Sensorimotor Integration in the Bat Echolocation System

HOME | PROJECTS                                                                by Melville Wohlgemuth
Hanging bats

    Sensorimotor transformations are fundamental to perceptually-guided behaviors in all animal systems, and yet a comprehensive understanding of the underlying mechanisms presents a major challenge in the field of neuroscience. With the goal of filling this gap, I am conducting a series of experiments on sensorimotor integration in the bat echolocation system, an animal whose stimulus environment and motor actions can be explicitly measured. My project involves recording neural activity from the midbrain superior colliculus (SC) of the echolocating bat as it produces sonar vocalizations and listens to echo returns from the environment. The SC is a laminated structure receiving superficial innervation from cortical and subcortical sensory structures, and containing premotor neurons in the deeper layers that play a role in directing orientation behaviors (May, 2006). It is hypothesized that sensorimotor integration for orientation occurs in both dorsal and ventral directions across the layers of the SC, with sensory information entering the superficial layers (Cyander et al, 1972; Goldberg and Wurtz, 1972) and motor information emanating from the deeper layers in the form of muscle commands and efference motor information (Dean et al, 1976; Marrocco et al, 1981; Huerta and Harting, 1982; Leigh et al, 1997; Meredith et al, 2001). My research on the neural mechanisms of sensorimotor integration exploits the active components of echolocation. Particularly valuable to my study is the bat’s ability to adaptively control the rate and duration of its sonar calls. Changes in these behavioral features can be accurately measured, providing a window into the bat’s ongoing perceptual experiences and processes.

    schematic

    Figure 1: Schematic of insect approach and capture in echolocating bats. a). The three phases of prey pursuit and capture: search, approach and terminal buzz. b). Spectrograms of representative sonar calls during each stage. Note the increase in call rate and decrease in call duration as the bat advances toward the insect.

Acoustic orientation by sonar allows the bat to search and capture insect prey in complete darkness. As a bat approaches an insect, it directs its sonar beam at the target by using information conveyed in the echoes (Ulanovsky and Moss, 2008). There are three distinct phases of insect pursuit and capture (Figure 1), and each phase is characterized by different temporal characteristics of sonar pulses (Surlykke and Moss, 2000). In the search phase, the bat emits long pulses at a rate of 5-10 Hz to scan the environment for insects (Fig.1, Search Phase). Once an insect has been selected, the bat switches to an approach phase that is distinguished by an increase in call rate and decrease in call duration, allowing the bat to sample the position of the target more frequently (Fig. 1, Approach Phase). In the final phase – the terminal buzz – the bat locks its sonar beam onto the target, and maximizes the rate of very short duration calls to accurately localize the position and velocity of the prey (Fig. 1, Buzz Phase). In each phase, the bat uses incoming auditory information to guide pre-motor commands for future vocalizations.

    Several lines of evidence suggest that the SC plays an important role in the sensorimotor integration necessary for species-specific orienting behaviors (Valentine and Moss, 1997; Valentine et al., 2002; Moss and Sinha, 2003). In visually guided primates (such as humans), the anatomy and physiology of the SC are dominated by vision (May, 2006). For bats, the principal method of exploration is echolocation: a behavior involving audition and vocalization (Moss and Sinha, 2003). Responses throughout the bat SC reflect this natural orienting behavior. Neurons in the intermediate layers of the bat SC primarily respond to auditory cues, including spatial location and echo delay (Valentine and Moss, 1997); while the deeper layers send efferents to areas controlling vocalizations (Sinha and Moss, 2007), pinna movements, and head direction (Valentine et al, 2002). Echolocation therefore involves a computation of stimulus location derived from auditory cues, followed by the production of vocalizations designed further inform the bat about stimulus position. How these auditory cues are processed into vocal premotor commands in the bat SC is the central question I am addressing in my research.

