Functional architecture of the inferior colliculus revealed with voltage-sensitive dyes.
Animals; Mice; Acoustic Stimulation/methods; Rats; local circuits; Auditory Pathways/chemistry/cytology/physiology; Fluorescent Dyes/*analysis; Inferior Colliculi/*chemistry/*cytology/physiology; laminar organization; microcircuits; Nerve Net/*chemistry/*cytology/physiology; population coding; post-inhibitory rebound; Voltage-Sensitive Dye Imaging/*methods; Long-Evans; Inbred CBA
We used optical imaging with voltage-sensitive dyes to investigate the spatio-temporal dynamics of synaptically evoked activity in brain slices of the inferior colliculus (IC). Responses in transverse slices which preserve cross-frequency connections and in modified sagittal slices that preserve connections within frequency laminae were evoked by activating the lateral lemniscal tract. Comparing activity between small and large populations of cells revealed response areas in the central nucleus of the IC that were similar in magnitude but graded temporally. In transverse sections, these response areas are summed to generate a topographic response profile. Activity through the commissure to the contralateral IC required an excitation threshold that was reached when GABAergic inhibition was blocked. Within laminae, module interaction created temporal homeostasis. Diffuse activity evoked by a single lemniscal shock re-organized into distinct spatial and temporal compartments when stimulus trains were used, and generated a directional activity profile within the lamina. Using different stimulus patterns to activate subsets of microcircuits in the central nucleus of the IC, we found that localized responses evoked by low-frequency stimulus trains spread extensively when train frequency was increased, suggesting recruitment of silent microcircuits. Long stimulus trains activated a circuit specific to post-inhibitory rebound neurons. Rebound microcircuits were defined by a focal point of initiation that spread to an annular ring that oscillated between inhibition and excitation. We propose that much of the computing power of the IC is derived from local circuits, some of which are cell-type specific. These circuits organize activity within and across frequency laminae, and are critical in determining the stimulus-selectivity of auditory coding.
Chandrasekaran Lakshmi; Xiao Ying; Sivaramakrishnan Shobhana
Frontiers in neural circuits
2013
1905-7
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.3389/fncir.2013.00041" target="_blank" rel="noreferrer noopener">10.3389/fncir.2013.00041</a>
Glycinergic "inhibition" mediates selective excitatory responses to combinations of sounds.
Animals; Acoustic Stimulation/methods; Neural Inhibition/drug effects/*physiology; *Sound; Excitatory Amino Acid Antagonists/pharmacology; Action Potentials/drug effects/physiology; Auditory Pathways/*physiology; Glycine Agents/pharmacology; Glycine/*physiology; Chiroptera/physiology; Drug Interactions; GABA Agents/pharmacology; Inferior Colliculi/cytology/drug effects/*physiology; Iontophoresis/methods; Neurons/drug effects/physiology/radiation effects; Piperazines/pharmacology; Dose-Response Relationship; Receptors; Radiation; GABA/physiology; N-Methyl-D-Aspartate/antagonists & inhibitors/physiology
In the mustached bat's inferior colliculus (IC), combination-sensitive neurons display time-sensitive facilitatory interactions between inputs tuned to distinct spectral elements in sonar or social vocalizations. Here we compare roles of ionotropic receptors to glutamate (iGluRs), glycine (GlyRs), and GABA (GABA(A)Rs) in facilitatory combination-sensitive interactions. Facilitatory responses to 36 single IC neurons were recorded before, during, and after local application of antagonists to these receptors. The NMDA receptor antagonist CPP [(+/-)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid], alone (n = 14) or combined with AMPA receptor antagonist NBQX (n = 22), significantly reduced or eliminated responses to best frequency (BF) sounds across a broad range of sound levels, but did not eliminate combination-sensitive facilitation. In a subset of neurons, GABA(A)R blockers bicuculline or gabazine were applied in addition to iGluR blockers. GABA(A)R blockers did not "uncover" residual iGluR-mediated excitation, and only rarely eliminated facilitation. In nearly all neurons for which the GlyR antagonist strychnine was applied in addition to iGluR blockade (22 of 23 neurons, with or without GABA(A)R blockade), facilitatory interactions were eliminated. Thus, neither glutamate nor GABA neurotransmission are required for facilitatory combination-sensitive interactions in IC. Instead, facilitation may depend entirely on glycinergic inputs that are presumed to be inhibitory. We propose that glycinergic inputs tuned to two distinct spectral elements in vocal signals each activate postinhibitory rebound excitation. When rebound excitations from two spectral elements coincide, the neuron discharges. Excitation from glutamatergic inputs, tuned to the BF of the neuron, is superimposed onto this facilitatory interaction, presumably mediating responses to a broader range of acoustic signals.
