Brainstem units of echolocating bats code binaural time differences in the microsecond range

Harnischfeger, G.

doi:10.1007/bf01153509

Cited by 25 publications

(4 citation statements)

References 13 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…In a 2-choice experiment, bats discriminate targets on the basis of echo time modulations as small as 500 nsec. Another bat, Molossus, with a well-developed medial superior olive, has brain stem units that code binaural time differences in the same range (500/6 change in firing rate over 15 psec) (Hamischfeger, 1980;Fig. 6 of Hamischfeger et al, 1985) as reported for the barn owl and Eigenmannia.…”

Section: Physiologymentioning

confidence: 89%

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

Carr¹,

Heiligenberg²,

Rose³

1986

J. Neurosci.

141

View full text Add to dashboard Cite

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.,

show abstract

Section: Physiologymentioning

confidence: 89%

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

Carr¹,

Heiligenberg²,

Rose³

1986

J. Neurosci.

141

View full text Add to dashboard Cite

show abstract

“…The degree of temporal precision is demonstrated by behavioral sensitivity to impressively small interaural time differences, within tens of microseconds (Harnischfeger, 1980;Moiseff and Konishi, 1981;Carr, 1993;Oertel, 1999). Through the first stages of neuronal sensory processing, spike time precision is improved with respect to the sound pressure waveform (Fukui et al, 2006).…”

Section: Introductionmentioning

confidence: 99%

Spike Encoding of Neurotransmitter Release Timing by Spiral Ganglion Neurons of the Cochlea

2012

View full text Add to dashboard Cite

Mammalian cochlear spiral ganglion neurons (SGNs) encode sound with microsecond precision. Spike triggering relies upon input from a single ribbon-type active zone of a presynaptic inner hair cell (IHC). Using patch-clamp recordings of rat SGN postsynaptic boutons innervating the modiolar face of IHCs from the cochlear apex, at room temperature, we studied how spike generation contributes to spike timing relative to synaptic input. SGNs were phasic, firing a single short-latency spike for sustained currents of sufficient onset slope. Almost every EPSP elicited a spike, but latency (300 -1500 s) varied with EPSP size and kinetics. When current-clamp stimuli approximated the mean physiological EPSC (Ϸ300 pA), several times larger than threshold current (rheobase, Ϸ50 pA), spikes were triggered rapidly (latency, Ϸ500 s) and precisely (SD, Ͻ50 s). This demonstrated the significance of strong synaptic input. However, increasing EPSC size beyond the physiological mean resulted in less-potent reduction of latency and jitter. Differences in EPSC charge and SGN baseline potential influenced spike timing less as EPSC onset slope and peak amplitude increased. Moreover, the effect of baseline potential on relative threshold was small due to compensatory shift of absolute threshold potential. Experimental first-spike latencies in response to a broad range of stimuli were predicted by a two-compartment exponential integrate-and-fire model, with latency prediction error of Ͻ100 s. In conclusion, the close anatomical coupling between a strong synapse and spike generator along with the phasic firing property lock SGN spikes to IHC exocytosis timing to generate the auditory temporal code with high fidelity.

show abstract

“…However, a recent study in our lab showed that in the (Harnischfeger, 1980). Apart from demonstrating that some mammalian neurons have the capacity to handle time differences in the microsecond range the study also indicates that fine time coding might be achieved with signals that would not appear to be optimal.…”

Section: Time-encoding In Echolocationmentioning

confidence: 94%

Ears adapted for the detection of motion, or how echolocating bats have exploited the capacities of the mammalian auditory system

Neuweiler

Bruns

Schuller

1980

The Journal of the Acoustical Society of America

View full text Add to dashboard Cite

Bats use the rich food resources of the night by specializing in audition. They emit short echolocation sounds and listen to the echoes returning from potential prey. The bat’s auditory system analyzes spectral and temporal parameters of echoes for detecting, locating, and identifying a target. Different bat species have solved the problem of acoustic target detection and pattern recognition even in clustered situations by focusing on certain acoustical features of a target. The specialized motion detection by horseshoe bats, for instance, analyzes small echofrequency shifts modulated onto a long constant frequency echolocation signal. These frequency modulations are Doppler shifts within echoes returning from wing beating insects. For detecting modulations as small as 10 Hz or 0.01%, horseshoe bats have in the cochlea an extremely narrow filter (Q?500) matched to the carrier frequency (i.e., echolocation sound) of 83 kHz. The filter is realized by structural differentiations of the basilar membrane and the filter frequencies are represented on the basilar membrane in an expanded fashion. We have called this specialized patch of the basilar membrane an ’’acoustical fovea.’’ The ’’foveal frequencies’’ are largely overrepresented in the tonopical arrangement of the ascending auditory pathway. The bats have developed a feedback system which lowers the emitted frequency during flight in such a way that the Doppler shifted echofrequency is kept precisely at a fixed reference frequency of the fovea. This feedback system and other neuronal data disclose an intricate coupling of the auditory and vocalizing system. The evolution of echolocation in bats has driven the analyzing capacities of audition in both frequency and time domain close to theoretical limits. Investigations of such specialized systems give fascinating insights into capacities and possible general principles of auditory information processing.

show abstract

Brainstem units of echolocating bats code binaural time differences in the microsecond range

Cited by 25 publications

References 13 publications

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

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

Spike Encoding of Neurotransmitter Release Timing by Spiral Ganglion Neurons of the Cochlea

Ears adapted for the detection of motion, or how echolocating bats have exploited the capacities of the mammalian auditory system

Contact Info

Product

Resources

About