents unique opportunities for recording from large portions of the circuit simultaneously, investigation of sensory processing in the AOB remains challenging, largely due to its experimentally disadvantageous location in the brain. Here, we demonstrate a multi-stage dissection that removes the intact AOB inside a single hemisphere of the anterior mouse skull, leaving connections to both the peripheral vomeronasal sensory neurons (VSNs) and local neuronal circuitry intact. The procedure exposes the AOB surface to direct visual inspection, facilitating electrophysiological and optical recordings from AOB circuit elements in the absence of anesthetics. Upon inserting a thin cannula into the vomeronasal organ (VNO), which houses the VSNs, one can directly expose the periphery to social odors and pheromones while recording downstream activity in the AOB. This procedure enables controlled inquiries into AOS information processing, which can shed light on mechanisms linking pheromone exposure to changes in behavior. Video LinkThe video component of this article can be found at

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Dynamic Sensory Representations in the Olfactory Bulb: Modulation by Wakefulness and Experience

Cited by 237 publications

References 68 publications

CaMKIIα Expression Defines Two Functionally Distinct Populations of Granule Cells Involved in Different Types of Odor Behavior

CaMKIIα Expression Defines Two Functionally Distinct Populations of Granule Cells Involved in Different Types of Odor Behavior

Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage

<em>Ex Vivo</em> Preparations of the Intact Vomeronasal Organ and Accessory Olfactory Bulb

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