Browsing by Author "Franks, Kevin M"
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Item Open Access Odor Coding by Distinct Classes of Principal Neurons in Piriform Cortex(2022) Nagappan, ShivathmihaiUnderstanding the roles that distinct neuron types play within a neural circuit will provide important mechanistic insight into understanding what the circuit does and how it does it. Piriform cortex (PCx) is the largest cortical recipient of odor information from the olfactory bulb (OB). It is thought to be the locus of odor perception and has been linked to several other crucial olfactory processing functions. However, the circuit mechanisms by which many of these ascribed functions occur as well as a comprehensive description of the role of PCx in olfaction remain unclear. PCx contains several different types of excitatory principal neurons. The two main types are semilunar cells (SL) and superficial pyramidal cells (PYR). SLs and PYRs have distinct morphologies, local connectivity, biophysical properties, and downstream projection targets, signifying potentially different roles in odor processing. An incisive study of if and how SLs and PYRs differentially encode odors will advance our understanding of PCx function and olfactory processing, as a whole.Odor processing in PCx has been hypothesized to occur in two sequential stages. First, SLs receive and integrate afferent OB inputs and then PYRs receive, transform, and transmit SL inputs to downstream regions. To probe if and how these two cell types differentially process odor information, I recorded from populations of optogenetically identified SLs and PYRs in awake, head-fixed mice. I then characterized their odor response properties, and selectively manipulated SL activity while mice were passively smelling odors and performing an odor-driven behavior. I found that SLs and PYRs received sensory information from the OB directly and simultaneously, and PYRs did not rely on SL activity to respond to odors, suggesting that these two cell types form parallel channels for processing odor information. Additionally, SLs and PYRs exhibited differences in odor response properties that were consistent with their distinct local connectivity, suggesting that distinct cell types differentially transform odor information. Finally, SLs and PYRs have distinct roles in mediating odor-driven behaviors. Together, my data show that SLs and PYRs form parallel channels for differentially processing odor information in and through PCx. More broadly, my findings provide evidence that PCx contains a functionally diverse population of neurons. Registering specific PCx functions to specific neuron types or subpopulations of neurons will provide a framework for determining what it is that PCx does for olfaction and how it does it.
Item Open Access Parallel processing by distinct classes of principal neurons in the olfactory cortex.(eLife, 2021-12) Nagappan, Shivathmihai; Franks, Kevin MUnderstanding how distinct neuron types in a neural circuit process and propagate information is essential for understanding what the circuit does and how it does it. The olfactory (piriform, PCx) cortex contains two main types of principal neurons, semilunar (SL) and superficial pyramidal (PYR) cells. SLs and PYRs have distinct morphologies, local connectivity, biophysical properties, and downstream projection targets. Odor processing in PCx is thought to occur in two sequential stages. First, SLs receive and integrate olfactory bulb input and then PYRs receive, transform, and transmit SL input. To test this model, we recorded from populations of optogenetically identified SLs and PYRs in awake, head-fixed mice. Notably, silencing SLs did not alter PYR odor responses, and SLs and PYRs exhibited differences in odor tuning properties and response discriminability that were consistent with their distinct embeddings within a sensory-associative cortex. Our results therefore suggest that SLs and PYRs form parallel channels for differentially processing odor information in and through PCx.Item Open Access Recurrent circuitry is required to stabilize piriform cortex odor representations across brain states.(eLife, 2020-07-14) Bolding, Kevin A; Nagappan, Shivathmihai; Han, Bao-Xia; Wang, Fan; Franks, Kevin MPattern completion, or the ability to retrieve stable neural activity patterns from noisy or partial cues, is a fundamental feature of memory. Theoretical studies indicate that recurrently connected auto-associative or discrete attractor networks can perform this process. Although pattern completion and attractor dynamics have been observed in various recurrent neural circuits, the role recurrent circuitry plays in implementing these processes remains unclear. In recordings from head-fixed mice, we found that odor responses in olfactory bulb degrade under ketamine/xylazine anesthesia while responses immediately downstream, in piriform cortex, remain robust. Recurrent connections are required to stabilize cortical odor representations across states. Moreover, piriform odor representations exhibit attractor dynamics, both within and across trials, and these are also abolished when recurrent circuitry is eliminated. Here, we present converging evidence that recurrently-connected piriform populations stabilize