scholarly journals Daily rewiring of a neural circuit generates a predictive model of environmental light

2020 ◽  
Author(s):  
Bryan J. Song ◽  
Slater J. Sharp ◽  
Dragana Rogulja

Ongoing sensations are compared to internal, experience-based, reference models; mismatch between reality and expectation can signal opportunity or danger, and can shape behavior. The nature of internal reference models is largely unknown. We describe a model that enables moment-to-moment luminance evaluation in flies. Abrupt shifts to lighting conditions inconsistent with the subjective time-of-day trigger locomotion, whereas shifts to appropriate conditions induce quiescence. The time-of-day prediction is generated by a slowly shifting activity balance between opposing neuronal populations, LNvs and DN1as. The two populations undergo structural changes in axon length that accord with, and are required for, conveying time-of-day information. Each day, in each population, the circadian clock directs cellular remodeling such that the maximum axonal length in one population coincides with the minimum in the other; preventing remodeling prevents transitioning between opposing internal states. We propose that a dynamic predictive model resides in the shifting connectivities of the LNv- DN1a circuit.

2021 ◽  
Vol 7 (13) ◽  
pp. eabe4284
Author(s):  
Bryan J. Song ◽  
Slater J. Sharp ◽  
Dragana Rogulja

Behavioral responsiveness to external stimulation is shaped by context. We studied how sensory information can be contextualized, by examining light-evoked locomotor responsiveness ofDrosophilarelative to time of day. We found that light elicits an acute increase in locomotion (startle) that is modulated in a time-of-day–dependent manner: Startle is potentiated during the nighttime, when light is unexpected, but is suppressed during the daytime. The internal daytime-nighttime context is generated by two interconnected and functionally opposing populations of circadian neurons—LNvs generating the daytime state and DN1as generating the nighttime state. Switching between the two states requires daily remodeling of LNv and DN1a axons such that the maximum presynaptic area in one population coincides with the minimum in the other. We propose that a dynamic model of environmental light resides in the shifting connectivities of the LNv-DN1a circuit, which helps animals evaluate ongoing conditions and choose a behavioral response.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Anamika Sharma ◽  
Gaiti Hasan

Innate behaviours, although robust and hard wired, rely on modulation of neuronal circuits, for eliciting an appropriate response according to internal states and external cues. Drosophila flight is one such innate behaviour that is modulated by intracellular calcium release through inositol 1,4,5-trisphosphate receptors (IP3Rs). Cellular mechanism(s) by which IP3Rs modulate neuronal function for specific behaviours remain speculative, in vertebrates and invertebrates. To address this, we generated an inducible dominant negative form of the IP3R (IP3RDN). Flies with neuronal expression of IP3RDN exhibit flight deficits. Expression of IP3RDN helped identify key flight-modulating dopaminergic neurons with axonal projections in the mushroom body. Flies with attenuated IP3Rs in these presynaptic dopaminergic neurons exhibit shortened flight bouts and a disinterest in seeking food, accompanied by reduced excitability and dopamine release upon cholinergic stimulation. Our findings suggest that the same neural circuit modulates the drive for food search and for undertaking longer flight bouts.


2019 ◽  
Author(s):  
Kenya Tanaka ◽  
Ginga Shimakawa ◽  
Shuji Nakanishi

AbstractAs an adaptation to periodic fluctuations of environmental light, photosynthetic organisms have evolved a circadian clock. Control by the circadian clock of many cellular physiological functions, including antioxidant enzymes, metabolism and the cell cycle, has attracted attention in the context of oxidative stress tolerance. However, since each physiological function works in an integrated manner to deal with oxidative stress, whether or not cell responses to oxidative stress are under circadian control remains an open question. In fact, circadian rhythms of oxidative stress tolerance have not yet been experimentally demonstrated. In the present work, we applied an assay using methyl viologen (MV), which generates reactive oxygen species (ROS) under light irradiation, and experimentally verified the circadian rhythms of oxidative stress tolerance in photosynthetic cells of the cyanobacterium Synechococcus elongatus PCC7942, a standard model species for investigation of the circadian clock. Here, we report that ROS generated by MV treatment causes damage to stroma components and not to the photosynthetic electron transportation chain, leading to reduced cell viability. The degree of decrease in cell viability was dependent on the subjective time at which oxidative stress was applied. Thus, oxidative stress tolerance was shown to exhibit circadian rhythms. In addition, the rhythmic pattern of oxidative stress tolerance disappeared in mutant cells lacking the essential clock genes. Notably, ROS levels changed periodically, independent of the MV treatment. Thus, we demonstrate for the first time that in cyanobacterial cells, oxidative stress tolerance shows circadian oscillation.


