James A. Simmons - US grants

This request for an ADAMHA Research Scientist Development Award is to support research on the mechanisms of spatial perception in the sonar of bats. The general aim is to determine the perceptual events which occur during the interception of flying insects by bats and to identify the role of neural spatial maps located in the auditory system for mediating aspects of perception of targets. Behavioral experiments will measure the accuracy with which bats track sonar targets with the aim of the head. They will exploit the bat's head-aim reaction as an index of target selection, echo signal-processing, and decision-making by the bat. Other experiments will measure the masking effect of one echo's presence on detection of another echo, as a means of directly studying the function of the neural map of range in the bat's auditory cortex. Physiological experiments will measure the accuracy of coding of echo delay in the auditory nerve and the display of target range in the auditory cortex to gather data for integration with behavioral data. Lesion experiments will determine the relative importance of auditory cortical maps of target range for tracking targets and for fine range resolution.

The goal of this research is to understand the mechanisms which the auditory system uses to determine the vertical direction of a sound source. These mechanisms are known in a general way to include an acoustic stage associated with the external ear as a receiving antenna for sound, auditory stages associated with the neural encoding of the waveform of sound and isolation of the specific acoustic dimensions carrying information about vertical direction, and a spatial perceptual stage associated with the transformation of neurally-encoded acoustic information into a specific neural representation of vertical direction itself. We presently lack an understanding of important aspects of each stage as well as how these stages are articulated together to form a working unit serving spatial auditory perception in mammals, including humans. This research is intended to develop a full description of the process of vertical localization in a mammal, taking advantage of the relative exaggeration of vertical- localizing capabilities in echolocating bats, which makes them ideal biological models for such experiments. Spatial perception may be mediated by neural mechanisms that undergo continuous recalibration through a kind of neural plasticity. Such a mechanisms associated with sound localization in a mammal may have clinical significance as an instance of plasticity in an adult, with implications for recovery of brain function after injury. The experiments will measure the directional information encoded by the external ear in sounds reaching the ear-drum, will determine the effects of manipulation of the external ear on the direction and accuracy of vertical localization, and will explore how vertical position is represented in the auditory nervous system.

The goals of the research are to determine the signal-processing capabilities of the real-time, three-dimensional acoustic imaging system in the big brown bat, Eptesicus fuscus, and how the bat uses sonar images to control interception of airborne targets. It will be determined if novel signal-processing or information- coding operations are employed during echolocation. A computational model will be developed and evaluated and improved based on behavioral and neurophysiological experiments designed to determine the properties of parallel time and frequency transforms that produce spatial images of targets. This research is important because the model will illustrate how to bring time- and frequency- domain information together to form images. This information could be used to advance the design of made-made systems for target tracking and target identification.

9622297 Simmons The general objective of the proposed research is to identify activity in the brain that causes perceptual images to have their particular content. The specific question is how specific numerical values for parameters of neural responses manifest themselves in corresponding numerical values for perceptual dimensions of images. This project uses target ranging in the biological sonar of the big brown bat, Eptesicus fuscus, as a "test-bed" for addressing questions about the formation and content of perceived images. Sonar and radar systems offer an especially well- developed body of theory about signal-processing and display of information that can be used to understand the mechanisms of biological systems evolved for the same purpose. Moreover, the exceptional real-time performance of biosonar systems in well-defined tasks of target localization, tracking, and classification make it obvious that there are technological advantages to understanding how echolocating animals achieve this performance. The starting point for the project is that bats have unusually good echo-delay accuracy of 10-15 ns and "two-point" echo-delay resolution of s. The initial problem is to account for this seemingly implausible performance with neural responses, which from physiological single-cell recording experiments appear to be 2-3 orders of magnitude less precise. New physiological experiments in the bat's midbrain and auditory cortex reveal that the "missing" high-precision temporal information is carried by the latencies of multi-cell neural responses using expanded time scales. There are two prominent competing hypotheses about neural substrates of perception which differ in the relative importance of response-rate and response-timing for determining image content. These hypotheses yield widely- divergent predictions from neural data for what bats should be able to perceive about target range. The combination of behavioral and physiological data from Ep tesicus leads to rejection of the hypothesis that relies exclusively on response-rate to represent information in images, while sustaining the hypothesis that response-timing may be "read out" directly into perception. The proposed research will examine these competing hypotheses in more detail because rejection of the response-rate model has widespread implications for neuroscience and for bioengineering, specifically for development of man-made systems that seek to emulate animal sonar performance. The proposed experiments will use 3-D video reconstructions of the bat's flight in sonar-guided interceptions to quantify how well the bat can locate and recognize targets in complex multiple- target sonar "scenes." New psychophysical experiments using electronically-simulated targets will measure the structure of the bat's sonar images to determine whether specific combinations of single and multiple overlapping echoes delivered from different directions lead to predicted echo- delay values appearing in the images. New physiological experiments will record and analyze the response in the bat's inferior colliculus that carry fine echo-delay information on expanded time scales to learn how these responses are combined to form images. A large-scale computational model of the bat's sonar will be used to evaluate experimental data in the context of emulating the bat's performance. ***

