Person: Klein, Mason
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Klein
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Mason
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Klein, Mason
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Publication Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics(eLife Sciences Publications, Ltd, 2015) Hernandez-Nunez, Luis; Belina, Jonas; Klein, Mason; Si, Guangwei; Claus, Lindsey; Carlson, John R; Samuel, AraviNeural circuits for behavior transform sensory inputs into motor outputs in patterns with strategic value. Determining how neurons along a sensorimotor circuit contribute to this transformation is central to understanding behavior. To do this, a quantitative framework to describe behavioral dynamics is needed. In this study, we built a high-throughput optogenetic system for Drosophila larva to quantify the sensorimotor transformations underlying navigational behavior. We express CsChrimson, a red-shifted variant of channelrhodopsin, in specific chemosensory neurons and expose large numbers of freely moving animals to random optogenetic activation patterns. We quantify their behavioral responses and use reverse-correlation analysis to uncover the linear and static nonlinear components of navigation dynamics as functions of optogenetic activation patterns of specific sensory neurons. We find that linear–nonlinear models accurately predict navigational decision-making for different optogenetic activation waveforms. We use our method to establish the valence and dynamics of navigation driven by optogenetic activation of different combinations of bitter-sensing gustatory neurons. Our method captures the dynamics of optogenetically induced behavior in compact, quantitative transformations that can be used to characterize circuits for sensorimotor processing and their contribution to navigational decision making. DOI: http://dx.doi.org/10.7554/eLife.06225.001Publication Electromagnetically induced transparency in paraffin-coated vapor cells(American Physical Society (APS), 2011) Klein, Mason; Hohensee; Phillips, David; Walsworth, RonaldAntirelaxation coatings in atomic vapor cells allow ground-state coherent spin states to survive many collisions with the cell walls. This reduction in the ground-state decoherence rate gives rise to ultranarrow-bandwidth features in electromagnetically induced transparency (EIT) spectra, which can form the basis of, for example, long-time scale slow and stored light, sensitive magnetometers, and precise frequency standards. Here we study, both experimentally and theoretically, how Zeeman EIT contrast and width in paraffin-coated rubidium vapor cells are determined by cell and laser-beam geometry, laser intensity, and atomic density. Using a picture of Ramsey pulse sequences, where atoms alternately spend “bright” and “dark” time intervals inside and outside the laser beam, we explain the behavior of EIT features in coated cells, highlighting their unique characteristics and potential applications.Publication Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons(Proceedings of the National Academy of Sciences, 2014) Luo, Linjiao; Cook, N.; Venkatachalam, Vivek; Martinez-Velazquez, L. A.; Zhang, Xiaosong; Calvo, A. C.; Hawk, J.; Macinnis, Bronwyn; Frank, Michelle; Ng, J. H. R.; Klein, Mason; Gershow, Marc; Hammarlund, M.; Goodman, M. B.; Colon-Ramos, D. A.; Zhang, Y.; Samuel, AraviThe nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (Ts) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above Ts (negative thermotaxis) and performs isothermal tracking near Ts. Under some conditions, the worm migrates up temperature gradients below Ts (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward Ts to study the role of specific neurons that have been proposed to be involved in thermotaxis using genetic ablation, behavioral tracking, and calcium imaging. We find differences in the strategies for positive and negative thermotaxis. Negative thermotaxis is achieved through biasing the frequency of reorientation maneuvers (turns and reversal turns) and biasing the direction of reorientation maneuvers toward colder temperatures. Positive thermotaxis, in contrast, biases only the direction of reorientation maneuvers toward warmer temperatures. We find that the AFD thermosensory neuron drives both positive and negative thermotaxis. The AIY interneuron, which is postsynaptic to AFD, may mediate the switch from negative to positive thermotaxis below Ts. We propose that multiple thermotactic behaviors, each defined by a distinct set of sensorimotor transformations, emanate from the AFD thermosensory neurons. AFD learns and stores the memory of preferred temperatures, detects temperature gradients, and drives the appropriate thermotactic behavior in each temperature regime by the flexible use of downstream circuits.Publication Sensory determinants of behavioral dynamics in Drosophila thermotaxis(Proceedings of the National Academy of Sciences, 2014) Klein, Mason; Afonso, Bruno; Vonner, Ashley