Man has long envied the august lifestyle of the soaring bat. As our closest living relative with the ability to fly, the bat enjoys all the perks of placental mammal-hood (i.e. a pleasantly warm internal body temperature and the convenience of internal reproduction), without being confined to the wearisome two-dimensional reality of the common surface dweller.

Even other creatures of the sky have good reason to be jealous of bats. While bird and insect wings are built primarily of stiff, dead tissue (keratin and chitin, respectively), the bat wing is a flexible living membrane. The skin that makes up the bat wing, called the patagium, contains sensory neurons and muscles that finely control the shape, area and camber of the wing membrane. These features endow the bat with unsurpassed aerial maneuverability and panache.

As bats are the only flying creatures with wings made of skin, an interesting question is how peripheral sensory neurons in the bat's wing are specialized to sense mechanical forces during flight. A recent collaborative study from the laboratories of Ellen Lumpkin and Cynthia Moss, at Columbia University, USA, and the University of Maryland, USA, has investigated this question by describing the identity and organization of mechanoreceptor neurons that innervate the wing of the big brown bat, Eptesicus fuscus.

Kara Marshall and colleagues first used fluorescent dye-fill techniques to trace the axons of wing mechanoreceptor neurons back into the spinal cord. They were surprised to discover that many of these neurons arose from lower regions of the spinal cord, which do not typically innervate forelimbs in other mammals. In contrast, they found that wing motor neurons exhibited a similar organization to the mouse spinal cord. This means that some sections of the bat spinal cord contain sensory and motor neurons that innervate distinct regions of the body, a unique arrangement that could have interesting implications for central sensorimotor processing in the spinal cord and brain.

The team next examined the occurrence and distribution of sensory receptors on the bat wing. They identified many of the same mechanoreceptor neurons found in mouse and human hairy skin, with some important distinctions. For example, they discovered that hair follicles on the bat wing are often innervated by two distinct sensory neuron classes: lanceolate endings, which detect hair movement, and Merkel cells, which respond to sustained indentation of the skin. This arrangement may allow the bat to monitor airflow across the wing during flight, via the lanceolate endings, while maintaining the ability to sense and manipulate objects with the forelimbs, using Merkel cell complexes.

Finally, the authors measured the activity of single neurons in somatosensory cortex while they mechanically stimulated the wing. They found that cortical neurons typically responded to the onset of touch stimuli, whether brief air puffs or sustained poking, by firing sparse bursts of action potentials. These results are consistent with cortical recordings in other mammalian species, indicating that tactile signals from the bat wing may be encoded much like touch signals from the primate hand or rodent paw.

Overall, this study reveals that several of the basic components of mammalian somatosensation, in particular the peripheral mechanosensory neurons in the wing membrane, are uniquely specialized to empower the bat's flamboyant flight style. In parallel with recent advances in the genetic identification and targeting of mechanoreceptors in hairy skin of mice, studies in the bat can show how similar sensory structures may be specialized to serve widely divergent functions. Unlocking the secrets of the patagium may also help to allay the plague of bat envy that has infected humankind for generations.

References

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