Touching the sky

Bats are amongst the most agile of fliers – but can it really be their sense of touch which is key to this incredible ability? 

We use the sense of touch for the most mundane tasks and the most sublime. Touch provides guidance and finesse to our skilled movements, alerts us to obstacles or crawling insects on our skin, and act as a medium for intimate social bonding. Whether holding a fork or a hand, touch is essential to our daily functioning as humans.

Primates are the first animals that come to mind when conjuring up examples of exquisite tactile acuity and manual dexterity, but many other mammals are adapted for environments where primate hands would be useless. Perhaps the most dramatic example of this is the domain of bats: the sky.

Bats are the only mammals that are capable of powered flight. This remarkable skill has proven to be an effective survival mechanism: bats make up around 20% of all mammalian species. This is, in part, because flight provides access to food sources that are difficult to reach for other mammals, such as flying insects. Bats use echolocation to hunt, but mid-air agility is also critical to chase prey during flight. Bats have developed remarkable acrobatic flying skills to keep up with their quick-moving food source in the sky.

One key to bats’ flying agility is their flexible, multi-jointed wings. A thin skin membrane connects the elongated finger bones, the arm, and the leg into a continuous structure to form an airfoil. Unlike bird wings, bat wings have articulated finger bones. This makes the wings useful for serving double duty as airfoils and hands because they retain the ability to manipulate objects, climb and cradle their young.

Humans rely on input from touch receptors in the hand skin to adjust the shape of our grip or to increase grip strength when an object is slipping. Given that wings are partly just enlarged hands, our collaborators in the lab of Cynthia Moss at Johns Hopkins University asked whether bats use wing tactile input to adjust flight. Sparse microscopic hairs decorate wing skin, and hair deflection on rodents is known to convey tactile information. Thus, the first simple experiment performed to study this question used a substance more often seen in bathrooms than in laboratories: hair-removal cream.

When researchers applied the gentle depilation cream to the bats’ wings to remove hairs, they observed that their flight patterns changed: they made wider turns and flew faster¹. This was the first evidence that wing hair deflection from airflow provides information to guide flight. In this way, bats use tactile information to adjust their “grip” of the air.

How does the body detect the sense of touch in the first place? It all begins in the skin, our barrier to the outside world and a remarkable sensory organ. A rich array of neurons tile the skin and send signals to the brain about temperature, pain, pressure, vibration and hair movement. Even within the neuronal subtypes that sense tactile information there are diverse morphologies that perform different functions: some neurons wrap around hairs to detect hair movement, some terminate at the skin’s surface to detect gentle forces, and others are buried deep in the dermis to sense vibration. The shape of these receptors in the skin and the signals that they send to the brain are unique to the type of stimulus they detect. One reason certain body parts, like your lips and fingertips, are more sensitive than others is that the skin in these areas is densely packed with receptors. This allows us to surmise what areas of the skin are specialised for different functions based on what types of receptors are most prominent there.

[caption id="attachment_49683" align="aligncenter" width="450"] Bat sensory neurons.[/caption]

When we investigated bat wing skin, we found three types of touch receptors that are distributed across the wing in complimentary patterns². Merkel cells – important for detecting gentle touch – are concentrated in areas that are well suited for that purpose, like the thumb pad and fingertips. Hair receptors that detect hair deflection were most densely packed along the leading edge of the wing and the finger bones. This arrangement was particularly interesting because kinematic studies of flying insects and bats have revealed that a vortex of air at the wing’s leading edge is critical for maintaining lift during flight. Thus, we think hair receptors are ideally poised to provide information about airflow to the bat. Lastly, we found receptors that are similar to stretch receptors in other animals primarily located in the membrane between the fingers. This is the area of the wing that is stretched the most dramatically with each wing beat. This beautiful distribution of touch receptors revealed that the wing has areas of tactile specialisation. Interestingly, these receptor types are found in other mammals, but bats have co-opted them in a unique combination for novel use in flight.