James; Hernandez-Nunez, Luis; Berck, Matthew; Tabone, Christopher; Kane, Elizabeth; Pieribone, Vincent A.; Nitabach, Michael N.; Cardona, Albert; Zlatic, Marta; Sprecher, Simon G.; Gershow, Marc; Garrity, Paul A.; Samuel, AraviComplex animal behaviors are built from dynamical relationships between sensory inputs, neuronal activity, and motor outputs in patterns with strategic value. Connecting these patterns illuminates how nervous systems compute behavior. Here, we study Drosophila larva navigation up temperature gradients toward preferred temperatures (positive thermotaxis). By tracking the movements of animals responding to fixed spatial temperature gradients or random temperature fluctuations, we calculate the sensitivity and dynamics of the conversion of thermosensory inputs into motor responses. We discover three thermosensory neurons in each dorsal organ ganglion (DOG) that are required for positive thermotaxis. Random optogenetic stimulation of the DOG thermosensory neurons evokes behavioral patterns that mimic the response to temperature variations. In vivo calcium and voltage imaging reveals that the DOG thermosensory neurons exhibit activity patterns with sensitivity and dynamics matched to the behavioral response. Temporal processing of temperature variations carried out by the DOG thermosensory neurons emerges in distinct motor responses during thermotaxis.Publication Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila(eLife Sciences Publications, Ltd, 2016) Knecht, Zachary A; Silbering, Ana F; Ni, Lina; Klein, Mason; Budelli, Gonzalo; Bell, Rati; Abuin, Liliane; Ferrer, Anggie J; Samuel, Aravi; Benton, Richard; Garrity, Paul AIonotropic Receptors (IRs) are a large subfamily of variant ionotropic glutamate receptors present across Protostomia. While these receptors are most extensively studied for their roles in chemosensory detection, recent work has implicated two family members, IR21a and IR25a, in thermosensation in Drosophila. Here we characterize one of the most evolutionarily deeply conserved receptors, IR93a, and show that it is co-expressed and functions with IR21a and IR25a to mediate physiological and behavioral responses to cool temperatures. IR93a is also co-expressed with IR25a and a distinct receptor, IR40a, in a discrete population of sensory neurons in the sacculus, a multi-chambered pocket within the antenna. We demonstrate that this combination of receptors is required for neuronal responses to dry air and behavioral discrimination of humidity differences. Our results identify IR93a as a common component of molecularly and cellularly distinct IR pathways important for thermosensation and hygrosensation in insects. DOI: http://dx.doi.org/10.7554/eLife.17879.001Publication Variability in thermal and phototactic preferences in Drosophila may reflect an adaptive bet‐hedging strategy(John Wiley and Sons Inc., 2015) Kain, Jamey S.; Zhang, Sarah; Akhund‐Zade, Jamilla; Samuel, Aravi; Klein, Mason; de Bivort, BenjaminOrganisms use various strategies to cope with fluctuating environmental conditions. In diversified bet‐hedging, a single genotype exhibits phenotypic heterogeneity with the expectation that some individuals will survive transient selective pressures. To date, empirical evidence for bet‐hedging is scarce. Here, we observe that individual Drosophila melanogaster flies exhibit striking variation in light‐ and temperature‐preference behaviors. With a modeling approach that combines real world weather and climate data to simulate temperature preference‐dependent survival and reproduction, we find that a bet‐hedging strategy may underlie the observed interindividual behavioral diversity. Specifically, bet‐hedging outcompetes strategies in which individual thermal preferences are heritable. Animals employing bet‐hedging refrain from adapting to the coolness of spring with increased warm‐seeking that inevitably becomes counterproductive in the hot summer. This strategy is particularly valuable when mean seasonal temperatures are typical, or when there is considerable fluctuation in temperature within the season. The model predicts, and we experimentally verify, that the behaviors of individual flies are not heritable. Finally, we model the effects of historical weather data, climate change, and geographic seasonal variation on the optimal strategies underlying behavioral variation between individuals, characterizing the regimes in which bet‐hedging is advantageous.Publication The Ionotropic Receptors IR21a and IR25a mediate cool sensing in Drosophila(eLife Sciences Publications, Ltd, 2016) Ni, Lina; Klein, Mason; Svec, Kathryn V; Budelli, Gonzalo; Chang, Elaine C; Ferrer, Anggie J; Benton, Richard; Samuel, Aravi; Garrity, Paul AAnimals rely on highly sensitive thermoreceptors to seek out optimal temperatures, but the molecular mechanisms of thermosensing are not well understood. The Dorsal Organ Cool Cells (DOCCs) of the Drosophila larva are a set of exceptionally thermosensitive neurons critical for larval cool avoidance. Here, we show that DOCC cool-sensing is mediated