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Murthy, V. N.

Publications and source records attributed to Murthy, V. N..

7 recordsLinked to original sources

Carpenter ants use diverse antennae sampling strategies to track odor trails

Directed and meaningful animal behavior depends on the ability to sense key features in the environment. Among the different environmental signals, olfactory cues are critically important for foraging, navigation, and social communication in many species, including ants. Ants use their two antennae to explore the olfactory world, but how they do so remains largely unknown. In this study, we use high resolution videography to characterize the antennae dynamics of carpenter ants (Camponotus pennsylvanicus). Antennae are highly active during both tracking and exploratory behavior. When tracking, ants used several distinct behavioral strategies with stereotyped antennae sampling patterns (which we call sinusoidal behavior, probing, and trail following). In all behaviors, left and right antennae movements were anti-correlated, and tracking ants exhibited biases in the use of left vs right antenna to sample the odor trail. These results suggest non-redundant roles for the two antennae. In one of the behavioral modules (trail following), ants used both antennae to detect trail edges and direct subsequent turns, suggesting a specialized form of tropotaxis. Lastly, removal of an antenna resulted not only in less accurate tracking but also in changes in the sampling pattern of the remaining antenna. Our quantitative characterization of odor trail tracking lays a foundation to build better models of olfactory sensory processing and sensorimotor behavior in terrestrial insects.\n\nSummary StatementHigh resolution imaging of antennae reveals distinct patterns of sampling with non-redundant roles in odor tracking.

animal behavior and cognition

Olfactory marker protein regulates refinement of the glomerular map

The olfactory glomerulus is the anatomical and functional unit of the olfactory bulb, defined by convergent input from olfactory sensory neuron (OSN) axons expressing the same type of odorant receptor (OR). A key marker of mature OSNs is the olfactory marker protein (OMP), whose deletion has been associated with deficits in OSN signal transduction and odor discrimination. Here, we have investigated glomerular odor responses and anatomical architecture in mice in which one or both alleles of OMP were replaced by the fluorescent synaptic activity reporter, synaptopHluorin (OMP+/- and OMP-/- mice, respectively). Functionally heterogeneous glomeruli, that is, ones with micro-domains with distinct odor responses were rare in OMP+/- mice, but occurred frequently in OMP-/- mice. Genetic targeting of single ORs revealed that these micro-domains arise from anomalous co-innervation of individual glomeruli by OSNs expressing different ORs. The glomerular mistargeting of OSNs in the absence of OMP is restricted to a local neighborhood of a few glomerular diameters. Our studies document functional heterogeneity in sensory input within individual glomeruli and uncover its anatomical correlate, revealing an unexpected role for OMP in the formation and refinement of the glomerular olfactory map.

neuroscience

Calcium-activated chloride channels clamp odor-evoked spike activity in olfactory receptor neurons

The calcium-activated chloride channel anoctamin-2 (Ano2) is thought to amplify transduction currents in ORNs, a hypothesis supported by previous studies in dissociated neurons from Ano2-/- mice. Paradoxically, despite a reduction in transduction currents in Ano2-/- ORNs, their spike output for odor stimuli may be higher. We examined the role of Ano2 in ORNs in their native environment in freely breathing mice by imaging activity in ORN axons as they arrive in the olfactory bulb glomeruli. Odor-evoked responses in ORN axons of Ano2-/- mice were consistently larger for a variety of odorants and concentrations. In an open arena, Ano2-/- mice took longer to approach a localized odor source than wild-type mice, revealing clear olfactory behavioral deficits. Our studies provide the first in vivo evidence toward an alternative role for Ano2 in the olfactory transduction cascade, where it may serve as a feedback mechanism to clamp ORN spike output.

neuroscience

Mosaic representations of odors in the input and output layers of the mouse olfactory bulb

