More Like this

1. Differences in olfactory bulb mitral cell spiking with ortho- and retronasal stimulation revealed by data-driven models

   https://doi.org/10.1371/journal.pcbi.1009169  

   Craft, Michelle F.; Barreiro, Andrea K.; Gautam, Shree Hari; Shew, Woodrow L.; Ly, Cheng (September 2021, PLOS Computational Biology)

   Migliore, Michele (Ed.)

   The majority of olfaction studies focus on orthonasal stimulation where odors enter via the front nasal cavity, while retronasal olfaction, where odors enter the rear of the nasal cavity during feeding, is understudied. The coding of retronasal odors via coordinated spiking of neurons in the olfactory bulb ( OB ) is largely unknown despite evidence that higher level processing is different than orthonasal. To this end, we use multi-electrode array in vivo recordings of rat OB mitral cells ( MC ) in response to a food odor with both modes of stimulation, and find significant differences in evoked firing rates and spike count covariances (i.e., noise correlations). Differences in spiking activity often have implications for sensory coding, thus we develop a single-compartment biophysical OB model that is able to reproduce key properties of important OB cell types. Prior experiments in olfactory receptor neurons ( ORN ) showed retro stimulation yields slower and spatially smaller ORN inputs than with ortho, yet whether this is consequential for OB activity remains unknown. Indeed with these specifications for ORN inputs, our OB model captures the salient trends in our OB data. We also analyze how first and second order ORN input statistics dynamically transfer to MC spiking statistics with a phenomenological linear-nonlinear filter model, and find that retro inputs result in larger linear filters than ortho inputs. Finally, our models show that the temporal profile of ORN is crucial for capturing our data and is thus a distinguishing feature between ortho and retro stimulation, even at the OB. Using data-driven modeling, we detail how ORN inputs result in differences in OB dynamics and MC spiking statistics. These differences may ultimately shape how ortho and retro odors are coded. 

   more » « less
2. Odor encoding by signals in the olfactory bulb

   https://doi.org/10.1152/jn.00449.2022  

   Verhagen, Justus V.; Baker, Keeley L.; Vasan, Ganesh; Pieribone, Vincent A.; Rolls, Edmund T. (February 2023, Journal of Neurophysiology)

   To understand the operation of the olfactory system, it is essential to know how information is encoded in the olfactory bulb. We applied Shannon information theoretic methods to address this, with signals from up to 57 glomeruli simultaneously optically imaged from presynaptic inputs in glomeruli in the mouse dorsal (dOB) and lateral (lOB) olfactory bulb, in response to six exemplar pure chemical odors. We discovered that, first, the tuning of these signals from glomeruli to a set of odors is remarkably broad, with a mean sparseness of 0.83 and a mean signal correlation of 0.64. Second, both of these factors contribute to the low information that is available from the responses of even populations of many tens of glomeruli, which was only 1.35 bits across 33 glomeruli on average, compared with the 2.58 bits required to perfectly encode these six odors. Third, although there is considerable interest in the possibility of temporal encoding of stimulus including odor identity, the amount of information in the temporal aspects of the presynaptic glomerular responses was low (mean 0.11 bits) and, importantly, was redundant with respect to the information available from the rates. Fourth, the information from simultaneously recorded glomeruli asymptotes very gradually and nonlinearly, showing that glomeruli do not have independent responses. Fifth, the information from a population became available quite rapidly, within 100 ms of sniff onset, and the peak of the glomerular response was at 200 ms. Sixth, the information from the lOB was not additive with that of the dOB. NEW & NOTEWORTHY We report broad tuning and low odor information available across the lateral and dorsal bulb populations of glomeruli. Even though response latencies can be significantly predictive of stimulus identity, such contained very little information and none that was not redundant with information based on rate coding alone. Last, in line with the emerging notion of the important role of earliest stages of responses (“primacy”), we report a very rapid rise in information after each inhalation. 

   more » « less
3. 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. 

   more » « less
4. Behavioral discrimination and olfactory bulb encoding of odor plume intermittency

   https://doi.org/10.7554/eLife.85303  

   Gumaste, Ankita; Baker, Keeley L; Izydorczak, Michelle; True, Aaron C; Vasan, Ganesh; Crimaldi, John P; Verhagen, Justus (March 2024, eLife)

   In order to survive, animals often need to navigate a complex odor landscape where odors can exist in airborne plumes. Several odor plume properties change with distance from the odor source, providing potential navigational cues to searching animals. Here, we focus on odor intermittency, a temporal odor plume property that measures the fraction of time odor is above a threshold at a given point within the plume and decreases with increasing distance from the odor source. We sought to determine if mice can use changes in intermittency to locate an odor source. To do so, we trained mice on an intermittency discrimination task. We establish that mice can discriminate odor plume samples of low and high intermittency and that the neural responses in the olfactory bulb can account for task performance and support intermittency encoding. Modulation of sniffing, a behavioral parameter that is highly dynamic during odor-guided navigation, affects both behavioral outcome on the intermittency discrimination task and neural representation of intermittency. Together, this work demonstrates that intermittency is an odor plume property that can inform olfactory search and more broadly supports the notion that mammalian odor-based navigation can be guided by temporal odor plume properties. 

   more » « less
5. Olfactory Sensing and Navigation in Turbulent Environments

   https://doi.org/10.1146/annurev-conmatphys-031720-032754  

   Reddy, Gautam; Murthy, Venkatesh N.; Vergassola, Massimo (March 2022, Annual Review of Condensed Matter Physics)

   Fluid turbulence is a double-edged sword for the navigation of macroscopic animals, such as birds, insects, and rodents. On the one hand, turbulence enables pheromone communication among mates and the possibility of locating food by their odors from long distances. Molecular diffusion would indeed be unable to spread odors over relevant distances in natural conditions. On the other hand, turbulent flows are hard to predict, and learning effective maneuvers to navigate them is challenging, as we discuss in this review. We first provide a summary of the olfactory organs that sense airborne or surface-bound odors, as well as the computational tasks that animals face when extracting information useful for navigation from an olfactory signal. A compendium of the dynamics of turbulent transport emphasizes those aspects that directly impact animals’ behavior. The state of the art on navigational strategies is discussed, followed by a concluding section dedicated to future challenges in the field. 

   more » « less