Sensorimotor processing of natural signals during adaptive motor planning

Melville Wohlgemuth

Abstract:

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. I am conducting both behavioral and neurophysiological studies of the echolocating bat to try and ascertain how sensory information is processed and used to drive adaptive changes in motor behaviors.

Research Summary:

We are interested in determining function of the midbrain superior colliculus (SC, or optic tectum in non-mammalian vertebrates), in processing sensory information into adaptive orienting behaviors. 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 of our research.

We chose 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. These aspects of bat echolocation will be utilized to collect empirical data in three experiments on sensorimotor integration in the superior colliculus:

1. SC responses to the bat’s own sonar calls.
2. Behavioral studies of adaptive sonar call design and echo reception.
3. SC sensorimotor activity during sonar target tracking of moving objects.

Experiment 1:

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 for 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 used the bat’s own vocalizations as a stimulus for the system, placing the bat in a more naturalistic condition and biologically relevant auditory computations in the SC can be assayed. Results of this study have shown that using a more naturally derived stimulus uncovers auditory response selectivity previously unknown for SC neurons. Furthermore, changes in response selectivity are correlated with the layer in which SC recordings were made: auditory responses from more superficial sensory layers demonstrate a high degree of selectivity, while deeper layer motor neurons respond to a wider variety of auditory stimuli. These results substantiate the functional roles of sensory and motor portions of the SC in terms of sensory processing and sensory signal assimilation, respectively. Furthermore, only by using a biologically inspired experimental approach was it possible to uncover these features of the SC, suggesting that future experiments should also be mindful of the relevance of the experimental methods to the life history of the animal model.

Publication: Wohlgemuth, MJ., and Moss, CF. (2016). Midbrain auditory selectivity to natural sounds. Proceedings of the National Academy of Sciences, 113(9): 2508-2513.

Experiment 2:

A large amount of research has focused upon the adaptive changes a bat makes to its sonar vocalizations as it tracks an insect, but an understanding of how the bat positions its head and ears to receive the cascade of reflect echoes is still unclear. In the current experiment, we have trained bats to rest on a platform and track a moving insect via echolocation. While the bat performs this task, recordings are made of the bat’s vocalizations as well as the 3D positions of its head and ears. Our analysis is then focused on how the bat changes ear and head position with respect to ongoing vocal behaviors, as well as the position, velocity, and acceleration of the insect being tracked. We have found that the bat does indeed adaptively modify the positions of the head and ears with respect to the location and movement of the target. These changes in body orientation allow the bat to modify both interaural differences between the ears, as well as the head-related transfer function of the pinna and tragus of the ear. Furthermore, the timing of these changes in head and ear position are correlated with different temporal aspects of the bat’s ongoing sonar vocal stream. The results of this study highlight how the bat modifies both the sensory signal (sonar vocalizations) and sensory reception to maximize the information gleaned from its environment.

We have also found that bats temporally organize the timing of successive vocalizations depending upon the sensory demands of the tracking task. In general, bats increase sonar pulse production rate as they approach a target. They also temporally isolate groups of sonar calls into sonar sound groups when the task is more demanding. Sonar sounds groups are defined as series of 2 or more calls produced at a shorter and more consistent interval as compared to surrounding calls. We have found that sonar sound group production increases in for increasing task complexity in bats hunting in the wild, hunting on the wing in the laboratory, and in our platform tracking task. These studies point to the benefits of altering the timing of sensory updates for different conditions.

Publication: Kothari, NB. Wohlgemuth, MJ. Hulgard, K. Surlykke, A. Moss, CF. 2014. Timing matters: sonar call groups facilitate target localization in bats. Frontiers in Physiology, 5.

Experiment 3:

The auditory responses identified in the first experiment will be characterized with respect to motor outputs through this third experiment. As in the second experiment, bats will be trained to rest on a platform and track a moving insect. While the bat performs this task, chronic neural recordings will be made in the SC. 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. Moreover, few studies of the SC have examined the sensory representation and motor coding for orienting in depth. This third dimension of depth is critically important for the bat when hunting and capturing insects on the wing, and through this experiment we can illuminate the process of how the SC codes for objects in depth.

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 experiments are 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 outlined 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.

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