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1.  Cooperative Integration and Representation Underlying Bilateral Network of Fly Motion-Sensitive Neurons 
PLoS ONE  2014;9(1):e85790.
How is binocular motion information integrated in the bilateral network of wide-field motion-sensitive neurons, called lobula plate tangential cells (LPTCs), in the visual system of flies? It is possible to construct an accurate model of this network because a complete picture of synaptic interactions has been experimentally identified. We investigated the cooperative behavior of the network of horizontal LPTCs underlying the integration of binocular motion information and the information representation in the bilateral LPTC network through numerical simulations on the network model. First, we qualitatively reproduced rotational motion-sensitive response of the H2 cell previously reported in vivo experiments and ascertained that it could be accounted for by the cooperative behavior of the bilateral network mainly via interhemispheric electrical coupling. We demonstrated that the response properties of single H1 and Hu cells, unlike H2 cells, are not influenced by motion stimuli in the contralateral visual hemi-field, but that the correlations between these cell activities are enhanced by the rotational motion stimulus. We next examined the whole population activity by performing principal component analysis (PCA) on the population activities of simulated LPTCs. We showed that the two orthogonal patterns of correlated population activities given by the first two principal components represent the rotational and translational motions, respectively, and similar to the H2 cell, rotational motion produces a stronger response in the network than does translational motion. Furthermore, we found that these population-coding properties are strongly influenced by the interhemispheric electrical coupling. Finally, to test the generality of our conclusions, we used a more simplified model and verified that the numerical results are not specific to the network model we constructed.
doi:10.1371/journal.pone.0085790
PMCID: PMC3900430  PMID: 24465711
2.  Selectivity and Plasticity in a Sound-Evoked Male-Male Interaction in Drosophila 
PLoS ONE  2013;8(9):e74289.
During courtship, many animals, including insects, birds, fish, and mammals, utilize acoustic signals to transmit information about species identity. Although auditory communication is crucial across phyla, the neuronal and physiologic processes are poorly understood. Sound-evoked chaining behavior, a display of homosexual courtship behavior in Drosophila males, has long been used as an excellent model for analyzing auditory behavior responses, outcomes of acoustic perception and higher-order brain functions. Here we developed a new method, termed ChaIN (Chain Index Numerator), in which we use a computer-based auto detection system for chaining behavior. The ChaIN system can systematically detect the chaining behavior induced by a series of modified courtship song playbacks. Two evolutionarily related Drosophila species, Drosophila melanogaster and Drosophila simulans, exhibited dramatic selective increases in chaining behavior when exposed to specific auditory cues, suggesting that auditory discrimination processes are involved in the acceleration of chaining behavior. Prolonged monotonous pulse sounds containing courtship song components also induced high intense chaining behavior. Interestingly, the chaining behavior was gradually suppressed over time when song playback continued. This behavioral change is likely to be a plastic behavior and not a simple sensory adaptation or fatigue, because the suppression was released by applying a different pulse pattern. This behavioral plasticity is not a form of habituation because different modality stimuli did not recover the behavioral suppression. Intriguingly, this plastic behavior partially depended on the cAMP signaling pathway controlled by the rutabaga adenylyl cyclase gene that is important for learning and memory. Taken together, this study demonstrates the selectivity and behavioral kinetics of the sound-induced interacting behavior of Drosophila males, and provides a basis for the systematic analysis of genes and neural circuits underlying complex acoustic behavior.
doi:10.1371/journal.pone.0074289
PMCID: PMC3782482  PMID: 24086330
3.  Mg2+ Block of Drosophila 
Neuron  2012;74(5):10.1016/j.neuron.2012.03.039.
SUMMARY
NMDA receptor (NMDAR) channels allow Ca2+ influx only during correlated activation of both pre- and postsynaptic cells; a Mg2+ block mechanism suppresses NMDAR activity when the postsynaptic cell is inactive. Although the importance of NMDARs in associative learning and long-term memory (LTM) formation has been demonstrated, the role of Mg2+ block in these processes remains unclear. Using transgenic flies expressing NMDARs defective for Mg2+ block, we found that Mg2+ block mutants are defective for LTM formation but not associative learning. We demonstrate that LTM-dependent increases in expression of synaptic genes, including homer, staufen, and activin, are abolished in flies expressing Mg2+ block defective NMDARs. Furthermore, we show that genetic and pharmacological reduction of Mg2+ block significantly increases expression of a CREB repressor isoform. Our results suggest that Mg2+ block of NMDARs functions to suppress basal expression of a CREB repressor, thus permitting CREB-dependent gene expression upon LTM induction.
doi:10.1016/j.neuron.2012.03.039
PMCID: PMC3651368  PMID: 22681692
4.  Lola regulates glutamate receptor expression at the Drosophila neuromuscular junction 
Biology Open  2012;1(4):362-375.
