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

Abstract

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...

Evidence for the importance of measuring total brain activity in neuroimaging

“…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)(2)(3)(4)(5)(6)(7)(8)(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).…”

“…A descriptive example, as shown in Fig. 1A and which is comparable to data presented by Li et al (1), illustrates behavior of a neuronal population (Fig. 1A, Left) as well as its dynamic pattern (Fig.…”

“…1B, Left). Therefore, if Li et al (1) subtracted the baseline neuronal activity measured during odor stimulation (Fig. 1B, Right), they would arrive at the opposite conclusion, that the neuronal activity during odor simulation is baseline dependent.…”

“…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)].…”

Recent progress of sensory system research in China

“…Additionally, investigation by Xu and colleagues (Wuhan Institute of Physics and Mathematics, Chinese Academy of Sciences) indicated that the M/T cells can encode the odor locations [17]. Their further work suggested the neural representation of peripheral stimulation in rat OB is independent of brain state [18].…”