2020 ◽  
Author(s):  
Giuseppe Barisano ◽  
Farshid Sepehrband ◽  
Nasim Sheikh-Bahaei ◽  
Meng Law ◽  
Arthur W. Toga

AbstractThe analysis of cerebral perivascular spaces (PVS) using magnetic resonance imaging (MRI) allows to explore in vivo their contributions to neurological disorders. To date the normal amount and distribution of PVS in healthy human brains are not known, thus hampering our ability to define with confidence pathogenic alterations. Furthermore, it is unclear which biological factors can influence the presence and size of PVS on MRI. We performed exploratory data analysis of PVS volume and distribution in a large population of healthy individuals (n = 897, age = 28.8 ± 3.7). Here we describe the global and regional amount of PVS in the white matter, which can be used as a reference for clinicians and researchers investigating PVS and may help the interpretation of the structural changes affecting PVS in pathological states. We found a relatively high inter-subject variability in the PVS amount in this population of healthy adults (range: 1.31-14.49 cm3). We then identified body mass index, time of day, and genetics as new elements significantly affecting PVS in vivo under physiological conditions, offering a valuable foundation to future studies aimed at understanding the physiology of perivascular flow.


2020 ◽  
pp. 0271678X2097285
Author(s):  
Giuseppe Barisano ◽  
Nasim Sheikh-Bahaei ◽  
Meng Law ◽  
Arthur W Toga ◽  
Farshid Sepehrband

The analysis of cerebral perivascular spaces (PVS) using magnetic resonance imaging (MRI) allows to explore in vivo their contributions to neurological disorders. To date the normal amount and distribution of PVS in healthy human brains are not known, thus hampering our ability to define with confidence pathogenic alterations. Furthermore, it is unclear which biological factors can influence the presence and size of PVS on MRI. We performed exploratory data analysis of PVS volume and distribution in a large population of healthy individuals (n = 897, age = 28.8 ± 3.7). Here we describe the global and regional amount of PVS in the white matter, which can be used as a reference for clinicians and researchers investigating PVS and may help the interpretation of the structural changes affecting PVS in pathological states. We found a relatively high inter-subject variability in the PVS amount in this population of healthy adults (range: 1.31–14.49 cm3). The PVS volume was higher in older and male individuals. Moreover, we identified body mass index, time of day, and genetics as new elements significantly affecting PVS in vivo under physiological conditions, offering a valuable foundation to future studies aimed at understanding the physiology of perivascular flow.


Endocrinology ◽  
2010 ◽  
Vol 152 (2) ◽  
pp. 595-606 ◽  
Author(s):  
Wilbur P. Williams ◽  
Stephan G. Jarjisian ◽  
Jens D. Mikkelsen ◽  
Lance J. Kriegsfeld

Abstract In spontaneously ovulating rodents, the preovulatory LH surge is initiated on the day of proestrus by a timed, stimulatory signal originating from the circadian clock in the suprachiasmatic nucleus (SCN). The present studies explored whether kisspeptin is part of the essential neural circuit linking the SCN to the GnRH system to stimulate ovulation in Syrian hamsters (Mesocricetus auratus). Kisspeptin neurons exhibit an estrogen-dependent, daily pattern of cellular activity consistent with a role in the circadian control of the LH surge. The SCN targets kisspeptin neurons via vasopressinergic (AVP), but not vasoactive intestinal polypeptide-ergic, projections. Because AVP administration can only stimulate the LH surge during a restricted time of day, we examined the possibility that the response to AVP is gated at the level of kisspeptin and/or GnRH neurons. Kisspeptin and GnRH activation were assessed after the administration of AVP during the morning (when AVP is incapable of initiating the LH surge) and the afternoon (when AVP injections stimulate the LH surge). Kisspeptin, but not GnRH, cellular activity was up-regulated after morning injections of AVP, suggesting that time-dependent sensitivity to SCN signaling is gated within GnRH but not kisspeptin neurons. In support of this possibility, we found that the GnRH system exhibits pronounced daily changes in sensitivity to kisspeptin stimulation, with maximal sensitivity in the afternoon. Together these studies reveal a novel mechanism of ovulatory control with interactions among the circadian system, kisspeptin signaling, and a GnRH gating mechanism of control.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Kristen Lee ◽  
Chris Q Doe

Individual neurons can undergo drastic structural changes, known as neuronal remodeling or structural plasticity. One example of this is in response to hormones, such as during puberty in mammals or metamorphosis in insects. However, in each of these examples it remains unclear whether the remodeled neuron resumes prior patterns of connectivity, and if so, whether the persistent circuits drive similar behaviors. Here, we utilize a well-characterized neural circuit in the Drosophila larva: the Moonwalking Descending Neuron (MDN) circuit. We previously showed that larval MDN induces backward crawling, and synapses onto the Pair1 interneuron to inhibit forward crawling (Carreira-Rosario et al., 2018). MDN is remodeled during metamorphosis and regulates backward walking in the adult fly. We investigated whether Pair1 is remodeled during metamorphosis and functions within the MDN circuit during adulthood. We assayed morphology and molecular markers to demonstrate that Pair1 is remodeled during metamorphosis and persists in the adult fly. MDN-Pair1 connectivity is lost during early pupal stages, when both neurons are severely pruned back, but connectivity is re-established at mid-pupal stages and persist into the adult. In the adult, optogenetic activation of Pair1 resulted in arrest of forward locomotion, similar to what is observed in larvae. Thus, the MDN-Pair1 neurons are an interneuronal circuit - a pair of synaptically connected interneurons – that is re-established during metamorphosis, yet generates similar locomotor behavior at both larval and adult stages.


