Dataset Information

A circuit for detection of interaural time differences in the nucleus laminaris of turtles.

ABSTRACT: The physiological hearing range of turtles is approximately 50-1000?Hz, as determined by cochlear microphonics ( Wever and Vernon, 1956a). These low frequencies can constrain sound localization, particularly in red-eared slider turtles, which are freshwater turtles with small heads and isolated middle ears. To determine if these turtles were sensitive to interaural time differences (ITDs), we investigated the connections and physiology of their auditory brainstem nuclei. Tract tracing experiments showed that cranial nerve VIII bifurcated to terminate in the first-order nucleus magnocellularis (NM) and nucleus angularis (NA), and the NM projected bilaterally to the nucleus laminaris (NL). As the NL received inputs from each side, we developed an isolated head preparation to examine responses to binaural auditory stimulation. Magnocellularis and laminaris units responded to frequencies from 100 to 600?Hz, and phase-locked reliably to the auditory stimulus. Responses from the NL were binaural, and sensitive to ITD. Measures of characteristic delay revealed best ITDs around ±200??s, and NL neurons typically had characteristic phases close to 0, consistent with binaural excitation. Thus, turtles encode ITDs within their physiological range, and their auditory brainstem nuclei have similar connections and cell types to other reptiles.

SUBMITTER: Willis KL

PROVIDER: S-EPMC5702041 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

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A circuit for detection of interaural time differences in the nucleus laminaris of turtles.

Willis Katie L KL Carr Catherine E CE

The Journal of experimental biology 20170925 Pt 22

The physiological hearing range of turtles is approximately 50-1000 Hz, as determined by cochlear microphonics ( Wever and Vernon, 1956a). These low frequencies can constrain sound localization, particularly in red-eared slider turtles, which are freshwater turtles with small heads and isolated middle ears. To determine if these turtles were sensitive to interaural time differences (ITDs), we investigated the connections and physiology of their auditory brainstem nuclei. Tract tracing experiment ...[more]

PMID: 28947499

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Project description:For amplitude-modulated sound, the envelope interaural time difference (ITDENV) is a potential cue for sound-source location. ITDENV is encoded in the lateral superior olive (LSO) of the auditory brainstem, by excitatory-inhibitory (EI) neurons receiving ipsilateral excitation and contralateral inhibition. Between human listeners, sensitivity to ITDENV varies considerably, but ultimately decreases with increasing stimulus carrier frequency, and decreases more strongly with increasing modulation rate. Mechanisms underlying the variation in behavioral sensitivity remain unclear. Here, with increasing carrier frequency (4-10 kHz), as we phenomenologically model the associated decrease in ITDENV sensitivity using arbitrarily fewer neurons consistent across populations, we computationally model the variable sensitivity across human listeners and modulation rates (32-800 Hz) as the decreasing range of membrane frequency responses in LSO neurons. Transposed tones stimulate a bilateral auditory-periphery model, driving model EI neurons where electrical membrane impedance filters the frequency content of inputs driven by amplitude-modulated sound, evoking modulation filtering. Calculated from Fisher information in spike-rate functions of ITDENV, for model EI neuronal populations distinctly reflecting the LSO range in membrane frequency responses, just-noticeable differences in ITDENV collectively reproduce the largest variation in ITDENV sensitivity across human listeners. These slow to fast model populations each generally match the best human ITDENV sensitivity at a progressively higher modulation rate, by membrane-filtering and spike-generation properties producing realistically less than Poisson variance. Non-resonant model EI neurons are also sensitive to interaural intensity differences. With peripheral filters centered between carrier frequency and modulation sideband, fast resonant model EI neurons extend ITDENV sensitivity above 500-Hz modulation.

Project description:While motion is important for parsing a complex auditory scene into perceptual objects, how it is encoded in the auditory system is unclear. Perceptual studies suggest that the ability to identify the direction of motion is limited by the duration of the moving sound, yet we can detect changes in interaural differences at even shorter durations. To understand the source of these distinct temporal limits, we recorded from single units in the inferior colliculus (IC) of unanesthetized rabbits in response to noise stimuli containing a brief segment with linearly time-varying interaural time difference ("ITD sweep") temporally embedded in interaurally uncorrelated noise. We also tested the ability of human listeners to either detect the ITD sweeps or identify the motion direction. Using a point-process model to separate the contributions of stimulus dependence and spiking history to single-neuron responses, we found that the neurons respond primarily by following the instantaneous ITD rather than exhibiting true direction selectivity. Furthermore, using an optimal classifier to decode the single-neuron responses, we found that neural threshold durations of ITD sweeps for both direction identification and detection overlapped with human threshold durations even though the average response of the neurons could track the instantaneous ITD beyond psychophysical limits. Our results suggest that the IC does not explicitly encode motion direction, but internal neural noise may limit the speed at which we can identify the direction of motion.NEW & NOTEWORTHY Recognizing motion and identifying an object's trajectory are important for parsing a complex auditory scene, but how we do so is unclear. We show that neurons in the auditory midbrain do not exhibit direction selectivity as found in the visual system but instead follow the trajectory of the motion in their temporal firing patterns. Our results suggest that the inherent variability in neural firings may limit our ability to identify motion direction at short durations.

Dataset Information

A circuit for detection of interaural time differences in the nucleus laminaris of turtles.

Publications

A circuit for detection of interaural time differences in the nucleus laminaris of turtles.

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