[unreadable] DESCRIPTION (provided by applicant): Echolocating big brown bats perceive sonar images that have distance, or target range, as their primary dimension. Distances to objects are determined from the delay of echoes, but the bat's images also depict the locations of reflecting points within each object as the basis for representing target shape. Echoes from parts of objects arrive so close together that that they overlap to form an interference spectrum, and the bat determines the separation of the target's parts from the frequencies of notches in this spectrum. However, the distance to each part of the object is depicted in the images by transforming the pattern of notches into true delay estimates. The objective of the proposed research is to understand how spectral information about the small time separations of echoes from different parts of the same object is bound with spike-timing information about the overall delay of echoes for the distance to the object as a whole. In the auditory cortex, this binding process is based on temporal coincidences between spikes representing overall delay independent of the echo spectrum and spikes representing the delay of echoes that have spectral notches, thus serving as a model for temporal feature binding as a general perceptual phenomenon. The project consists of behavioral experiments to measure the width of the bat's time windows for binding spectral delay estimates to temporal delay estimates and neuropsychological experiments to trace the movement of information about the echo spectrum from one delay to another using the same acoustic stimuli as in the behavioral experiments. A biologically realistic computational model of echo processing will be used as a tool for linking the behavioral and physiological findings. [unreadable] [unreadable]

This project examines how bats use sonar to perceive the location and shape of targeted objects, like prey, and simultaneously avoid interference caused by clutter, the echoes from untargeted objects. Bat sonar broadcasts are composed of a wide range of ultrasonic frequencies. Experiments reveal that small differences in the frequency content between broadcasts and their echoes have disproportionate effects on the perception of objects. The echoes from targets, located in front of a bat, contain all of the frequencies in the broadcast except for those few that are removed by the target itself and bats perceive both their shape and location. In contrast, bats perceive only the location, not the shape, of objects located to the side or farther away. More frequencies are removed from echoes that arrive from these locations. The bat's failure to perceive shape and, at the same time, perceive the location of untargeted objects allows the bat to avoid obstacles and orient to a target because the clutter itself disappears from the part of the perceived scene concerned with the identification of targets. This novel process is a defocusing method that deemphasizes background objects in the bat's images and it has technological significance for man-made sonar designs. Experiments using electronically-controlled echoes will determine the effects of removing or displacing selected frequencies on the perception of echo delay, used to determine target location, and the echo spectrum, used to determine target shape. Experiments with bats carrying a miniature radio microphone (Telemike) while they fly through a dense obstacle array composed of rows of chains hanging from the ceiling will determine whether bats make changes in the frequencies of successive sonar sounds to avoid interference caused by clutter. The broader impacts of this proposal include training of a postdoctoral fellow and a graduate student and the results of this study are likely to be incorporated into human-devised guidance devices.