by Ionotropic Receptors (IRs), a family of sensory receptors widely studied in invertebrate chemical sensing. We find that two IRs, IR21a and IR25a, are required to mediate DOCC responses to cooling and are required for cool avoidance behavior. Furthermore, we find that ectopic expression of IR21a can confer cool-responsiveness in an Ir25a-dependent manner, suggesting an instructive role for IR21a in thermosensing. Together, these data show that IR family receptors can function together to mediate thermosensation of exquisite sensitivity. DOI: http://dx.doi.org/10.7554/eLife.13254.001Publication Pan-neuronal imaging in roaming Caenorhabditis elegans(Proceedings of the National Academy of Sciences, 2015) Venkatachalam, Vivek; Ji, Ni; Wang, Xian-Ling; Clark, Christopher; Mitchell, James; Klein, Mason; Tabone, Christopher; Florman, Jeremy; Ji, Hongfei; Greenwood, Joel S.f.; Chisholm, Andrew; Srinivasan, Jagan; Alkema, Mark; Zhen, Mei; Samuel, AraviWe present an imaging system for pan-neuronal recording in crawling Caenorhabditis elegans. A spinning disk confocal microscope, modified for automated tracking of the C. elegans head ganglia, simultaneously records the activity and position of ∼80 neurons that coexpress cytoplasmic calcium indicator GCaMP6s and nuclear localized red fluorescent protein at 10 volumes per second. We developed a behavioral analysis algorithm that maps the movements of the head ganglia to the animal’s posture and locomotion. Image registration and analysis software automatically assigns an index to each nucleus and calculates the corresponding calcium signal. Neurons with highly stereotyped positions can be associated with unique indexes and subsequently identified using an atlas of the worm nervous system. To test our system, we analyzed the brainwide activity patterns of moving worms subjected to thermosensory inputs. We demonstrate that our setup is able to uncover representations of sensory input and motor output of individual neurons from brainwide dynamics. Our imaging setup and analysis pipeline should facilitate mapping circuits for sensory to motor transformation in transparent behaving animals such as C. elegans and Drosophila larva.Publication Bet-hedging, seasons and the evolution of behavioral diversity in Drosophila(2015) Kain, Jamey; Zhang, Sarah; Klein, Mason; Samuel, Aravi; de Bivort, BenjaminOrganisms use various strategies to cope with fluctuating environmental conditions. In diversified bet-hedging, a single genotype exhibits phenotypic heterogeneity with the expectation that some individuals will survive transient selective pressures. To date, empirical evidence for bet-hedging is scarce. Here, we observe that individual Drosophila melanogaster flies exhibit striking variation in light- and temperature-preference behaviors. With a modeling approach that combines real world weather and climate data to simulate temperature preference-dependent survival and reproduction, we find that a bet-hedging strategy may underlie the observed inter-individual behavioral diversity. Specifically, bet-hedging outcompetes strategies in which individual thermal preferences are heritable. Animals employing bet-hedging refrain from adapting to the coolness of spring with increased warm seeking that inevitably becomes counterproductive in the hot summer. This strategy is particularly valuable when mean seasonal temperatures are typical, or when there is considerable fluctuation in temperature within the season. The model predicts, and we experimentally verify, that the behaviors of individual flies are not heritable. Finally, we model the effects of historical weather data, climate change, and geographic seasonal variation on the optimal strategies underlying behavioral variation between individuals, characterizing the regimes in which bet-hedging is advantageous.Publication Sensorimotor structure of Drosophila larva phototaxis(Proceedings of the National Academy of Sciences, 2013) Kane, E. A.; Gershow, Marc; Afonso, Bruno; Larderet, I.; Klein, Mason; Carter, A. R.; de Bivort, Benjamin; Sprecher, S. G.; Samuel, AraviThe avoidance of light by fly larvae is a classic paradigm for sensorimotor behavior. Here, we use behavioral assays and video microscopy to quantify the sensorimotor structure of phototaxis using the Drosophila larva. Larval locomotion is composed of sequences of runs (periods of forward movement) that are interrupted by abrupt turns, during which the larva pauses and sweeps its head back and forth, probing local light information to determine the direction of the successive run. All phototactic responses are mediated by the same set of sensorimotor transformations that require temporal processing of sensory inputs. Through functional imaging and genetic inactivation of specific neurons downstream of the sensory periphery, we have begun to map these sensorimotor circuits into the larval central brain. We find that specific sensorimotor pathways that govern distinct light-evoked responses begin to segregate at the first relay after the photosensory neurons.