    I have chosen the big brown bat, Eptesicus fuscus, as the subject for empirical studies on echolocation and the SC. This bat species has been the subject of research on echolocation behavior and performance over the past 30 years, and data on spatial acuity, adaptive sonar call production during prey capture, and beam-directing behavior, lay a solid foundation for probing the neural mechanisms of sensorimotor transformations for spatial orientation in the SC (e.g. Simmons, 1973; 1979; Simmons et al., 1990a,b; Moss and Surlykke, 2001; Ghose and Moss, 2003; 2006; Ghose et al., 2006; Surlykke et al, 2009). Bat echolocation is unique due to its stroboscopic nature. Unlike other more continuous modalities such as vision or chemosensation, the brief and temporally discrete signals used by the big brown bat to sense the world define a precise window for correlating changes brain and behavior. In addition, the bat adapts its sonar calls in response to information extracted from echoes, providing a window into the bat’s perception through an analysis of changes in acoustic features with respect to changes in neural activity. Finally, the different phases of bat insect capture represent different behavioral states, which are predicted to recruit different populations of neurons which can be directly studied. These three aspects of bat echolocation will be utilized to collect empirical data in three experiments on sensorimotor integration in the superior colliculus:

    • Experiment 1: SC responses to echo returns from the bat’s own sonar calls.
    • Experiment 2: SC sensorimotor activity during sonar target tracking of single objects.
    • Experiment 3: SC sensorimotor activity during sonar target tracking of multiple objects.

    Experiment 1: SC responses to echo returns from the bat’s own sonar calls.

    Previous research on the auditory response properties of the bat SC have used artificially generated sonar sounds in the passively listening bat (Valentine and Moss, 1997). From this research, two classes of auditory neurons were identified, 2-D and 3-D. Spatial selectivity of 3-D neurons depends on the azimuth, elevation and distance (echo delay) of simulated sonar targets. It has been hypothesized that these neurons code the spatial location of sonar targets to guide behaviorally appropriate orienting behaviors. Although this research has demonstrated 3-D spatial response profiles in the bat SC, the behavioral relevance of these data are limited by the methods employed. In this study, I will use the bat’s own vocalizations to drive the system, placing the bat in a more naturalistic condition where it is engaged in the task, and biologically relevant auditory computations in the SC can be assayed.

    Experiment 2: SC sensorimotor activity during sonar target tracking of single objects.

    The auditory responses identified in the first experiment will be characterized with respect to motor outputs through this second experiment. Previous research has examined either the superficial layers or the deeper layers of the SC, but few recordings have been made of neural signals from several layers concurrently. Neural activity collected simultaneously from sensory and motor areas in the SC is necessary to generate an understanding of sensorimotor transformations across the structure. The data from this experiment will be informative about the contribution of sensory and motor encoding in each layer of the SC, and will also reveal how neural activity evolves from a sensory signal to a motor signal across the layers of the SC.

    Experiment 3: SC sensorimotor activity during sonar target tracking of multiple objects.

    Behavioral studies in the Moss laboratory on bat echolocation have identified differential control of the rate and duration of echolocation pulses. This result was demonstrated by placing distracting objects in the bat’s field of view as it echolocates an approaching food reward. It was found that call duration is determined by the closest object, irrespective of the objects reward value; whereas echolocation pulse rate was solely determined by the distance to the food reward. The bat is therefore tracking multiple objects in space, and this behavioral paradigm will be used to identify the role of the SC in the more naturalistic condition of multiple-target tracking. How the SC is involved in the tracking of multiple targets is not well understood. The results of the current experiment will generate new data on the effects of multiple objects on SC activity.

    Conclusions and Broader Impacts:

    The results of the three proposed experiments will generate new data on the process of sensorimotor integration for perceptually-guided behaviors. Although the proposal is focused on the bat echolocation system, the data generated by each experiment will contribute to a deeper and broader understanding of sensorimotor integration for spatial orientation. In particular, the results of the proposed experiments will be beneficial to research on auditory and visual guidance, as well as research on the design of artificial systems using sensorimotor integration (e.g., robotics and prosthetics). The data generated by the proposed experiments will also be used to develop computational models of sensorimotor integration. These data will be of particular value to modeling efforts, because they will include population level activity of sensory, motor and sensorimotor activity in the SC.