Summary
Communication between pre- and post-synaptic cells is a key process in the development and modulation of synapses. Reciprocal induction between pre- and postsynaptic cells involves regulation of gene transcription, yet the underlying genetic program remains largely unknown. To investigate how innervation-dependent gene expression in postsynaptic cells supports synaptic differentiation, we performed comparative microarray analysis of Drosophila muscles before and after innervation, and of prospero mutants, which show a delay in motor axon outgrowth. We identified 84 candidate genes that are potentially up- or downregulated in response to innervation. By systematic functional analysis, we found that one of the downregulated genes, longitudinals lacking (lola), which encodes a BTB-Zn-finger transcription factor, is required for proper expression of glutamate receptors. When the function of lola was knocked down in muscles by RNAi, the abundance of glutamate receptors (GluRs), GluRIIA, GluRIIB and GluRIII, as well as that of p-21 activated kinase (PAK), was greatly reduced at the neuromuscular junctions (NMJs). Recordings of the synaptic response revealed a decrease in postsynaptic quantal size, consistent with the reduction in GluR levels. Lola appears to regulate the expression of GluRs and PAK at the level of transcription, because the amount of mRNAs encoding these molecules was also reduced in the mutants. The transcriptional level of lola, in turn, is downregulated by increased neural activity. We propose that Lola coordinates expression of multiple postsynaptic components by transcriptional regulation.
doi:10.1242/bio.2012448
PMCID: PMC3509458  PMID: 23213426
Synapse formation; Transcriptional regulation; Neuromuscular junction; Drosophila; longitudinals lacking (lola); Glutamate receptor
5.  Differential Control of Presynaptic CamKII Activation and Translocation to Active Zones 
The release of neurotransmitters, neurotrophins and neuropeptides is modulated by Ca2+ mobilization from the endoplasmic reticulum (ER) and activation of Ca2+/calmodulin-dependent protein kinase II (CamKII). Furthermore, when neuronal cultures are subjected to prolonged depolarization, presynaptic CamKII redistributes from the cytoplasm to accumulate near active zones (AZs), a process that is reminiscent of CamKII translocation to the postsynaptic side of the synapse. However, it is not known how presynaptic CamKII activation and translocation depend on neuronal activity and ER Ca2+ release. Here these issues are addressed in Drosophila motoneuron terminals by imaging a fluorescent reporter of CamKII activity and subcellular distribution. We report that neuronal excitation acts with ER Ca2+ stores to induce CamKII activation and translocation to a subset of AZs. Surprisingly, activation is slow reflecting T286 autophosphorylation and the function of presynaptic ER ryanodine receptors (RyRs) and inositol trisphosphate receptors (IP3Rs). Furthermore, translocation is not simply proportional to CamKII activity, as T286 autophosphorylation promotes activation, but does not affect translocation. In contrast, RNAi-induced knockdown of the AZ scaffold protein Bruchpilot (BRP) disrupts CamKII translocation without affecting activation. Finally, RyRs comparably stimulate both activation and translocation, but IP3Rs preferentially promote translocation. Thus, Ca2+ provided by different presynaptic ER Ca2+ release channels is not equivalent. These results suggest that presynaptic CaMKII activation depends on autophosphorylation and global Ca2+ in the terminal, while translocation to AZs requires Ca2+ microdomains generated by IP3Rs.
doi:10.1523/JNEUROSCI.0550-11.2011
PMCID: PMC3123710  PMID: 21697360
6.  Crystal structures of Lymnaea stagnalis AChBP in complex with neonicotinoid insecticides imidacloprid and clothianidin 
Invertebrate Neuroscience   2008;8(2):71-81.
Neonicotinoid insecticides, which act on nicotinic acetylcholine receptors (nAChRs) in a variety of ways, have extremely low mammalian toxicity, yet the molecular basis of such actions is poorly understood. To elucidate the molecular basis for nAChR–neonicotinoid interactions, a surrogate protein, acetylcholine binding protein from Lymnaea stagnalis (Ls-AChBP) was crystallized in complex with neonicotinoid insecticides imidacloprid (IMI) or clothianidin (CTD). The crystal structures suggested that the guanidine moiety of IMI and CTD stacks with Tyr185, while the nitro group of IMI but not of CTD makes a hydrogen bond with Gln55. IMI showed higher binding affinity for Ls-AChBP than that of CTD, consistent with weaker CH–π interactions in the Ls-AChBP–CTD complex than in the Ls-AChBP–IMI complex and the lack of the nitro group-Gln55 hydrogen bond in CTD. Yet, the NH at position 1 of CTD makes a hydrogen bond with the backbone carbonyl of Trp143, offering an explanation for the diverse actions of neonicotinoids on nAChRs.
doi:10.1007/s10158-008-0069-3
PMCID: PMC2413115  PMID: 18338186
Acetylcholine binding protein (Lymnaea stagnalis); Crystal structures; Neonicotinoids; Nicotinic acetylcholine receptors; Ion channels

Results 1-6 (6)