Neural processing of target distance by echolocating bats: Functional roles of the auditory midbrain

Abstract

Using their biological sonar, bats estimate distance to avoid obstacles and capture moving prey. The primary distance cue is the delay between the bat's emitted echolocation pulse and the return of an echo. The mustached bat's auditory midbrain (inferior colliculus, IC) is crucial to the analysis of pulse–echo delay. IC neurons are selective for certain delays between frequency modulated (FM) elements of the pulse and echo. One role of the IC is to create these “delay-tuned”, “FM–FM” response properties through a series of spectro-temporal integrative interactions. A second major role of the midbrain is to project target distance information to many parts of the brain. Pathways through auditory thalamus undergo radical reorganization to create highly ordered maps of pulse–echo delay in auditory cortex, likely contributing to perceptual features of target distance analysis. FM–FM neurons in IC also project strongly to pre-motor centers including the pretectum and the pontine nuclei. These pathways may contribute to rapid adjustments in flight, body position, and sonar vocalizations that occur as a bat closes in on a target.

Introduction

The extraordinary ability of bats to analyze echoes from self-generated sounds allows them to orient through complex environments in complete darkness. In the case of aerial-hawking insectivorous bats, information obtained from echoes is also used to capture flying prey. A key piece of information obtained from echoes is the distance to a target, used by bats to create percepts that allow them to judge the distance and relative velocity of single targets (Simmons, 1971, Simmons, 1973, Simmons et al., 1979, Wenstrup and Suthers, 1984) and to distinguish and track multiple elements of a complex environment (Moss and Surlykke, 2010, Surlykke et al., 2009). Bats also use this information to adaptively adjust motor control of flight, body position, and sonar vocalizations (Chiu et al., 2009, Moss and Surlykke, 2001, Moss and Surlykke, 2010). For example, as an insectivorous bat searches for prey, it emits a sonar signal with long duration and narrow bandwidth that is well suited for target detection. As the bat begins to track and approach potential prey, it increases the repetition rate, decreases the duration, and progressively modifies the amount of frequency modulation (FM) in its sonar signals (Griffin, 1986, Jones and Holderied, 2007, Kalko and Schnitzler, 1993, Schnitzler and Kalko, 1998, Simmons et al., 1979, Surlykke and Moss, 2000). These active adjustments in the sonar signal that occur as the bat closes in on its prey create an optimal signal for localizing the position of the prey item in three dimensions (Jones and Holderied, 2007, Moss and Schnitzler, 1995, Simmons and Stein, 1980). It is likely that multiple brain circuits process and represent distance information within echoes to form the basis for these distance-based percepts and behaviors.

To determine target distance, echolocating bats use the time delay between their emitted sonar signal and the returning echo (Simmons, 1971, Simmons, 1973, Simmons et al., 1979). Downward FM sweeps, used in most bat echolocation signals, provide for very good estimates of pulse–echo delays (Simmons and Stein, 1980). These time delays are encoded within the central auditory system of echolocating bats by specialized neurons that respond only to a limited range of pulse–echo delays (Feng et al., 1978, O’Neill and Suga, 1979). These so-called delay-tuned neurons are sensitive to delays between the FM sweep in the emitted pulse and the returning FM sweep in the echoes. Populations of delay-tuned neurons presumably contribute to the bat's analysis of the distance to objects.

Delay-tuned neurons occur in auditory systems of many bat species (Pteronotus parnellii, O’Neill and Suga, 1979, Suga et al., 1979; Myotis lucifugus, Sullivan, 1982a, Sullivan, 1982b; Eptesicus fuscus, Dear et al., 1993, Feng et al., 1978), Rhinolophus rouxi, Schuller et al., 1988, Schuller et al., 1991b; Carollia perspicillata, Hagemann et al., 2010). In most of these species, the delay-tuned neurons respond to the same FM harmonic in the emitted pulse and the returning echo (Dear et al., 1993, Feng et al., 1978, Hagemann et al., 2010, Sullivan, 1982a). In the mustached bat (Pteronotus parnellii) however, delay-tuned neurons respond to different FM harmonics in the pulse and echo. The mustached bat emits a four-harmonic echolocation pulse that contains a long (20–30 ms) constant frequency (CF) portion followed by a short (2–3 ms) FM sweep (Henson et al., 1987, Novick and Vaisnys, 1964) (Fig. 1A). Delay-tuned neurons in this bat respond specifically to the delay between the FM component of the first harmonic (FM₁, 29–24 kHz) in the emitted pulse and one of the higher harmonic FM components (FM₂, 59–48 kHz; FM₃, 89–72 kHz; FM₄, 119–96 kHz) in the returning echo (O’Neill and Suga, 1982, Olsen and Suga, 1991b) (Fig. 1B and C). Collectively, the physiological response properties of these so-called FM–FM neurons and their underlying neural mechanisms have been well studied in the mustached bat, providing a good understanding of how the auditory system of bats has evolved so they can accurately and quickly determine the distance to a target. In this review we describe the neural mechanisms for target distance analyses in the mustached bat.

In particular, we focus on the functional role of the auditory midbrain in processing target distance information, as delay-tuned, FM–FM response properties emerge here (Marsh et al., 2006, Nataraj and Wenstrup, 2005, Portfors and Wenstrup, 2001b). Moreover, the mustached bat's inferior colliculus (IC, the main auditory midbrain nucleus) projects to multiple brain regions that may contribute to both perception of the distance of sonar targets and coordination of motor responses that depend on target distance (Frisina et al., 1989, Wenstrup and Grose, 1995, Wenstrup et al., 1994).