A VLSI Model of the Bat Dorsal Nucleus of the Lateral Lemniscus for Azimuthal Echolocation

Fu, Xiao Wen, Borys L. Brezden, and Shu Hui Wu. Hyperpolarization-activated inward current in neurons of the rat's dorsal nucleus of the lateral lemniscus in vitro. J. Neurophysiol. 78: 2235–2245, 1997. The hyperpolarization-activated current ( I h) underlying inward rectification in neurons of the rat's dorsal nucleus of the lateral lemniscus (DNLL) was investigated using whole cell patch-clamp techniques. Patch recordings were made from DNLL neurons of young rats (21–30 days old) in 400 μm tissue slices. Under current clamp, injection of negative current produced a graded hyperpolarization of the cell membrane, often with a gradual sag in the membrane potential toward the resting value. The rate and magnitude of the sag depended on the amount of hyperpolarizing current. Larger current resulted in a larger and faster decay of the voltage. Under voltage clamp, hyperpolarizing voltage steps elicited a slowly activating inward current that was presumably responsible for the sag observed in the voltage response to a steady hyperpolarizing current recorded under current clamp. Activation of the inward current ( I h) was voltage and time dependent. The current just was seen at a membrane potential of −70 mV and was activated fully at −140 mV. The voltage value of half-maximal activation of I h was −78.0 ± 6.0 (SE) mV. The rate of I h activation was best approximated by a single exponential function with a time constant that was voltage dependent, ranging from 276 ± 27 ms at −100 mV to 186 ± 11 ms at −140 mV. Reversal potential ( E h) of I h current was more positive than the resting potential. Raising the extracellular potassium concentration shifted E h to a more depolarized value, whereas lowering the extracellular sodium concentration shifted E h in a more negative direction. I h was sensitive to extracellular cesium but relatively insensitive to extracellular barium. The current amplitude near maximal-activation (about −140 mV) was reduced to 40% of control by 1 mM cesium but was reduced to only 71% of control by 2 mM barium. When the membrane potential was near the resting potential (about −60 mV), cesium had no effect on the membrane potential, current-evoked firing rate and input resistance but reduced the spontaneous firing. When the membrane potential was more negative than −70 mV, cesium hyperpolarized the cell, decreased current-evoked firing and increased the input resistance. I h in DNLL neurons does not contribute to the normal resting potential but may enhance the extent of excitation, thereby making the DNLL a consistently powerful inhibitory source to upper levels of the auditory system.

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The roles of GABAergic and glycinergic inhibition on binaural processing in the dorsal nucleus of the lateral lemniscus of the mustache bat

Journal of Neurophysiology ◽

10.1152/jn.1994.71.6.1999 ◽

1994 ◽

Vol 71 (6) ◽

pp. 1999-2013 ◽

Cited By ~ 55

Author(s):

L. Yang ◽

G. D. Pollak

Keyword(s):

Tone Burst ◽

Gabaergic Inhibition ◽

Gamma Aminobutyric Acid ◽

Lateral Lemniscus ◽

Dorsal Nucleus ◽

Iontophoretic Application ◽

Monaural Stimulation ◽

Contralateral Ear ◽

Glycinergic Inhibition ◽

Stimulation Of

1. We studied the monaural and binaural response properties of 99 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat before and during the iontophoretic application of antagonists that blocked gamma-aminobutyric acid-A (GABAA) receptors (bicuculline) or glycine receptors (strychnine). All cells were driven by monaural stimulation of the contralateral ear, whereas monaural stimulation of the ipsilateral ear never evoked discharges. The binaural properties of 81 neurons were determined by holding the intensity constant at the contralateral ear and presenting a variety of intensities to the ipsilateral ear. This procedure generated interaural intensity disparity (IID) functions and allowed us to determine the effect of ipsilaterally evoked inhibition on a constant excitatory drive evoked by the contralateral ear. 2. One of the main findings is that the IID functions in the majority of DNLL neurons were not affected by application of either strychnine or bicuculline. Blocking glycinergic inhibition with strychnine had no effect on the IID functions in 75% of the cells studied. However, strychnine did change the IID functions in approximately 25% of the DNLL population. In those cells glycinergic inhibition appeared to be partially, or, in a few cases, entirely responsible for the ipsilaterally evoked spike suppression. In contrast, blocking GABAergic inhibition with bicuculline had no discernible effect on the ipsilaterally evoked spike suppression in any of the excitatory/inhibitory cells that we recorded. GABAergic inhibition, therefore, plays no role in the formation of IID functions of neurons in the DNLL. Furthermore, the results suggest that glycinergic inhibition also does not contribute to the suppression of spikes evoked by stimulation of the contralateral ear in the vast majority of DNLL neurons. 3. Although the majority of IID functions were not influenced when either GABAergic or glycinergic innervation was blocked, ipsilateral stimulation alone evoked both a glycinergic and GABAergic inhibition in most DNLL cells. These inhibitory events were demonstrated in 18 other cells by evoking discharges with the iontophoretic application of glutamate. Stimulating the ipsilateral ear alone under these conditions caused a suppression of the glutamate-evoked discharges. Furthermore, the spike suppression persisted for a period of time that was longer than the duration of the tone burst at the ipsilateral ear. 4. The application of bicuculline or strychnine had different effects on the glutamate-elicited spikes. Bicuculline reduced the duration of the inhibition, and it was always the latter portion of the inhibition that was abolished by bicuculline. In more than half of the cells studied strychnine also reduced the duration of the inhibition.(ABSTRACT TRUNCATED AT 400 WORDS)

