The evolution of whisker-mediated somatosensation in mammals: Sensory processing in barrelless S1 cortex of a marsupial, Monodelphis domestica.

Abstract

Movable tactile sensors in the form of whiskers are present in most mammals, but sensory coding in the cortical whisker representation has been studied almost exclusively in mice and rats. Many species that possess whiskers lack the modular "barrel" organization found in the primary somatosensory cortex (S1) of mice and rats, but it is unclear how whisker-related input is represented in these species. We used single-unit extracellular recording techniques to characterize receptive fields and response properties in S1 of Monodelphis domestica (short-tailed opossum), a nocturnal, terrestrial marsupial that shared its last common ancestor with placental mammals over 160 million years ago. Short-tailed opossums lack barrels and septa in S1 but show active whisking behavior similar to that of mice and rats. Most neurons in short-tailed opossum S1 exhibited multiwhisker receptive fields, including a single best whisker (BW) and lower magnitude responses to the deflection of surrounding whiskers. Mean tuning width was similar to that reported for mice and rats. Both symmetrical and asymmetrical receptive fields were present. Neurons tuned to ventral whiskers tended to show broad tuning along the rostrocaudal axis. Thus, despite the absence of barrels, most receptive field properties were similar to those reported for mice and rats. However, unlike those species, S1 neuronal responses to BW and surround whisker deflection showed comparable latencies in short-tailed opossums. This dissimilarity suggests that some aspects of barrel cortex function may not generalize to tactile processing across mammalian species and may be related to differences in the architecture of the whisker-to-cortex pathway. J. Comp. Neurol. 524:3587-3613, 2016. © 2016 Wiley Periodicals, Inc.