Acuity of horizontal angle discrimination by the echolocating bat,Eptesicus fuscus

Differential-phase-sensitive neurons in the electrosensory lateral line lobe (ELL) of the African electric fish, Gymnarchus niloticus, are sensitive to time disparities on the order of microseconds between afferent action potentials. These action potentials fire in a phase-locked manner in response to the animal's own wave-type electric organ discharges (EODs) (Kawasaki and Guo, 1996). The time disparity is one of the essential cues for an electrical behavior, the jamming avoidance response (JAR). To gain an insight into the accurate temporal processing in the ELL, firing time accuracy and dynamic response properties of action potentials of the phaselocked neurons (PLNs) in the ELL were examined. The temporal accuracy of the entire neuronal circuit for the JAR was also measured using behavioral responses.Standard deviation of firing times of PLNs' action potentials was ϳ6 sec. The PLNs represent zerocrossing times of each stimulus cycle with this accuracy even when stimulus phase was modulated at high frequencies (ϳ50 Hz). Distinct JAR occurred when time disparity was diminished below 1 sec, and a marginal JAR could still be detected with a time disparity of 100 nsec. Standard deviation of the firing times of EODs was approximately several hundred nanoseconds. This stability of the EOD, however, was demonstrated to be unnecessary for the JAR. JARs occurred even when a large artificial jitter (ϳ60 sec) was introduced to a stimulus that mimicked fish's own EOD and the time disparity for JAR was diminished to 1 sec. This immunity of JAR to the EOD jitter is explained by the insensitivity of the differential-phase-sensitive neurons in the ELL to a common phase modulation.The JAR of the South American electric fish, Eigenmannia, also occurs in response to stimuli that generate comparably small phase differences (Rose and Heiligenberg, 1985b;Carr et al., 1986a). The present study revealed that the independently evolved Eigenmannia and Gymnarchus exhibit a comparative level of remarkable temporal accuracy.

Section: Temporal Sensitivity Expressed In the Jarmentioning

confidence: 74%

mentioning

confidence: 99%

Representation of Accurate Temporal Information in the Electrosensory System of the African Electric Fish,Gymnarchus niloticus

Guo

Kawasaki

1997

“…Binaural differences in arrival time, intensity, and spectrum of echoes encode the location of an object in azimuth and elevation (Lawrence and Simmons, 1982;Simmons et al, 1983;Pollak, 1988). The third dimension, the distance between the bat and a target, is determined from the time delay between the outgoing sound and the returning echo (Hartridge, 1945;Simmons, 1973).…”

Section: Abstract: Superior Colliculus; Echolocation; Bats; Acousticmentioning

confidence: 99%

Spatially Selective Auditory Responses in the Superior Colliculus of the Echolocating Bat

Valentine

Moss

1997

When a bat approaches a target, it continuously modifies its echolocation sounds and relies on incoming echo information to shape the characteristics of its subsequent sonar cries. In addition, acoustic information about the azimuth and elevation of a sonar target elicits orienting movements of the head and pinnae toward the sound source. This requires a common sensorimotor interface, where echo information is used to guide motor behaviors.Using single-unit neurophysiological methods and free-field auditory stimulation, we present data on biologically relevant specializations in the superior colliculus (SC) of the bat for orientation by sonar. In the bat's SC, two classes of spatially tuned neurons are distinguished by their sensitivity to echoes. One population shows facilitated, delay-tuned responses to pairs of sounds, simulating sonar emissions and echoes. Delay tuning, related to encoding target range, may play a role in guiding motor responses in echolocation, because the bat adjusts its emissions with changes in target distance. The delay-facilitated response depends on the direction of stimulation and on the temporal relationship between the simulated emission and echo in the sound pair, suggesting that this class of neurons represents the location of a target in three dimensions. A second population encodes the target in two dimensions, azimuth and elevation, and does not show a facilitated response to echoes delivered from any locus. Encoding of azimuth and elevation may be important for directing head aim, and this class may function in transforming auditory spatial information into signals used to guide acoustic orientation. Key words: superior colliculus; echolocation; bats; acoustic orientation; spatial perception; sensorimotor integrationThe midbrain superior colliculus (SC; optic tectum) of vertebrates is thought to play a role in spatial perception and in the translation of multisensory signals into commands for the control of quick (saccadic) orienting responses. In individual species, the organization of the SC reflects the importance of a particular sensory modality to an animal's goal-directed behavioral responses. By analogy with the role of the SC in the saccadic eye-movement system of primates (Sparks, 1986), in gaze-control orientation behavior in cat and barn owl (Knudsen, 1982;Middlebrooks and Knudsen, 1984;Du Lac and Knudsen, 1990;Munoz et al., 1991), and in prey-catching behavior in pit viper and frog (Hartline et al., 1978;Grobstein, 1988), the SC of the echolocating bat may play a role in integrating sensory and motor signals that drive this animal's acoustic orientation by sonar.The bat guides its flight and forages in darkness by emitting ultrasonic vocal signals and listening to the echoes returning to its ears from objects in space (Griffin, 1958;Moss and Schnitzler, 1995). Binaural differences in arrival time, intensity, and spectrum of echoes encode the location of an object in azimuth and elevation (Lawrence and Simmons, 1982;Simmons et al., 1983;Pollak, 1988). The third dim...

“…Similar results have been obtained in mammals. Simmons et al (1983) suggest that bats are able to resolve interaural time differences as small as 500 nsec. In addition to comparing binaural inputs, bats also compare an echolocating cry and its echo.…”

Section: Physiologymentioning

confidence: 99%

A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology

Carr¹,

Heiligenberg²,

Rose³

1986

141

Behavioral experiments show that the weakly electric fish, Eigenmannia, detects differences in timing as small as 400 nsec between electric signals from different parts of its body surface. The neural basis of this remarkable temporal resolution was investigated by recording from elements of the phase-coding system, a chain of electrotonically connected neurons devoted to the processing of temporal information. Each element of this system fires a single action potential for every cycle of the electric signal (either the fish's own electric organ discharge or a sinusoidal signal of similar frequency). For phase-coding primary afferents and midbrain neurons, the temporal resolution was determined by measuring each unit's capacity to lock its spike to a particular phase of the stimulus cycle. The jitter of a neuron's response (measured as the standard deviation of the timing of the spikes with respect to the stimulus) decreases from the level of the primary afferent (mean = 30 ctsec) to the midbrain torus (mean = 11 rsec); these results can be correlated with morphological measures of convergence. The temporal resolution of single neurons is still inferior to that displayed at the behavioral level.The detection of small temporal disparities between two signals is a process of general interest in sensory physiology, mediating localization of sound in the auditory system and providing an illusion of depth perception in vision (Pulfrich phenomenon). We employ a behavioral assay, the Jamming Avoidance Response (JAR), to demonstrate that the weakly electric fish, Eigenmannia, is able to detect temporal disparities of electrical signals as small as 400 nsec. In order to understand the origins of this sensitivity, we used intracellular recording techniques to identify the individual elements of the underlying neuronal circuit with respect to their response properties and morphology. In a subsequent study (Carr et al., in press), ultrastructural techniques have been used to reconstruct the midbrain circuit that performs these time comparisons.Eigenmannia is a South American gymnotiform fish which produces a high-frequency wave-type electric organ discharge. It uses this discharge both for electrolocation and for social communication. These fish possess a simple behavior, the JAR, whereby they shift the frequency of their electric organ discharge so as to avoid being jammed by a neighboring conspecific with a similar frequency (usually within +/-20 Hz; Bullock et al.,