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Spectral Composition of Concurrent Noise Affects Neuronal Sensitivity to Interaural Time Differences of Tones in the Dorsal Nucleus of the Lateral Lemniscus

Journal of Neurophysiology ◽

10.1152/jn.00275.2007 ◽

2007 ◽

Vol 98 (5) ◽

pp. 2705-2715 ◽

Cited By ~ 5

Author(s):

Ida Siveke ◽

Christian Leibold ◽

Benedikt Grothe

Keyword(s):

White Noise ◽

Response Rate ◽

Spectral Composition ◽

Low Frequency ◽

Maximal Response ◽

Lateral Lemniscus ◽

Interaural Time Differences ◽

Binaural Cues ◽

Dorsal Nucleus ◽

Monaural Stimulation

We are regularly exposed to several concurrent sounds, producing a mixture of binaural cues. The neuronal mechanisms underlying the localization of concurrent sounds are not well understood. The major binaural cues for localizing low-frequency sounds in the horizontal plane are interaural time differences (ITDs). Auditory brain stem neurons encode ITDs by firing maximally in response to “favorable” ITDs and weakly or not at all in response to “unfavorable” ITDs. We recorded from ITD-sensitive neurons in the dorsal nucleus of the lateral lemniscus (DNLL) while presenting pure tones at different ITDs embedded in noise. We found that increasing levels of concurrent white noise suppressed the maximal response rate to tones with favorable ITDs and slightly enhanced the response rate to tones with unfavorable ITDs. Nevertheless, most of the neurons maintained ITD sensitivity to tones even for noise intensities equal to that of the tone. Using concurrent noise with a spectral composition in which the neuron's excitatory frequencies are omitted reduced the maximal response similar to that obtained with concurrent white noise. This finding indicates that the decrease of the maximal rate is mediated by suppressive cross-frequency interactions, which we also observed during monaural stimulation with additional white noise. In contrast, the enhancement of the firing rate to tones at unfavorable ITD might be due to early binaural interactions (e.g., at the level of the superior olive). A simple simulation corroborates this interpretation. Taken together, these findings suggest that the spectral composition of a concurrent sound strongly influences the spatial processing of ITD-sensitive DNLL neurons.

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Differential Response Properties to Amplitude Modulated Signals in the Dorsal Nucleus of the Lateral Lemniscus of the Mustache Bat and the Roles of GABAergic Inhibition

Journal of Neurophysiology ◽

10.1152/jn.1997.77.1.324 ◽

1997 ◽

Vol 77 (1) ◽

pp. 324-340 ◽

Cited By ~ 41

Author(s):

Lichuan Yang ◽

George D. Pollak

Keyword(s):

