Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI

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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...

Section: Discussionmentioning

confidence: 94%

Section: Effects Of Brain States On the Lfp Signals And Representatiomentioning

confidence: 99%

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confidence: 99%

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

Gong

2011

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“…As a result, odor stimulation reproducibly activates small glomeruli ensembles. These patterns of glomerular activation have been revealed by several methods including (i) BOLD fMRI (18)(19)(20), (ii) optical imaging of calcium (21), voltage (22), and intrinsic signals (23)(24)(25)(26)(27)(28), (iii) electrophysiological recordings (29)(30)(31), and (iv) measurements of 2-deoxyglucose consumption (32,33). Here, we use two-photon imaging to determine with a high spatial resolution the relationship between RBC flow in individual capillaries and neuronal activation.…”

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confidence: 99%

Two-photon imaging of capillary blood flow in olfactory bulb glomeruli

Chaigneau

Oheim

Audinat

et al. 2003

280

239

Analysis of the spatiotemporal coupling between neuronal activity and cerebral blood flow requires the precise measurement of the dynamics of RBC flow in individual capillaries that irrigate activated neurons. Here, we use two-photon microscopy in vivo to image individual RBCs in glomerular capillaries in the rat dorsal olfactory bulb. We find that odor stimulation evokes capillary vascular responses that are odorant-and glomerulus-specific. These responses consist of increases as well as decreases in RBC flow, both resulting from independent changes in RBC velocity or linear density. Finally, measuring RBC flow with micrometer spatial resolution and millisecond temporal resolution, we demonstrate that, in olfactory bulb superficial layers, capillary vascular responses precisely outline regions of synaptic activation.N oninvasive imaging techniques have been widely used to determine the distributions of brain regions activated by sensory stimulations. Although several techniques detect contrast changes based on activity-dependent hemodynamic changes, the precise coupling between neuronal activation, energy demand, and changes in blood flow remains unclear (for review, see refs. 1-3). Analysis of the coupling requires a simultaneous measurement of the activity of neurons and the dynamics of local blood flow. Recently, measurements of extracellular activity combined with functional MRI (fMRI) have shown that field potential amplitude (4) and spiking frequency (5) are related to blood oxygen level-dependent (BOLD) signals (6, 7). These observations are a technical tour de force; yet, the spatial and temporal resolutions of fMRI are not sufficient to provide a precise understanding of the entire chain of cellular and vascular events elicited by the stimulation. In the cerebellar cortex, recent ''semiinvasive'' techniques requiring a craniotomy and using electrophysiological recordings combined with laser Doppler flowmetry have allowed more precise investigations and have demonstrated that the relationship between presynaptic and postsynaptic activity with blood flow varies according to the activated input (8-11). However, these studies did not measure blood flow in the individual capillaries that precisely irrigate the activated neurons, a prerequisite to analyzing the neurovascular coupling in detail.Two-photon microscopy imaging of blood flow represents an alternative approach to studying this coupling (12) in vivo. It allows measurements of RBC flow with micrometer spatial resolution and millisecond temporal resolution in individual capillaries and can be combined with electrophysiological recordings (13,14). If performed in a brain region where synaptic interactions are topographically organized, two-photon imaging should allow measurements of vascular flow in a given capillary irrigating a small population of neurons and glial cells. Because of its anatomical and functional organization, the rodent main olfactory bulb (15) is particularly suitable for such a study: all sensory cells expressing a given odorant r...

“…This phenomenon was observed regardless of which bulbar layer (mitral, granular) the recordings were obtained from, the type of anesthetic (pentobarbital, chloral hydrate) that was used to achieve the baseline state, and the type (aldehyde, ketone, ester) and concentration (up to fivefold difference) of the odor that was exposed to the rat. Previous optical imaging and fMRI studies examined odor-induced bulbar activity patterns and how topologies and intensities vary with concentration (11,12). For a given odor the topology of the bulbar activity pattern is largely independent of concentration, but the intensity of bulbar activity correlates positively with concentration.…”

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Evidence for the importance of measuring total brain activity in neuroimaging

Hyder

Rothman

2011

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A principal goal in neuroscience is to understand how neuronal populations across different brain regions process information from the vibrant world, rich in moment-to-moment variations of sight, smell, sound, touch, etc. Traditional inquiries examine how the evoked neuronal responses differ with stimuli (e.g., sound or touch). However, the brain detects stimuli reliably even when ambient (or background) conditions shift owing to external (e.g., light vs. dark) and/or internal (e.g., alert vs. sleepy) factors. Recent investigations have assessed whether evoked neuronal activity (ΔN) varies when the brain's operational (or baseline) state is altered, whereby including an independent measure of baseline (or spontaneous) neuronal activity (N o ) provides a total measure of neuronal activity for the perturbed state (N). In PNAS, Li et al.(1) demonstrate in the rat's olfactory bulb that total bulbar activity level reached upon odor exposure (i.e., N = ΔN + N o )-measured by extracellular recordings-is independent of the bulb's baseline activity level. This result agrees well with previous observations from other cortical sensory systems, using a variety of neuroimaging techniques [e.g., functional MRI (fMRI), optical imaging, and electrophysiology (2-9)]. Taken together, these studies (1-9) imply that there may be inherent neuronal mechanisms to ensure a similar level of information transfer from sensory input, regardless of external/internal situations that may impact the brain's baseline state (10).Li et al.(1) measured odor-induced bulbar activity under different baseline states. Whereas spontaneous neuronal activity in the two baseline states (achieved by varying anesthetic doses) differed by approximately twofold, nearly identical levels of total neuronal activity were reached upon the same odor exposure from each baseline state. This phenomenon was observed regardless of which bulbar layer (mitral, granular) the recordings were obtained from, the type of anesthetic (pentobarbital, chloral hydrate) that was used to achieve the baseline state, and the type (aldehyde, ketone, ester) and concentration (up to fivefold difference) of the odor that was exposed to the rat. Previous optical imaging and fMRI studies examined odor-induced bulbar activity patterns and how topologies and intensities vary with concentration (11, 12). For a given odor the topology of the bulbar activity pattern is largely independent of concentration, but the intensity of bulbar activity correlates positively with concentration. Because these studies were conducted with only one baseline state, results from Li et al. (1) extend the previous findings regarding the neuronal encoding of quality (with pattern topology) and concentration of odor (with pattern intensity) across different baseline states. If the baseline state variation studies of the olfactory bulb (1) are combined with similar studies of the olfactory cortex (13), we may deduce that, regardless of the baseline state, maintaining high-fidelity transmission of smell signals-from the...