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The nervous system coordinates a sequence of muscle movements to give rise to animal behaviors. In complex invertebrates or lab-studied vertebrates, due to the large number of cells in their nervous systems and the complexities of their behaviors, it is difficult to address how circuits process information to direct each motor output of the behavior. In this dissertation, I used the Caenorhabditis elegans male copulation behavior as a model to address how a compact circuit coordinates different behavioral programs. Insertion of a male copulatory organ into a suitable mate is a conserved and necessary behavioral step for most terrestrial mating. However, the detailed molecular and cellular mechanisms for this distinct social interaction have not been elucidated in any animal. During mating, the C. elegans male cloaca is positioned over the hermaphrodite’s vulva as he attempts to insert his copulatory spicules repetitively. Rhythmic spicule thrusts cease when insertion is sensed. Circuit components consisting of sensory/motor neurons and sex muscles for these steps have been previously identified, but it was unclear how their outputs are integrated to generate a coordinated behavior pattern. Here, I show that contraction of the male oblique muscles is required to sustain genital contact between the sexes. These muscles are innervated by the postcloacal sensilla (p.c.s.) sensory/motor neurons, which secret ACh to activate the levamisole-sensitive AChR and the ACR-16-containing ionotropic AChR on the oblique muscles. For spicules to rhythmically thrust during genital contact, activity of the oblique muscles and the gubernacular muscles is transmitted to the spicule protractor muscles instantaneously via gap junctions between these muscles and causes shallow protractor contractions. The rhythmic protractor contractions eventually switch to sustained contraction, as the SPC sensory-motor neurons integrate information of spicule position at the vulva with inputs from the hook and cloacal sensilla. The ERG-like K+ channel, UNC-103, which decreases the spicule circuit excitability, is likely to set a threshold requirement for integration of these inputs, so that sustained spicule muscle contraction is not stimulated by fewer inputs. In addition, I demonstrate that a cholinergic signaling pathway mediated by a muscarinic acetylcholine receptor, GAR-3, is used to enhance the ionotropic AChRs-mediated fast synaptic transmission in the copulation circuit. GAR-3 is expressed in multiple cells of the copulation circuit, but mainly in the cholinergic p.c.s. neurons and SPC neurons. Activation of GAR-3 is coupled to Gαq to trigger downstream signal transduction events that modulate neurotransmitter release from these neurons. Males with a loss-of-function allele of the gar-3 gene are defective in inserting their spicules into the hermaphrodite’s vulva efficiently. Since the p.c.s. neurons regulate the male’s contact with the hermaphrodite’s vulva, and the SPC neurons are required for spicule insertion during mating, GAR-3 probably facilitates male mating behavior via enhancing synaptic transmission from these neurons to their postsynaptic partners.

The nematode Caenorhabditis elegans, with its sequenced genome, compact nervous system and stereotyped behaviors is an ideal model organism in which to study the integration of sensory input with motor output. Male mating behavior is among the most complex of these behaviors and males utilize a number of sensory organs in its execution. Among these are the rays, which are nine pairs of sensory organs that are arranged laterally along the male tail. Each ray is composed of two ultra-structurally distinct neuron types, an A type and a B type, surrounded by a glia-like structural cell. Though compositionally identical, each pair of rays maintains a unique, genetically-hardwired identity based on wiring, morphology, and neurotransmitter fate. Three techniques were used to investigate the role of the rays in male mating behavior. First, cauterization of the tips of the rays removed their sensory endings, leading to ray neuron death. Second, a heterologous light-activated cation channel was utilized to activate specific ray neuron types. Finally, ray neuron types were genetically targeted to undergo apoptosis by expression of heterologous caspases. The results show that the rays play important roles in multiple steps of male mating behavior, including contact response, scanning, and turning. The rays as a whole mediate posture change and backing during contact response. The ability to respond to hermaphrodite contact is shared among the rays, as is initiation of backward locomotion, though all rays are required for efficient, prolonged backward scanning. Both A and B neuron types appear capable of initiating contact response. Direct activation of B neurons through ChR2 causes a contact response-like ventral tail flexure, and elimination of both A and B neurons reduces contact response. A neurons additionally have a unique role in turning.

付記する学位プログラム名: 霊長類学・ワイルドライフサイエンス・リーディング大学院 / 京都大学 / 新制・課程博士 / 博士(理学) / 甲第24876号 / 理博第4986号 / 新制||理||1712(附属図書館) / 京都大学大学院理学研究科生物科学専攻 / (主査)教授 平田 聡, 教授 三谷 曜子, 教授 松田 一希 / 学位規則第4条第1項該当 / Doctor of Science / Kyoto University / DGAM

京都大学 / 0048 / 新制・課程博士 / 博士(理学) / 甲第20556号 / 理博第4314号 / 新制||理||1619(附属図書館) / 京都大学大学院理学研究科生物科学専攻 / (主査)教授 古市 剛史, 教授 湯本 貴和, 教授 平井 啓久 / 学位規則第4条第1項該当 / Doctor of Science / Kyoto University / DGAM