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1. An Evolutionary Microcircuit Approach to the Neural Basis of High Dimensional Sensory Processing in Olfaction

   https://doi.org/10.3389/fncel.2021.658480  

   Shepherd, Gordon M.; Rowe, Timothy B.; Greer, Charles A. (April 2021, Frontiers in Cellular Neuroscience)

   null (Ed.)

   Odor stimuli consist of thousands of possible molecules, each molecule with many different properties, each property a dimension of the stimulus. Processing these high dimensional stimuli would appear to require many stages in the brain to reach odor perception, yet, in mammals, after the sensory receptors this is accomplished through only two regions, the olfactory bulb and olfactory cortex. We take a first step toward a fundamental understanding by identifying the sequence of local operations carried out by microcircuits in the pathway. Parallel research provided strong evidence that processed odor information is spatial representations of odor molecules that constitute odor images in the olfactory bulb and odor objects in olfactory cortex. Paleontology provides a unique advantage with evolutionary insights providing evidence that the basic architecture of the olfactory pathway almost from the start ∼330 million years ago (mya) has included an overwhelming input from olfactory sensory neurons combined with a large olfactory bulb and olfactory cortex to process that input, driven by olfactory receptor gene duplications. We identify a sequence of over 20 microcircuits that are involved, and expand on results of research on several microcircuits that give the best insights thus far into the nature of the high dimensional processing. 

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2. Getting Nosy: Olfactory Rosette Morphology and Lamellar Microstructure of Two Chondrichthyan Species

   https://doi.org/10.1093/icb/icae103  

   Simonitis, Lauren_Eve; Clark, Aubrey_E; Barskaya, Elizaveta; Castillo, Gabriella; Porter, Marianne; Meredith, Tricia (July 2024, Integrative And Comparative Biology)

   Synopsis To smell, fish rely on passive water flow into their olfactory chambers and through their olfactory rosettes to detect chemical signals in their aquatic environment. The olfactory rosette is made up of secondarily folded tissues called olfactory lamellae. The olfactory morphology of cartilaginous fishes varies widely in both rosette gross morphology and lamellar microstructure. Previous research has shown differences in lamellar sensory morphology depending on the position along the rosette in hammerheads (family Sphyrnidae). Here, we investigate if this pattern continues in members of two other chondrichthyan families: Squalidae and Chimaeridae. Using contrast-enhanced microCT and scanning electron microscopy, we investigated patterns in lamellar morphology based on lamellar position along the olfactory rosette in Pacific spiny dogfish (Squalus suckleyi) and spotted ratfish (Hydrolagus colliei). We describe the gross olfactory rosette anatomy and lamellar microstructure of both species. We also put forth a new method, combining 3D morphological microCT data with 2D SEM microstructure data to better approximate lamellar sensory surface area. We found that in both species, lamellae in the center of the rosette were larger with more secondary folds. However, we found no significant differences in lamellar sensory surface area among lamellar positions. Previously, differences in lamellar sensory morphology have been tied to the internal fluid dynamics of the olfactory chamber. It is possible that the internal flow dynamics of these species are like other chondrichthyan models, where water flow patterns differ in the lateral vs the medial part of the organ, and the consistent distribution of sensory tissue does not correspond to this flow. Alternatively, the olfactory morphology of these species may result in uniform flow patterns throughout the olfactory chamber, correlating with the consistent distribution of sensory tissue throughout the organ. This study emphasizes that further investigations into chondrichthyan fluid dynamics is paramount to any future studies on the correlations between distribution of sensory tissues and water flow. 