The elementary stimulus features encoded by the olfactory system remain poorly understood. We examined the relationship between 1,666 physical-chemical descriptors of odors and the activity of olfactory bulb inputs as well as outputs in awake mice. Glomerular and M/T cell responses were sparse and locally heterogeneous, with only a coarse dependence of glomerular positions on physical-chemical properties. Odor features represented by ensembles of M/T cells were overlapping, but distinct from those represented in glomeruli, consistent with extensive interplay between feedforward and feedback inputs to the bulb. This reformatting was well-described as a rotation in odor space. The descriptors accounted for a small fraction in response variance, and the similarity of odors in physical-chemical space was a poor predictor of similarity in neuronal representations. Our results suggest that commonly used physical-chemical properties are not systematically represented in bulbar activity and encourage further search for better descriptors of odor space.

neuroscience

Antagonism in olfactory receptor neurons and its implications for the perception of odor mixtures

Natural environments feature mixtures of odorants of diverse quantities, qualities and complexities. Olfactory receptor neurons (ORNs) are the first layer in the sensory pathway and transmit the olfactory signal to higher regions of the brain. Yet, the response of ORNs to mixtures is strongly non-additive, and exhibits antagonistic interactions among odorants. Here, we model the processing of mixtures by mammalian ORNs, focusing on the role of inhibitory mechanisms. Theoretically predicted response curves capture experimentally determined glomerular responses imaged by a calcium indicator expressed in ORNs of live, breathing mice. Antagonism leads to an effective \"normalization\" of the ensemble glomerular response, which arises from a novel mechanism involving the distinct statistical properties of receptor binding and activation, without any recurrent neuronal circuitry. Normalization allows our encoding model to outperform noninteracting models in odor discrimination tasks, and to explain several psychophysical experiments in humans.

neuroscience

Embryonic and postnatal neurogenesis produce functionally distinct subclasses of dopaminergic neuron

Most neurogenesis in the mammalian brain is completed embryonically, but in certain areas the production of neurons continues throughout postnatal life. The functional properties of mature postnatally-generated neurons often match those of their embryonically-produced counterparts. However, we show here that in the olfactory bulb (OB), embryonic and postnatal neurogenesis produce functionally distinct subpopulations of dopaminergic (DA) neurons. We define two subclasses of OB DA neuron by the presence or absence of a key subcellular specialisation: the axon initial segment (AIS). Large AIS-positive axon-bearing DA neurons are exclusively produced during early embryonic stages, leaving small anaxonic AIS-negative cells as the only DA subtype generated via adult neurogenesis. These populations are functionally distinct: large DA cells are more excitable, yet display weaker and - for certain long-latency or inhibitory events - more broadly-tuned responses to odorant stimuli. Embryonic and postnatal neurogenesis can therefore generate distinct neuronal subclasses, placing important constraints on the functional roles of adult-born neurons in sensory processing.

neuroscience

Distinct projection patterns of different classes of layer 2 principal neurons in the olfactorycortex

Processing of olfactory information in the anterior piriform cortex (APC) is widely thought to be non-topographic due to distributed projections from the olfactory bulb (OB). Layer 2 principal neurons in the APC can be divided into 2 subtypes: semilunar (SL) and superficial pyramidal (SP) cells. Although it is known that SL and SP cells receive differential inputs from the OB, little is known about their projection pattern to downstream structures, such as the posterior piriform cortex (PPC). Here we examined feedforward and feedback axonal projections of SL and SP cells using a combination of mouse genetics, and retrograde labeling. Retrograde tracing from the OB or PPC showed that the APC projects to these higher and lower brain regions mainly through layer 2b cells, while dual-labeling revealed a sizeable fraction of cells extending collaterals to both target regions. Furthermore, a transgenic mouse line specifically labeling SL cells showed that they send profuse axonal projections to olfactory cortical areas, but not to the OB. These findings support a model in which information flow from SL to SP cells and back to the OB forms a hierarchical feedback circuit whereas the two cell types process recurrent and feedforward information in a parallel manner.

neuroscience