Are superficial neuromasts proprioceptors underlying fast copulatory behavior?

Autor: Martinez-Rivera N; Biological Imaging Group, Department of Pharmacology and Toxicology, The University of Kansas, Lawrence, KS, United States.; Biology Department, University of Puerto Rico-Rio Piedras, San Juan, Puerto Rico.; Puerto Rico Center for Environmental Neuroscience, Institute of Neurobiology, University of Puerto Rico-Medical Sciences, Old San Juan, Puerto Rico., Serrano-Velez JL; Biology Department, University of Puerto Rico-Rio Piedras, San Juan, Puerto Rico., Torres-Vazquez II; Biology Department, University of Puerto Rico-Rio Piedras, San Juan, Puerto Rico.; Bi-campus Neuroscience Graduate Program, The University of Kansas, Lawrence, KS, United States., Langerhans RB; Department of Biological Sciences, North Carolina State University, Raleigh, NC, United States., Rosa-Molinar E; Biological Imaging Group, Department of Pharmacology and Toxicology, The University of Kansas, Lawrence, KS, United States.; Biology Department, University of Puerto Rico-Rio Piedras, San Juan, Puerto Rico.; Puerto Rico Center for Environmental Neuroscience, Institute of Neurobiology, University of Puerto Rico-Medical Sciences, Old San Juan, Puerto Rico.; Bi-campus Neuroscience Graduate Program, The University of Kansas, Lawrence, KS, United States.
Jazyk: angličtina
Zdroj: Frontiers in neural circuits [Front Neural Circuits] 2022 Aug 23; Vol. 16, pp. 921568. Date of Electronic Publication: 2022 Aug 23 (Print Publication: 2022).
DOI: 10.3389/fncir.2022.921568
Abstrakt: In male Poeciliid fishes, the modified anal fin (i.e., gonopodium) and its axial and appendicular support are repositioned within the axial skeleton, creating a novel sexually dimorphic ano-urogenital region. During copulation, the relative location of the gonopodium is crucial for successful insemination. Therefore, the repositioning of these structures and organ relied on the reorganization of the efferent circuitry that controls spinal motor neurons innervating appendicular muscles critical for the movement of the gonopodium, including the fast and synchronous torque-trust motion during insemination attempts. Copulation occurs when a male positions himself largely outside a female's field of view, circumducts his gonopodium, and performs a rapid, complex maneuver to properly contact the female urogenital sinus with the distal tip of the gonopodium and transfers sperm. Although understanding of the efferent circuitry has significantly increased in the last 24 years, nothing is known about the cutaneous receptors involved in gonopodium movement, or how the afferent signals are processed to determine the location of this organ during copulation. Using Western mosquitofish, Gambusia affinis , as our model, we attempt to fill this gap in knowledge. Preliminary data showed cutaneous nerves and sensory neurons innervating superficial neuromasts surrounding the base of adult male gonopodium; those cutaneous nerves projected ventrally from the spinal cord through the 14th dorsal root ganglion and its corresponding ventral root towards the base and fin rays of the gonopodium. We asked what role the cutaneous superficial neuromasts play in controlling the positioning and timing of the gonopodium's fast and synchronous movements for effective sperm transfer. First, we found a greater number of superficial neuromasts surrounding the base of the male's gonopodium compared to the base of the female's anal fin. Second, we systemically removed superficial neuromasts surrounding the gonopodium base and observed significant impairment of the positioning and timing of gonopodial movements. Our findings provide a first step to supporting the following hypothesis: during radical reorganization of the Poeciliid body plan, superficial neuromasts have been partially co-opted as proprioceptors that allow the gonopodium to control precise positioning and timing during copulatory attempts.
Competing Interests: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
(Copyright © 2022 Martinez-Rivera, Serrano-Velez, Torres-Vazquez, Langerhans and Rosa-Molinar.)
Databáze: MEDLINE