sensory representations in response to degraded inputs, consistent with an auto-associative function for piriform cortex supported by recurrent circuitry.Item Embargo Salience encoding in the mouse olfactory system(2024) Diaz, CarolynInternal representations of the external world guide organisms in executing appropriate behavior. The olfactory system in mice is a prime model of this process as mice rely heavily on their sense of smell to survive and determine whether to approach and investigate or avoid and flee. Otherwise known as valence, this is the intrinsic quality of the attractiveness or averseness of an odor and is arguably the first aspect of description organisms use to describe and categorize odors. Even before this categorization, these odorants must be defined as salient. The salience of a stimulus is defined as the intensity of a stimulus and serves to direct the attention of an organism to focus their perceptual and cognitive resources on the pertinent sensory stimulus. Furthermore, many odors trigger instinctive aversive or attractive responses, thus carrying an innate, unlearned value.While several higher-order olfactory regions have been implicated in processing innate valence of odorants, none have been shown to harbor an internal representation of innate odor valence. The central amygdala (CeA) has largely been studied in the context of emotion and fear processing, with studies demonstrating encoding of both innate and learned valence to various stimuli. One subpopulation of cells in the CeA, activated by general anesthetics (CeAGA), has been shown to be responsive to innately salient pain stimuli. To probe whether cells within the CeA encode innate valence of odorant stimuli, I recorded odor-evoked neural responses from populations of optogenetically identified CeAGA cells in awake, head-fixed mice and characterized their odor response properties. I found that CeAGA neurons respond to a variety of odorants and encode innate odor salience. Because CeAGA receives substantial input from a region called the amygdala-piriform transition zone (AmPir), which has been implicated in predator odor processing, I recorded the odor-evoked neural responses from populations of cells within this region. I found that AmPir shows odor response properties similar to piriform and does not harbor a representation of innate odor salience. Finally, the strongly valent predator odor 2MT induces robust defensive behaviors in mice. To probe the role of CeA cells in these defensive behaviors, I optogenetically manipulated their activity in the presence of innately salient predator odor and pain stimuli. I found no robust changes in defensive behaviors to predator odor and pain stimuli. Together, these studies reveal the first evidence of innate odor categorization in the mouse through innate odor salience.
Item Open Access Structure and flexibility in cortical representations of odour space(Nature, 2020-07) Pashkovski, Stan L; Iurilli, Giuliano; Brann, David; Chicharro, Daniel; Drummey, Kristen; Franks, Kevin M; Panzeri, Stefano; Datta, Sandeep RobertItem Open Access The spiking output of the mouse olfactory bulb encodes large-scale temporal features of natural odor environments.(bioRxiv, 2024-07-01) Lewis, Suzanne M; Suarez, Lucas M; Rigolli, Nicola; Franks, Kevin M; Steinmetz, Nicholas A; Gire, David HIn natural odor environments, odor travels in plumes. Odor concentration dynamics change in characteristic ways across the width and length of a plume. Thus, spatiotemporal dynamics of plumes have informative features for animals navigating to an odor source. Population activity in the olfactory bulb (OB) has been shown to follow odor concentration across plumes to a moderate degree (Lewis et al., 2021). However, it is unknown whether the ability to follow plume dynamics is driven by individual cells or whether it emerges at the population level. Previous research has explored the responses of individual OB cells to isolated features of plumes, but it is difficult to adequately sample the full feature space of plumes as it is still undetermined which features navigating mice employ during olfactory guided search. Here we released odor from an upwind odor source and simultaneously recorded both odor concentration dynamics and cellular response dynamics in awake, head-fixed mice. We found that longer timescale features of odor concentration dynamics were encoded at both the cellular and population level. At the cellular level, responses were elicited at the beginning of the plume for each trial, signaling plume onset. Plumes with high odor concentration elicited responses at the end of the plume, signaling plume offset. Although cellular level tracking of plume dynamics was observed to be weak, we found that at the population level, OB activity distinguished whiffs and blanks (accurately detected odor presence versus absence) throughout the duration of a plume. Even ~20 OB cells were enough to accurately discern odor presence throughout a plume. Our findings indicate that the full range of odor concentration dynamics and high frequency fluctuations are not encoded by OB spiking activity. Instead, relatively lower-frequency temporal features of plumes, such as plume onset, plume offset, whiffs, and blanks, are represented in the OB.