Focal electrical stimulation of dorsal nucleus of the lateral lemniscus modulates auditory response properties of inferior collicular neurons in the albino mouse

1. We examined the physiological properties of neurons in the dorsal nucleus of the lateral lemniscus (DNLL) of the rat in a 400-microns tissue slice taken in the frontal plane through the auditory midbrain. The brain slice was placed in a small chamber and was perfused fully submerged in a warm, continuously circulating oxygenated saline solution. We made intracellular recordings with glass pipettes filled with 4 M potassium acetate. Synaptic potentials were evoked by electrical stimulation of either the lateral lemniscus or the commissure of Probst. 2. We tested the membrane characteristics of DNLL neurons by recording the electrical potentials produced by intracellular injection of positive or negative current. Typically, DNLL neurons had nearly linear current-voltage curves and responded to depolarizing currents with a sustained train of action potentials. Injection of intense or prolonged depolarizing currents frequently resulted in a pronounced afterhyperpolarization of the cell membrane. Intense hyperpolarizing currents were often followed by a large rebound depolarization. 3. The action potentials of most DNLL neurons were characterized by a double undershoot, i.e., the initial hyperpolarization after a spike was followed by a second, longer-latency hyperpolarization. Seventy-nine percent of the cells recorded had this type of double undershoot. The remaining cells had a single undershoot in which the postspike hyperpolarization was followed by a steady return to resting potential without any indication of a second phase of hyperpolarization. 4. Electrical stimulation of the lateral lemniscus evoked both excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs) in DNLL. The EPSPs were evoked alone without any evidence of an IPSP in 67% of neurons and IPSPs were evoked alone in 6% of the neurons from which recordings were made. In 27% of the recordings both EPSPs and IPSPs were elicited in the same neuron by stimulation of a single location on the lateral lemniscus. 5. The combined EPSPs and IPSPs produced by lemniscal stimulation could often be dissociated by their different thresholds and/or different response latencies. For 35% of the neurons in which both an EPSP and IPSP were present, the IPSP had a lower threshold; for 23% of the cells, the EPSP had a lower threshold. For the remaining cells the thresholds for producing an EPSP and IPSP were the same. 6. DNLL neurons were capable of responding with great fidelity to a single pulse of stimulation delivered to the lateral lemniscus, i.e., an action potential was evoked after every stimulus.(ABSTRACT TRUNCATED AT 400 WORDS)

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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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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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Azimuthal receptive fields are shaped by GABAergic inhibition in the inferior colliculus of the mustache bat

Journal of Neurophysiology ◽

10.1152/jn.1994.72.3.1080 ◽

1994 ◽

Vol 72 (3) ◽

pp. 1080-1102 ◽

Cited By ~ 53

Author(s):

T. J. Park ◽

G. D. Pollak

Keyword(s):

Inferior Colliculus ◽

Action Potentials ◽

Receptive Fields ◽

Sound Field ◽

Glass Electrode ◽

Gabaergic Inhibition ◽

Gamma Aminobutyric Acid ◽

Response Properties ◽

Inferior Collicular ◽

Stimulation Of

1. In this study we examine the effects of GABAergic inhibition on the response properties and the constructed azimuthal receptive fields of 54 excitatory/inhibitory (EI) neurons tuned to 60 kHz in the inferior colliculus of the mustache bat. The constructed azimuthal receptive fields predict the spike counts that would be evoked by different intensities of 60-kHz sounds presented from each of 13 azimuthal locations in the frontal sound field. 2. Action potentials were recorded with a micropipette attached to a multibarrel glass electrode. Bicuculline, an antagonist specific for gamma-aminobutyric acid-A (GABAA) receptors, was iontophoretically applied through the multibarrel electrode. Both monaural and binaural response properties were initially recorded at a variety of interaural intensity disparities (IIDs) and absolute intensities, and the same response properties were subsequently assessed while GABAergic inhibition was blocked by bicuculline. Azimuthal receptive fields both before and during the application of bicuculline were constructed from response properties obtained with earphones after correcting for the directional properties of the ear and the IIDs generated by 60-kHz sounds presented from a variety of azimuthal locations. 3. Bicuculline had virtually no effect on either the monaural or binaural properties of 19 cells (35%). The constructed azimuthal receptive fields of these cells were also unaffected by bicuculline. Presumably the properties of these cells were formed in a lower nucleus, most likely the contralateral lateral superior olive (LSO), and were imposed on the collicular cell via the crossed projection from the LSO to the inferior colliculus, which is known to be excitatory. 4. In more than half of the neurons (65%) GABAergic inhibition influenced one or more features of the cell's response properties and thus its azimuthal receptive field. Some response properties were formed in the colliculus through GABAergic inhibition, whereas others appear to have been shaped initially in a lower nucleus and then further modified by GABAergic inhibition in the inferior colliculus. Moreover, a number of features of GABAergic inhibition that acted on inferior collicular cells were evoked by stimulation of the contralateral (excitatory) ear, whereas other features were influenced by stimulation of the ipsilateral (inhibitory) ear. 5. In 20 cells (37%) blocking GABAergic inhibition reduced or abolished the inhibition evoked by the ipsilateral ear. The receptive fields of cells in which the ipsilaterally evoked inhibition was reduced by bicuculline expanded further into the ipsilateral sound field than they did before bicuculline.(ABSTRACT TRUNCATED AT 400 WORDS)