Phase Locking ◽

Modulation Frequency ◽

Tone Burst ◽

Differential Response ◽

Gabaergic Inhibition ◽

Lateral Lemniscus ◽

Response Properties ◽

Dorsal Nucleus ◽

Modulated Signals ◽

Onset Response

Yang, Lichuan and George D. Pollak. Differential response properties to amplitude modulated signals in the dorsal nucleus of the lateral lemniscus of the mustache bat and the roles of GABAergic inhibition. J. Neurophysiol. 77: 324–340, 1997. We studied the phase-locking of 89 neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the mustache bat to sinusoidally amplitude modulated (SAM) signals and the influence that GABAergic inhibition had on their response properties. Response properties were determined with tone bursts at each neuron's best frequency and then with a series of SAM signals that had modulation frequencies ranging from 50–100 to 800 Hz in 100-Hz steps. DNLL neurons were divided into two principal types: sustained neurons (55%), which responded throughout the duration of the tone burst, and onset neurons (45%), which responded only at the beginning of the tone burst. Sustained and onset neurons responded differently to SAM signals. Sustained neurons responded with phase-locked discharges to modulation frequencies ≤400–800 Hz. In contrast, 70% of the onset neurons phase-locked only to low modulation frequencies of 100–300 Hz, whereas 30% of the onset neurons did not phase-lock to any modulation frequency. Signal intensity differentially affected the phase-locking of sustained and onset neurons. Sustained neurons exhibited tight phase-locking only at low intensities, 10–30 dB above threshold. Onset neurons, in contrast, maintained strong phase-locking even at relatively high intensities. Blocking GABAergic inhibition with bicuculline had different effects on the phase-locking of sustained and onset neurons. In sustained neurons, there was an overall decline in phase-locking at all modulation frequencies. In contrast, 70% of the onset neurons phase-locked to much higher modulation frequencies than they did when inhibition was intact. The other 30% of onset neurons phase-locked to SAM signals, although they fired only with an onset response to the same signals before inhibition was blocked. In both cases, blocking GABAergic inhibition transformed their responses to SAM signals into patterns that were more like those of sustained neurons. We also propose mechanisms that could explain the differential effects of GABAergic inhibition on onset neurons that locked to low modulation frequencies and on onset neurons that did not lock to any SAM signals before inhibition was blocked. The key features of the proposed mechanisms are the absolute latencies and temporal synchrony of the excitatory and inhibitory inputs.

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The Role of the Dorsal Nucleus of the Lateral Lemniscus in Shaping the Auditory Response Properties of the Central Nucleus of the Inferior Collicular Neurons in the Albino Mouse

Neuroscience ◽

10.1016/j.neuroscience.2018.08.015 ◽

2018 ◽

Vol 390 ◽

pp. 30-45 ◽

Cited By ~ 1

Author(s):

Huimei Wang ◽

Shuang Shen ◽

Tihua Zheng ◽

Liyan Bi ◽

Bo Li ◽

...

Keyword(s):

Central Nucleus ◽

Lateral Lemniscus ◽

Response Properties ◽

Dorsal Nucleus ◽

Auditory Response ◽

Inferior Collicular

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Differing Roles of Inhibition in Hierarchical Processing of Species-Specific Calls in Auditory Brainstem Nuclei

Journal of Neurophysiology ◽

10.1152/jn.00688.2005 ◽

2005 ◽

Vol 94 (6) ◽

pp. 4019-4037 ◽

Cited By ~ 37

Author(s):

Ruili Xie ◽

John Meitzen ◽

George D. Pollak

Keyword(s):

Auditory Brainstem ◽

Lateral Lemniscus ◽

Response Properties ◽

Hierarchical Processing ◽

Tuning Curves ◽

Neuronal Populations ◽

Dorsal Nucleus ◽

Brainstem Nuclei ◽

Communication Calls ◽

Species Specific

Here we report on response properties and the roles of inhibition in three brain stem nuclei of Mexican-free tailed bats: the inferior colliculus (IC), the dorsal nucleus of the lateral lemniscus (DNLL) and the intermediate nucleus of the lateral lemniscus (INLL). In each nucleus, we documented the response properties evoked by both tonal and species-specific signals and evaluated the same features when inhibition was blocked. There are three main findings. First, DNLL cells have little or no surround inhibition and are unselective for communication calls, in that they responded to ∼97% of the calls that were presented. Second, most INLL neurons are characterized by wide tuning curves and are unselective for species-specific calls. The third finding is that the IC population is strikingly different from the neuronal populations in the INLL and DNLL. Where DNLL and INLL neurons are unselective and respond to most or all of the calls in the suite we presented, most IC cells are selective for calls and, on average, responded to ∼50% of the calls we presented. Additionally, the selectivity for calls in the majority of IC cells, as well as their tuning and other response properties, are strongly shaped by inhibitory innervation. Thus we show that inhibition plays only limited roles in the DNLL and INLL but dominates in the IC, where the various patterns of inhibition sculpt a wide variety of emergent response properties from the backdrop of more expansive and far less specific excitatory innervation.

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