Influence of temperature on motor behaviors in newborn opossums (Monodelphis domestica): an in vitro study

Abstract

External thermosensation is crucial to regulate animal behavior and homeostasis, but the development of the mammalian thermosensory system is not well known. We investigated if temperature could play a role in the control of movements in a mammalian model born very immature, the opossum (Monodelphis domestica). Like other marsupials, at birth the opossum performs alternate and rhythmic movements with its forelimbs to reach a teat where it attaches in order to continue its development. It was shown that forelimb movements can be induced by mechanical stimulation of the snout in in vitro preparations of newborns consisting of the neuraxis with skin and forelimbs intact. In the present study, we used puff ejections of cold, neutral (bath temperature) and hot liquid directed towards the snout to induce forelimb responses in such preparations. Either the responses were visually observed under a microscope or triceps muscle activity was recorded. Cold liquid systematically induced forelimb movements and triceps contractions, but neutral and hot temperatures were less potent to do so. Sections of the trigeminal nerves and removal of the facial skin diminished responses to cold and nearly abolished those to hot and neutral stimulations. TRPM8 being the major cold receptor cation channel in adult mammals, we employed immunohistochemistry and RT-PCR to test for its expression, but found that it is not expressed before 13 postnatal days. Overall our results indicate that cold thermosensation exerts a strong influence on motor behaviors in newborn opossums.

Significance Statement External thermosensation is crucial for survival, but its development in mammals is not well understood, particularly at the systemic level. Herein, we tested if temperature perceived by the face influences motor behaviors in newborn opossums, a marsupial with a gestation period one week shorter than rodents of comparable size, thus offering access to early developmental stages. We found that cold temperatures systematically induced forelimb motor responses, but neutral and hot temperatures rarely did so. Moreover, in newborn opossums, cold thermosensation does not involve the major cold receptor in adult mammals, TRPM8. Cold avoidance may be important to sustain motor behaviors of newborn marsupials, when they must find a teat and attach to it in order to pursue their development.