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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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Responses from two firing patterns in inferior colliculus neurons to stimulation of the lateral lemniscus dorsal nucleus

Neural Regeneration Research ◽

10.4103/1673-5374.182706 ◽

2016 ◽

Vol 11 (5) ◽

pp. 787 ◽

Cited By ~ 1

Author(s):

Ning-yu Wang ◽

Xiao-ting Li ◽

Yan-jun Wang ◽

Zhi-qing Xu ◽

Jin-feng Liu ◽

...

Keyword(s):

Inferior Colliculus ◽

Lateral Lemniscus ◽

Firing Patterns ◽

Dorsal Nucleus ◽

Stimulation Of

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In vitro brain slice studies of the rat's dorsal nucleus of the lateral lemniscus. III. synaptic pharmacology

Journal of Neurophysiology ◽

10.1152/jn.1996.75.3.1271 ◽

1996 ◽

Vol 75 (3) ◽

pp. 1271-1282 ◽

Cited By ~ 40

Author(s):

S. H. Wu ◽

J. B. Kelly

Keyword(s):

Amino Acid ◽

Brain Slice ◽

Nmda Antagonist ◽

Membrane Resistance ◽

Short Latency ◽

Lateral Lemniscus ◽

Dorsal Nucleus ◽

Long Latency ◽

Single Spike ◽

Stimulation Of

1. The synaptic pharmacology of the dorsal nucleus of the lateral lemniscus (DNLL) of the rat was investigated in a brain slice preparation of the auditory midbrain. The brain slice was cut in the coronal plane and placed in a small recording chamber where warm, oxygenated saline was continuously perfused over and underneath the tissue. Intracellular recordings were made with glass microelectrodes filled with 4 M potassium acetate. Synaptic potentials were elicited by electrical stimulation of the lateral lemniscus or commissure of Probst and pharmacological effects were tested by bath application of amino acid agonists and antagonists. 2. The cells in DNLL were challenged with the excitatory amino acid (EAA) agonists, alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid (AMPA), N-methyl-D-aspartic acid (NMDA) in 0 Mg2+, and L-glutamate. Each of these caused a depolarization of the cell membrane, a reduction in cell membrane resistance, and the onset of spontaneous firing. 3. Short-latency excitatory postsynaptic potentials (EPSPs) were evoked by stimulation of the lateral lemniscus in 77% of the neurons tested. The mean latency to initial depolarization was 0.9 ms. A single spike with relatively constant latency (mean 1.5 ms) was typically elicited when the strength of lemniscal stimulation was increased. A longer-latency EPSP (mean 2.9 ms) was seen in 34% of the neurons tested either with the slice in normal saline or after pharmacological block of the earlier, short-latency EPSP. The long-latency EPSP was followed by a single spike of multiple spikes with highly variable latencies (range 3.2-24 ms). In 28% of the neurons tested, both early and late EPSPs were observed in response to stimulation of a single location on the lateral lemniscus. 4. Stimulation of the commissure of Probst elicited short-latency EPSPs (mean 0.9 ms) in 37% of the neurons tested. Longer-latency EPSPs (mean 3.0 ms) were found in only 3% of the neurons in response to commissural stimulation. 5. The nonspecific EAA antagonist kynurenic acid blocked both short-and long-latency EPSPs evoked by either lemniscal or commissural stimulation. The non-NMDA antagonist 6-cyano-7-nitro-quinoxaline-2,3-dione (CNQX), at very low concentrations, blocked the short-latency EPSPs but had no effect on the longer-latency EPSPs. The short-latency EPSPs were unaffected by the NMDA antagonist D,L-2-amino-5-phosphonovaleric acid (APV). In contrast, the longer-latency EPSPs were blocked by APV, but never by CNQX. 6. DNLL neurons were affected by the inhibitory amino acid agonists gamma-aminobutyric acid (GABA) and glycine. The membrane resistance of the neurons was decreased by GABA and glycine in a solution of either normal or calcium-free saline in a concentration-dependent manner. 7. Inhibitory postsynaptic potentials (IPSPs) were elicited by stimulation of the lateral lemniscus in 53% of the neurons and the commissure of the Probst in 18% of the neurons tested. The mean latencies were 1.0 and 0.9 ms, respectively. The reversal potentials of the IPSPs were around -70 mV. 8. The IPSPs evoked by stimulation of the lateral lemniscus were blocked by the glycine receptor antagonist strychnine, but not by the GABA receptor antagonist bicuculline, whereas the IPSPs elicited by stimulation of the commissure of Probst were blocked by bicuculline but not strychnine.

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