Chemosensory Information Processing

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Trigeminal fibers terminate within the facial mucosa and skin and transmit tactile, proprioceptive, chemical, and nociceptive sensations. Trigeminal sensations can arise from the direct stimulation of intraepithelial free nerve endings or indirectly through information transmission from adjacent cells at the peripheral innervation area.

For mechanical and thermal cues, communication processes between skin cells and somatosensory neurons have already been suggested.

Chemosensory Information Processing by Detlev Schild, Paperback | Barnes & Noble®

To address this, Markus Rothermel presented data on some of the pathways involved. Diagram of bottom-up and top-down inputs into the olfactory bulb. Olfactory sensory neurons OSNs located in the olfactory epithelium project axons into the olfactory bulb OB , transmitting sensory information to this brain region. Mitral cells also make connections with granule cells GCs and PGs. Several regions of the brain, including the Raphe, anterior olfactory nucleus AON and horizontal limb of the diagonal band of Broca HDB also project back to the OB top—down to modulate the perception of odors.

Courtesy of A. Puche, modified from Aungst et al.

Olfaction and olfactory adaptation: From anatomy to neuronal coding

The OB receives centrifugal input from two major types of modulatory systems whose role in shaping early olfactory processing remains unclear: classical neuromodulatory inputs and cortical inputs. The functional investigation of these systems in vivo is complicated by the fact that most of these centers are comprised of heterogeneous cell populations and typically project to multiple brain areas that themselves are interconnected.

The ability to drive optogenetic tools in restricted neuronal subpopulations and their axonal processes Atasoy et al.

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To examine how neuromodulatory projections to the OB shape output neuron activity, optogenetic activation of the axons of cholinergic neurons projecting from the horizontal limb of the diagonal band of Broca HDB to the OB in ChAT choline acetyltransferase -Cre animals was used Rothermel et al. This modulation was rapid and transient. Replication of the experimental setup in this publication, using the same mouse line, method of anesthesia and stimulation protocol, was not able to clarify all discrepancies however, it was clearly shown that axonal versus somatic stimulation i.

To investigate another source of neuromodulatory input to the OB, activation of serotonergic centrifugal projections originating in the raphe nucleus in Slc6a4 solute carrier family 6, serotonin transporter -cre animals was used Brunert et al. These results are in general agreement with a recent publication that used an imaging approach and observed that mitral cell activity increases as well as decreases in response to raphe stimulation Kapoor et al.

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Selective expression of GCaMP in AON projection neurons revealed that odorants evoked large signals in the axon terminals in the OB that were transient and coupled to odorant inhalation both in the anesthetized and awake mouse. These data suggest that feedback from AON to the OB is rapid and robust across different brain states. In comparison to other work Boyd et al. The strength of AON feedback signals increased during wakefulness, suggesting a state-dependent modulation of cortical feedback. Finally, AON feedback projections were also activated when stimulating other neuromodulatory centers—for example, the HDB.

These results point to the AON as a multifunctional cortical area that provides ongoing feedback to the OB and also serves as a descending relay for other neuromodulatory systems.

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The work presented by Rothermel detailed the different pathways that provide top—down input to the OB. These pathways can be used by multiple, different behavior states, and by a large number of neurotransmitters and hormones. Following this talk, Debi Fadool presented work identifying the roles that specific neurohormones can play to regulate neuronal function and the pathways to which they converge.

In mammals, olfactory perception has an intricate link with feeding behavior, reward and appetite. It has long been known that odors are a determinant for food choice or rejection, but also that feeding state, by controlling internal energy homeostasis, can regulate the perception of odors at both central and peripheral levels [for review see Palouzier-Paulignan et al. In this scope, Fadool and colleagues investigated if an unbalanced energy homeostasis could disrupt olfactory anatomy and function.

These studies found that mice challenged with fatty diets exhibit a loss of OSNs, a reduction in glomerular projections, an associated reduction in electro-olfactogram amplitude, and olfactory dysfunction in odor discrimination and odor reversal learning assessed by olfactometry Tucker et al. They currently hypothesize that the olfactory system is designed to encode external and internal chemical information, the latter being energy important molecules that modulate mitral cell firing frequency to give information about the state of nutrient availability.

