scholarly journals A locomotor neural circuit persists and functions similarly in larvae and adult Drosophila

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.

2021 ◽  
Author(s):  
Kristen M. Lee ◽  
Chris Q. Doe

AbstractIndividual 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. In the adult, optogenetic activation of Pair1 resulted in arrest of forward locomotion, similar to what is observed in larvae. MDN and Pair1 are also synaptic partners in the adult, showing that the MDN-Pair1 interneuron circuit is retained in the adult following hormone-driven pupal remodeling. Thus, the MDN-Pair1 neurons are an interneuronal circuit – i.e. a pair of synaptically connected interneurons – that persists through metamorphosis, taking on new input/output neurons, yet generating similar locomotor behavior at both stages.


2020 ◽  
Author(s):  
Ivar S. Stein ◽  
Deborah K. Park ◽  
Nicole Claiborne ◽  
Karen Zito

SUMMARYExperience-dependent refinement of neuronal connections is critically important for brain development and learning. Here we show that ion flow-independent NMDAR signaling is required for the long-term dendritic spine growth that is a vital component of brain circuit plasticity. We found that inhibition of p38 MAPK, shown to be downstream of non-ionotropic NMDAR signaling in LTD and spine shrinkage, blocked LTP-induced spine growth but not LTP. We hypothesized that non-ionotropic NMDAR signaling drives the cytoskeletal changes that support bidirectional spine structural plasticity. Indeed, we found that key signaling components downstream of non-ionotropic NMDAR function in LTD-induced spine shrinkage also are necessary for LTP-induced spine growth. Furthermore, NMDAR conformational signaling with coincident Ca2+ influx is sufficient to drive CaMKII-dependent long-term spine growth, even when Ca2+ is artificially driven through voltage-gated Ca2+ channels. Our results support a model in which non-ionotropic NMDAR signaling gates the bidirectional spine structural changes vital for brain plasticity.


2017 ◽  
Vol 2017 ◽  
pp. 1-13 ◽  
Author(s):  
Yu Shu ◽  
Tonghui Xu

Chronic stress is associated with occurrence of many mental disorders. Previous studies have shown that dendrites and spines of pyramidal neurons of the prefrontal cortex undergo drastic reorganization following chronic stress experience. So the prefrontal cortex is believed to play a key role in response of neural system to chronic stress. However, how stress induces dynamic structural changes in neural circuit of prefrontal cortex remains unknown. In the present study, we examined the effects of chronic social defeat stress on dendritic spine structural plasticity in the mouse frontal association (FrA) cortexin vivousing two-photon microscopy. We found that chronic stress altered spine dynamics in FrA and increased the connectivity in FrA neural circuits. We also found that the changes in spine dynamics in FrA are correlated with the deficit of sucrose preference in defeated mice. Our findings suggest that chronic stress experience leads to adaptive change in neural circuits that may be important for encoding stress experience related memory and anhedonia.


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.


2016 ◽  
Author(s):  
Matthew C. W. Oswald ◽  
Paul S. Brooks ◽  
Maarten F. Zwart ◽  
Amrita Mukherjee ◽  
Ryan J. H. West ◽  
...  

AbstractNeurons are inherently plastic, adjusting their structure, connectivity and excitability in response to changes in activity. How neurons sense changes in their activity level and then transduce these to structural changes remains to be fully elucidated. Working with the Drosophila larval locomotor network, we show that neurons use reactive oxygen species (ROS), metabolic byproducts, to monitor their activity. ROS signals are both necessary and sufficient for activity-dependent structural adjustments of both pre- and postsynaptic terminals and for network output, as measured by larval crawling behavior. We find the highly conserved Parkinson’s disease-linked protein DJ-1ß acts as a redox sensor in neurons where it regulates pre- and postsynaptic structural plasticity, in part via modulation of the PTEN-PI3Kinase pathway. Neuronal ROS thus play an important physiological role as second messengers required for neuronal and network tuning, whose dysregulation in the ageing brain and under neurodegenerative conditions may contribute to synaptic dysfunction.


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.


Genetics ◽  
1995 ◽  
Vol 141 (3) ◽  
pp. 1163-1171 ◽  
Author(s):  
L H Rieseberg ◽  
C R Linder ◽  
G J Seiler

Abstract The sexual transfer of genes between taxa possessing different structural karyotypes must involve the passage of genes through a chromosomal sterility barrier. Yet little is known about the effects of structural differences on gene introgression within or adjacent to the rearranged chromosomal fragments or about the patterns of introgression in collinear regions. Here, we employ 197 mapped molecular markers to study the effects of chromosomal structural differences on introgression in backcrossed progeny of the domesticated sunflower, Helianthus annuus, and its karyotypically divergent wild relative, H. petiolaris. Forty percent of the genome from the seven collinear linkages introgressed, whereas only 2.4% of the genome from the 10 rearranged linkages was transferred. Thus, chromosomal rearrangements appear to provide an effective mechanism for reducing or eliminating introgression in rearranged chromosomal segments. On the other hand, observations that 60% of the markers from within the collinear portion of the genome did not introgress suggests that genic factors also resist introgression in Helianthus. That is, selection against H. petiolaris genes in concert with linkage may have reduced or eliminated parts of the genome not protected by structural changes. Thus, barriers to introgression in Helianthus appear to include both chromosomal structural and genic factors.