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3. The influence of olfactory experience on the birthrates of olfactory sensory neurons with specific odorant receptor identities

   https://doi.org/10.1002/dvg.23611  

   Rufenacht, Karlin_E; Asson, Alexa_J; Hossain, Kawsar; Santoro, Stephen_W (June 2024, genesis)

   Summary Olfactory sensory neurons (OSNs) are one of a few neuron types that are generated continuously throughout life in mammals. The persistence of olfactory sensory neurogenesis beyond early development has long been thought to function simply to replace neurons that are lost or damaged through exposure to environmental insults. The possibility that olfactory sensory neurogenesis may also serve an adaptive function has received relatively little consideration, largely due to the assumption that the generation of new OSNs is stochastic with respect to OSN subtype, as defined by the single odorant receptor gene that each neural precursor stochastically chooses for expression out of hundreds of possibilities. Accordingly, the relative birthrates of different OSN subtypes are predicted to be constant and impervious to olfactory experience. This assumption has been called into question, however, by evidence that the birthrates of specific OSN subtypes can be selectively altered by manipulating olfactory experience through olfactory deprivation, enrichment, and conditioning paradigms. Moreover, studies of recovery of the OSN population following injury provide further evidence that olfactory sensory neurogenesis may not be strictly stochastic with respect to subtype. Here we review this evidence and consider mechanistic and functional implications of the prospect that specific olfactory experiences can regulate olfactory sensory neurogenesis rates in a subtype‐selective manner. 

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4. The Role of the Stimulus in Olfactory Plasticity

   https://doi.org/10.3390/brainsci13111553  

   Coppola, David M.; Reisert, Johannes (November 2023, Brain Sciences)

   Cheetham, Claire E. (Ed.)

   Plasticity, the term we use to describe the ability of a nervous system to change with experience, is the evolutionary adaptation that freed animal behavior from the confines of genetic determinism. This capacity, which increases with brain complexity, is nowhere more evident than in vertebrates, especially mammals. Though the scientific study of brain plasticity dates back at least to the mid-19th century, the last several decades have seen unprecedented advances in the field afforded by new technologies. Olfaction is one system that has garnered particular attention in this realm because it is the only sensory modality with a lifelong supply of new neurons, from two niches no less! Here, we review some of the classical and contemporary literature dealing with the role of the stimulus or lack thereof in olfactory plasticity. We have restricted our comments to studies in mammals that have used dual tools of the field: stimulus deprivation and stimulus enrichment. The former manipulation has been implemented most frequently by unilateral naris occlusion and, thus, we have limited our comments to research using this technique. The work reviewed on deprivation provides substantial evidence of activity-dependent processes in both developing and adult mammals at multiple levels of the system from olfactory sensory neurons through to olfactory cortical areas. However, more recent evidence on the effects of deprivation also establishes several compensatory processes with mechanisms at every level of the system, whose function seems to be the restoration of information flow in the face of an impoverished signal. The results of sensory enrichment are more tentative, not least because of the actual manipulation: What odor or odors? At what concentrations? On what schedule? All of these have frequently not been sufficiently rationalized or characterized. Perhaps it is not surprising, then, that discrepant results are common in sensory enrichment studies. Despite this problem, evidence has accumulated that even passively encountered odors can “teach” olfactory cortical areas to better detect, discriminate, and more efficiently encode them for future encounters. We discuss these and other less-established roles for the stimulus in olfactory plasticity, culminating in our recommended “aspirations” for the field going forward. 

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5. Pheromone Perception in Fish: Mechanisms and Modulation by Internal Status

   https://doi.org/10.1093/icb/icad049  

   Bowers, Jessica_M; Li, Cheng-Yu; Parker, Coltan_G; Westbrook, Molly_E; Juntti, Scott_A (June 2023, Integrative And Comparative Biology)

   Synopsis Pheromones are chemical signals that facilitate communication between animals, and most animals use pheromones for reproduction and other forms of social behavior. The identification of key ligands and olfactory receptors used for pheromonal communication provides insight into the sensory processing of these important cues. An individual’s responses to pheromones can be plastic, as physiological status modulates behavioral outputs. In this review, we outline the mechanisms for pheromone sensation and highlight physiological mechanisms that modify pheromone-guided behavior. We focus on hormones, which regulate pheromonal communication across vertebrates including fish, amphibians, and rodents. This regulation may occur in peripheral olfactory organs and the brain, but the mechanisms remain unclear. While this review centers on research in fish, we will discuss other systems to provide insight into how hormonal mechanisms function across taxa. 

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