Over the years, the Fadool laboratory has found electrophysiological evidence for the modulation of the primary output neurons of the OB, mitral cells, by several nutrients and hormones, such as insulin Fadool et al. All of these neurohormones or metabolic factors are found to modulate firing frequency of mitral cells by targeting the voltage-dependent potassium channel, Kv1. These approaches have allowed the discovery that insulin and GLP-1 receptors are co-localized in mitral cells and thereby have the capacity to coordinate excitability.

In current-clamp recordings of ex vivo OB slices, GLP-1 and its synthetic agonist, Exendin-4, increased firing frequency of mitral cells in a dose-dependent manner that is dependent upon Kv1. Spike analysis revealed that increased excitability was attributed to a decrease in the action potential pause duration interburst interval rather than interspike interval. Those results were also confirmed by using voltage ramps and ion substitution to support a decrease in potassium conductance following GLP-1 application, which was not present in transgenic mice deficient for Kv1.

Current-clamp recordings showed that optogenetic activation of PPG-neurons resulted in a biphasic inhibition-excitation control of action potential firing in mitral cells, revealing a novel microcircuit involving the deep short axon cells, granule cells, and mitral cells in the OB.

This unique modulation of mitral cells by PPG-neurons suggests a fine tuning of the olfactory output.

Further investigation will be needed to determine the reciprocal molecular interaction between glucose sensing, insulin, and GLP-1 pathways in the OB, as well as their combined action on the output of olfactory processing. The importance of centrifugal projections to the OB, in particular coming from the hypothalamic areas, remains to be systemically studied to determine the origin of the signals linking the regulation of olfaction with feeding states.

Model of neuromodulatory signaling in the olfactory bulb relying upon metabolic cues. Glucose, insulin, and glucagon-like peptide GLP-1 levels are sensed in mitral cells of the OB through phosphorylation and post-translational changes of a potassium ion channel, Kv1. While hunger and satiety are easily identifiable physiological processes incorporating learning and expectation into neuromodulation are less well defined.

Animals come in contact with numerous odors in their daily lives. How does the nervous system know to give more attention to some odors over others? Experience is one way in which this can occur, modulating the system to prime it for detection of specific odors. In his talk, John McGann presented a range of data supporting the claim that neural processing of olfactory information incorporates learned information about the world as early as the axon terminals of the OSNs potentially through synapses with periglomular PG cells Figure 1.

Methods in rodent chemosensory cognition

He framed expectations as the use of pre-existing information, generally learned from previous experience, to anticipate or interpret incoming sensory input. Prior information about the olfactory world is potentially available directly to the olfactory system through long-term experience-dependent plasticity, but information about how odors relate to non-olfactory stimuli e. In the olfactory system, critical forms of these expectations include i which odorants are common in the environment, ii which odorants predict ecologically-important events, and iii when can a given odor be expected based on other stimuli in the environment.

The talk applied this conceptual framework to explore how the population-level neural representations of odorants in the OB could exhibit each form of expectation. Optical neurophysiological methods were used to observe the odorant-evoked neural activity of the OSN presynaptic terminals, including presynaptic calcium signaling in dye-loaded mice Wachowiak and Cohen and exocytosis in OMP-spH mice Bozza et al.

This neural plasticity is correlated with changes in OSN neurotransmitter release dynamics during odorant presentation and a modest increase in olfactory discrimination acuity Kass et al.


This result was obtained using a strong exposure paradigm. In this paradigm, the mouse lives in an exposure chamber where an odorant is pumped into the chamber for 4 out of every 8 hours. This paradigm is unlike the briefer odor exposures employed by Takaki Komiyama in his experiments Kato et al. To address the second form of plasticity, previously published data were shown illustrating that discriminative odor-cued fear conditioning, where the mouse learns that one odorant predicts an impending electric shock while another odorant does not, evokes odor-specific enhancement of the OSN synaptic output evoked by the shock-predictive odorant Kass et al.

Among the sensory systems, chemosensation is the least studied. Substantial amount of work was done to understand the chemosensory coding in the level of receptor neurons. However, little is known about the chemosensory information processing in the higher brain areas.

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Ultimately, these experiments will help us to understand the fundamental principles of sensory information processing in the brains of vertebrates, including humans. Model system : zebrafish. Nat Neuroscience: 13 4 Ann N Y Acad Sci.