1997 ◽  
Vol 78 (6) ◽  
pp. 3047-3060 ◽  
Author(s):  
Miriam A. Ashley-Ross ◽  
George V. Lauder

Ashley-Ross, Miriam A. and George V. Lauder. Motor patterns and kinematics during backward walking in the Pacific Giant Salamander: evidence for novel motor output. J. Neurophysiol. 78: 3047–3060, 1997. Kinematic and motor patterns during forward and backward walking in the salamander Dicamptodon tenebrosus were compared to determine whether the differences seen in mammals also apply to a lower vertebrate with sprawling posture and to measure the flexibility of motor output by tetrapod central pattern generators. During treadmill locomotion, electromyograms (EMGs) were recorded from hindlimb muscles of Dicamptodon while simultaneous high-speed video records documented movement of the body, thigh, and crus and allowed EMGs to be synchronized to limb movements. In forward locomotion, the trunk was lifted above the treadmill surface. The pelvic girdle and trunk underwent smooth side-to-side oscillations throughout the stride. At the beginning of the stance phase, the femur was protracted and the knee joint extended. The knee joint initially flexed in early stance and then extended as the foot pushed off in late stance, reaching maximum extension just before foot lift-off. The femur retracted steadily throughout the stance. In the swing phase, the femur rapidly protracted, and the leg was brought forward in an “overhand crawl” motion. In backward walking, the body frequently remained in contact with the treadmill surface. The pelvic girdle, trunk, and femur remained relatively still during stance phase, and most motion occurred at the knee joint. The knee joint extended throughout most of stance, as the body moved back, away from the stationary foot. The knee flexed during swing. Four of five angles showed significantly smaller ranges in backward than in forward walking. EMGs of forward walking showed that ventral muscles were coactive, beginning activity just before foot touchdown and ceasing during the middle of stance phase. Dorsal muscles were active primarily during swing. Backward locomotion showed a different pattern; all muscles except one showed primary activity during the swing phase. This pattern of muscle synergy in backward walking never was seen in forward locomotion. Also, several muscles demonstrated lower burst rectified integrated areas (RIA) or durations during backward locomotion. Multivariate statistical analysis of EMG onset and RIA completely separated forward and backward walking along the first principal component, based on higher RIAs, longer durations of muscle activity, and greater synergy between ventral muscles during early stance in forward walking. Backward walking in Dicamptodon uses a novel motor pattern not seen during forward walking in salamanders or during any other locomotor activity in previously studied tetrapods. The central neuronal mechanisms mediating locomotion in this primitive tetrapod are thus capable of considerable plasticity.


1997 ◽  
Vol 136 (3) ◽  
pp. 679-692 ◽  
Author(s):  
Pico Caroni ◽  
Ludwig Aigner ◽  
Corinna Schneider

Long-term functional plasticity in the nervous system can involve structural changes in terminal arborization and synaptic connections. To determine whether the differential expression of intrinsic neuronal determinants affects structural plasticity, we produced and analyzed transgenic mice overexpressing the cytosolic proteins cortical cytoskeleton–associated protein 23 (CAP-23) and growth-associated protein 43 (GAP-43) in adult neurons. Like GAP-43, CAP-23 was downregulated in mouse motor nerves and neuromuscular junctions during the second postnatal week and reexpressed during regeneration. In transgenic mice, the expression of either protein in adult motoneurons induced spontaneous and greatly potentiated stimulus-induced nerve sprouting at the neuromuscular junction. This sprouting had transgene-specific features, with CAP-23 inducing longer, but less numerous sprouts than GAP-43. Crossing of the transgenic mice led to dramatic potentiation of the sprout-inducing activities of GAP-43 and CAP-23, indicating that these related proteins have complementary and synergistic activities. In addition to ultraterminal sprouting, substantial growth of synaptic structures was induced. Experiments with pre- and postsynaptic toxins revealed that in the presence of GAP-43 or CAP-23, sprouting was stimulated by a mechanism that responds to reduced transmitter release and may be independent of postsynaptic activation. These results demonstrate the importance of intrinsic determinants in structural plasticity and provide an experimental approach to study its role in nervous system function.


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