2017 ◽  
Author(s):  
Stephan Gerhard ◽  
Ingrid Andrade ◽  
Richard D. Fetter ◽  
Albert Cardona ◽  
Casey M. Schneider-Mizell

AbstractThroughout an animal’s postembryonic development, neuronal circuits must maintain appropriate output even as the body grows. The contribution of structural adaptation — neuronal morphology and synaptic connectivity — to circuit development remains unclear. In a previous paper (Schneider-Mizell et al., 2016), we measured the detailed neuronal morphological structures subserving neuronal connectivity in Drosophila. Here, we examine how neuronal morphology and connectivity change across postembyronic development. Using new and existing serial section electron microscopy volumes, we reconstructed an identified nociceptive circuit in two larvae, one 1st instar and one 3rd instar. We found extremely consistent, topographically-arranged circuit structure. Five-fold increases in size of interneurons were associated with compensatory structural changes that maintained cell-type-specific synaptic input as a fraction of total inputs. An increase in number of synaptic contacts was accompanied with a disproportionate increase in the number of small dendritic terminal branches relative to other neuronal compartments. We propose that these precise patterns of structural growth act to conserve the computational function of a circuit, for example determining the location of a nociceptive stimulus.


2020 ◽  
Author(s):  
Anamika Sharma ◽  
Gaiti Hasan

AbstractInnate behaviours, though robust and hard wired, rely on modulation of neuronal circuits, for eliciting an appropriate response according to internal states and external cues. Drosophila flight is one such innate behaviour that is modulated by intracellular calcium release through inositol 1,4,5-trisphosphate receptors (IP3Rs). Cellular mechanism(s) by which IP3Rs modulate neuronal function for specific behaviours remain speculative, in vertebrates and invertebrates. To address this, we generated an inducible dominant negative form of the IP3R (IP3RDN). Flies with neuronal expression of IP3RDN exhibit flight deficits. Spatiotemporal expression of IP3RDN helped identify key flight-modulating dopaminergic neurons with axonal projections in the mushroom body. Attenuation of IP3R function in these presynaptic dopaminergic neurons resulted in flies with shortened flight bouts and a disinterest in seeking food, accompanied by reduced excitability and dopamine release upon cholinergic stimulation. Our findings suggest that the same neural circuit modulates the drive for food search and for undertaking longer flight bouts.


2019 ◽  
Vol 10 (1) ◽  
pp. 79-90
Author(s):  
Jeremiah R. Heise ◽  
Christopher K. Williams ◽  
Paul M. Castelli

Abstract The wintering period is often a limiting time for waterfowl. To understand the behavioral dynamics of Atlantic brant Branta bernicla hrota wintering along coastal New Jersey, USA, we conducted observations across the full 24-h diel period in an effort to construct an accurate time-budget model for the wintering population. In most behavioral studies, it is only possible to collect diurnal and crepuscular behavior data, forcing the assumption that these data are representative of nocturnal behavior in order to model the full 24-h diel period. We collected behavior data in 5,902 instantaneous observational scans across 4 time periods (morning crepuscular, diurnal, evening crepuscular, and nocturnal) from the third week in October to the third week in February 2009–2010 and 2010–2011. Brant primarily allocated time toward swimming (43.5%), feeding (26.4%), resting (15.4%), and flying (7.7%); these proportions differed significantly across times of day. Brant exhibited decreased flight (4.8% vs. 9.3%) and feeding (22.3% vs. 29.6%) and increased resting behavior (24.4% vs. 10.5%) nocturnally compared with diurnal periods. We further modeled explanatory environmental variables, hunting effects (open vs. closed seasons, locations open vs. closed to hunting), and time of day (diurnal and nocturnal only) on wintering behaviors. Feeding, resting, and swimming behavior presence were most influenced by a predictive model of (Hunt Season × Hunt Location × Period) + (Tide × Period). Flight behavior presence were most influenced by a predictive model of (Hunt Season × Hunt Location × Period) + (Tide × Temperature). There is an interactive effect of hunting pressure and period of day on observed activity; therefore, our results demonstrate that not accounting for nocturnal variation in behavior can lead to biases when extrapolating to energy expenditure models. Additionally, hunting areas proved to be nocturnally valuable because these areas contain valuable energy resources that may be unavailable diurnally, and our observations show that brant will shift their activities around hunting pressures to make use of these areas.


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