From the Cover: Echolocating bats rely on an innate speed-of-sound reference

Animals must encode fundamental physical relationships in their brains. A heron plunging its head underwater to skewer a fish must correct for light refraction, an archerfish shooting down an insect must “consider” gravity, and an echolocating bat that is attacking prey must account for the speed of sound in order to assess its distance. Do animals learn these relations or are they encoded innately and can they adjust them as adults are all open questions. We addressed this question by shifting the speed of sound and assessing the sensory behavior of a bat species that naturally experiences different speeds of sound. We found that both newborn pups and adults are unable to adjust to this shift, suggesting that the speed of sound is innately encoded in the bat brain. Moreover, our results suggest that bats encode the world in terms of time and do not translate time into distance. Our results shed light on the evolution of innate and flexible sensory perception.

Every organism must reliably sense its environment in order to survive and reproduce (1). Some sensory systems are innate and unalterable (2), allowing for efficient use even by naïve newborn animals (3–5). Others require learning or experience-dependent development—usually during a critical period during ontogeny (6, 7), though sometimes retained through adulthood (8), allowing for adapting sensing to changing environments (9, 10). The ability to accurately estimate distances with sub-centimeter accuracy is a hallmark of bat echolocation (11–13). Bats achieve this accuracy by means of delay-tuned neurons—neurons that are activated by specific call–echo time delays, supposedly encoding target distance (14–19), although it should be noted that some work suggests that the tuning width of delay-tuned neurons might not allow the accuracy that bats exhibit in delay perception (20). Though delay tuning has been shown to be (at least partially) innate at the neural level (21), this has never been tested behaviorally. Namely, when a newborn bat takes off for the first time, does its brain correctly translate time delays into distance?Translating time into distance relies on a reference of the speed of sound (SOS). This physical characteristic of the environment is not as stable as it may seem. The SOS may change considerably due to various environmental factors such as humidity, altitude, and temperature (22). Bats (Chiroptera) are a specious and widely distributed order of highly mobile and long-lived animals. They therefore experience a range of SOSs (with more than 5% variation, see below) between species, among species, and even within the life of a single individual. We therefore speculated that the reference of the SOS may not be innate to allow for the environmentally dependent SOS experienced by each animal.To test this, we examined the acquisition of the SOS reference by exposing neonatal bats to an increased SOS environment from birth (Materials and Methods). We reared two groups of bats from birth to independent flight in two flight chambers: six bats in normal air (henceforth: “air pups”) and five bats in a helium-enriched air environment (Heliox), where the speed of sound was 15% higher (henceforth: “Heliox pups”). Notably, Heliox pups were never active and did not echolocate in non-Heliox environment (Materials and Methods). This 15% shift is higher than the ecological range and was chosen because it is high enough to enable us to document behavioral changes but low enough so as to allow the bats to function (that is, to fly despite the change in air density). In order to feed, the bats had to fly to a target positioned 1.3 m away from their wooden slit roost. Once the bats learned to fly to the target independently (after ca. 9 wk), we first documented their echolocation in the environment where they were brought up, and we then moved them to the other treatment for testing (Materials and Methods). Because bats adjust their echolocation parameters to the distance of the target, before and during flight (23), we used their echolocation to assess the bats’ target range estimates. If the SOS reference is learned based on experience, the bats raised in Heliox should have learned a faster reference, so that when they flew in normal air, they would have perceived the target as farther than it really was. We also ran the same experiments on adult bats to test adult plasticity.