    BIBLIOGRAPHY

    • Cynader, M. Berman, N. 1972. Receptive field organization of monkey superior colliculus. Journal of Neurophysiology 35: 187-201.
    • Dean, P. Redgrave, P. Sahibzadad, N. Tsuji, K. 1986. Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19(2): 367-380.
    • Ghose, K. Horiuchi, TK. Krishnaprasad, PS. Moss, CF. 2006. Echolocating bats use a nearly time-optimal strategy to intercept prey. PLoS Biology 4(5): e108.
    • Ghose, K. Moss, CF. 2003. The sonar beam pattern of a flying bat as it tracks tethered insects. Journal of the Acoustical Society of America 114(2): 1120-1131.
    • Goldberg, ME, Wurtz, R H. 1972. Activity of superior colliculus cells in behaving monkey. I. Visual receptive fields of single cells. Journal of Neurophysiology 35: 542-559.
    • Huerta, MF. Harting, JK. 1982. Projections of the superior colliculus to the supraspinal nucleus and cervical spinal cord gray of the cat. Brain Research 242: 326-331.
    • Leigh, RJ. Rottach, KG. Das, VE. 1997. Transforming sensory perceptions in motor commands: evidence from programming of eye movements. Annals of the New York Academy of Sciences 835: 353-362.
    • Marrocco, RT. McClurkin, JW. Young, RA. 1981. Spatial properties of superior colliculus cells projection to the inferior pulvinar and parabigeminal nucleus of the monkey. Brain Research 222: 150-154.
    • May, PJ. 2006. The mammalian superior colliculus: laminar structure and connections. Progress in Brain Research 151: 321-378.
    • Meredith, MA. Miller, LK. Ramoa, AS. Clemo, HRH. Behan, M. 2001. Organizations of neurons of origin of the descending pathways from the ferret superior colliculus. Neuroscience Research 40: 301-313.
    • Moss, CF. Sinha, SR. 2003. Neurobiology of echolocating bats. Current Opinion in Neurobiology 13: 751-758.
    • Moss, CF. Surlykke, A. 2001. Auditory scence analysis by echolocating bats. Journal fo the Acoustic Society of America 110(4): 2201-2226.
    • Simmons, JA. 1973. The resolution of target range by echolocating bats. Journal of the Acoustic Society of America 54(1): 157-173.
    • Simmons, JA. 1979. Perception of echo phase information in bat sonar. Science 204(4399): 1336-1338.
    • Simmons, JA. Ferragamo, M. Moss, CF. Stevenson, SB. Altes, RA. 1990a. Discrimination of jittered echoes by the echolocating bat, Eptesicus fuscus: the shape of target images in echolocation. Journal of Comparative Physiology A 167(5): 589-616.
    • Simmons, JA. Moss, CF. Ferragamo, M. 1990b. Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus.
    • Sinha, SR. Moss, CF. 2007. Vocal premotor activity in the superior colliculus. Journal of Neuroscience 27(1): 98-110.
    • Surlykke, A. Ghose, K. Moss, CF. 2009. Acoustic scanning of natural scenes by echolocation in the big brown bat, Eptesicus fuscus. Journal of Experimental Biology 212(Pt. 7): 1011-1020.
    • Surlykke, A. Moss, CF. 2000. Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. Journal of Acoustical Society of America 108:2419 –2429.
    • Ulanovsky, N. Moss, CF. 2008. What the bat’s voice tells the bat’s brain. PNAS 105(25): 8491-8498.
    • Valentine, DE. Sinha, SR. Moss, CF. 2002. Orienting responses and vocalizations produced by microstimulation in the superior colliculus of the echolocating bat, Eptesicus fuscus. Journal of Comparative Physiology 188:89-108.
    • Valentine, DE. Moss, CF. 1997. Spatially selective auditory responses in the superior colliculus of the echolocating bat. Journal of Neuroscience 17(5): 1720-1733.