The innervation of the body skin is exquisitely organised into discrete strips, each of which receives innervation from a single level of the spinal column. This organisation is carried through the central nervous system all the way to the brain, where the somatosensory cortex has a map of every body part. This map of the body in the brain is distorted, but is roughly organised by body location: a paradigm called somatotopy. Some studies of bat somatotopic maps have revealed that they are organised differently than most mammals: the wing, back, and stomach areas are mixed together. To understand why this could be the case, we studied the origin of wing innervation in bats. Most mammals do not have skin that connects the hand, arm and leg: how does the bat’s nervous system incorporate this unusual wing structure? We used fluorescent tracer dyes to trace the wing innervation back to the cell bodies of sensory neurons and motor neurons². In all mammals where forelimb innervation has been mapped, sensory neurons innervating the arm extended entirely from the adjacent spinal regions. In bats, we found an additional subset of neurons arising from much lower in the spinal column, in the region that would normally innervate the side or back.

This localisation of neurons was very surprising, but makes sense when one considers the unusual way that the wing forms. The flap of skin that connects the pinky finger to the bat’s body grows out from the trunk of the bat embryo to fuse with the arm, hand and leg. We hypothesise that this origin of the inner wing skin is the reason that it receives innervation from spinal areas in the mid-back. This unusual pattern of innervation could also explain the disordered somatotopic maps in bats that other researchers have described.

The final puzzle piece was to measure how the bat brain processes touch and airflow. Mohit Chadha and Susanne Sterbing-D’Angelo recorded responses to airflow and touch on the wing, and found that the brain encodes these stimuli with short, precisely timed bursts of activity². The responses to touch and airflow were indistinguishable, which indicates that the same pathways were transmitting both types of information. We think the brain’s fast firing could facilitate quick maneuvering if bats are using the information to adjust flight. This confirmed that the bat was incorporating tactile information from the wings in a way that could be important.

From these studies on bat touch we are just beginning to learn how tactile mechanisms could tune flight. The unusual architecture of the bat’s forelimb also provides an excellent system to study how the nervous system incorporates evolutionarily new body parts like wings. These studies set the stage for more complex questions: now that we understand the basic components of wing touch, we can begin asking how the information collected by the wing is integrated by the bat and used during flight.

In addition to answering biological questions, this work can inform the engineering of flying aircraft technologies. Nature has been solving the problem of flight for millions of years, whereas humans have only been tweaking our flying technology for about a century. We have plenty of catching up to do if we hope to build small flying aircraft as agile as insects or bats. Studying the ways that nature has solved these problems can give us ideas for improving our own technology. Hair receptors that might be using to detect airflow on wings could inspire similarly designed systems to detect airspeed on aircraft wings. This technology could replace or enhance current airspeed detectors – pitot tubes – which are prone to getting plugged and causing dangerous errors. Moreover, our anatomical observations of receptor density on the wing suggest specific locations on an airfoil that would be ideal for placing such sensors.

Human touch is well adapted for our purposes, but we can never underestimate the creative ways that the animal kingdom employs the same systems. We are only distantly related to bats, our fellow mammals, yet through engineering we seek to emulate their agility in the air. To get a handle on the biology of touch and flight, we can turn to these unusual specialists that grip the sky.

References:

1. Sterbing-D'Angelo, S., Chadha, M., Chiu, C., Falk, B., Xian, W., Barcelo, J., Zook, J. M. & Moss, C. F. 2011. Bat wing sensors support flight control. Proc Natl Acad Sci U S A, 108, 11291-6.
2.  Marshall, K. L., Chadha, M., De Souza, L. A., Sterbing-D'angelo, S. J., Moss, C. F. & Lumpkin, E. A. 2015. Somatosensory subrates of flight control in bats. Cell Reports, in press.

The author: 

Kara Marshall is finishing her PhD at Columbia University in the laboratory of Dr Ellen Lumpkin, where she studies mammalian touch receptors.