Sanchez Jason Tait; Gans Donald; Wenstrup Jeffrey J
The Journal of neuroscience : the official journal of the Society for Neuroscience
2008
2008-01
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/JNEUROSCI.3572-07.2008" target="_blank" rel="noreferrer noopener">10.1523/JNEUROSCI.3572-07.2008</a>
Exploiting development to evaluate auditory encoding of amplitude modulation.
Female; Male; Animals; Acoustic Stimulation/methods; Age Factors; Auditory Perception/*physiology; Gerbillinae; Auditory Threshold/*physiology; Auditory Cortex/*growth & development; Auditory Pathways/*growth & development
During development, detection for many percepts matures gradually. This provides a natural system in which to investigate the neural mechanisms underlying performance differences: those aspects of neural activity that mature in conjunction with behavioral performance are more likely to subserve detection. In principle, the limitations on performance could be attributable to either immature sensory encoding mechanisms or an immature decoding of an already-mature sensory representation. To evaluate these alternatives in awake gerbil auditory cortex, we measured neural detection of sinusoidally amplitude-modulated (sAM) stimuli, for which behavioral detection thresholds display a prolonged maturation. A comparison of single-unit responses in juveniles and adults revealed that encoding of static tones was adult like in juveniles, but responses to sAM depth were immature. Since perceptual performance may reflect the activity of an animal's most sensitive neurons, we analyzed the d prime curves of single neurons and found an equivalent percentage with highly sensitive thresholds in juvenile and adult animals. In contrast, perceptual performance may reflect the pooling of information from neurons with a range of sensitivities. We evaluated a pooling model that assumes convergence of a population of inputs at a downstream target neuron and found poorer sAM detection thresholds for juveniles. Thus, if sAM detection is based on the most sensitive neurons, then immature behavioral performance is best explained by an immature decoding mechanism. However, if sAM detection is based on a population response, then immature detection thresholds are more likely caused by an inadequate sensory representation.
Rosen Merri J; Semple Malcolm N; Sanes Dan H
The Journal of neuroscience : the official journal of the Society for Neuroscience
2010
2010-11
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/JNEUROSCI.3340-10.2010" target="_blank" rel="noreferrer noopener">10.1523/JNEUROSCI.3340-10.2010</a>
Projection to the inferior colliculus from the basal nucleus of the amygdala.
Animals; Acoustic Stimulation/methods; Species Specificity; Action Potentials/physiology; Amygdala/*cytology/physiology; Dextrans; Rhodamines; Fluorescent Dyes; *Stilbamidines; Auditory Cortex/cytology; Auditory Pathways/*cytology/physiology; Axonal Transport/physiology; Brain Stem/cytology; Chiroptera/*anatomy & histology/physiology; Cholera Toxin/pharmacokinetics; Inferior Colliculi/*cytology/physiology; Neurons/cytology/physiology; Wheat Germ Agglutinin-Horseradish Peroxidase Conjugate; Electrodes; Implanted
This report describes a projection from the amygdala, a forebrain center mediating emotional expression, to the inferior colliculus (IC), the midbrain integration center of the ascending auditory system. In the IC of mustached bats (Pteronotus parnellii) and pallid bats (Antrozous pallidus), we placed deposits of retrograde tracers at physiologically defined sites and then searched for retrogradely labeled somata in the forebrain. Labeling was most sensitive in experiments using cholera toxin B-subunit as tracer. We consistently observed retrograde labeling in a single amygdalar subdivision, the magnocellular subdivision of the basal nucleus (Bmg). The Bmg is distinctive across mammals, containing the largest cells in the amygdala and the most intense acetylcholinesterase staining. Labeled amygdalar cells occurred ipsilateral and contralateral to IC deposits, but ipsilateral labeling was greater, averaging 72%. Amygdalar labeling was observed after tracer deposits throughout the IC, including its central nucleus (ICC). In comparison, labeling in the auditory cortex (layer V) was heavily ipsilateral (averaging 92%). Cortical labeling depended on the location of IC deposits: dorsomedial deposits resulted in the most labeled cells, whereas ventrolateral deposits labeled few or no cortical cells. Cortical labeling occurred after several deposits in the ICC. Across experiments, the average number of labeled cells in the amygdala was similar to that in the auditory cortex, indicating that the amygdalocollicular projection is significant. The results demonstrate a direct, widespread projection from the basal amygdala to the IC. They also suggest the presence of a rapid thalamoamygdalocollicular feedback circuit that may impose emotional content onto processing of sensory stimuli at a relatively low level of an ascending sensory pathway.
Marsh Robert A; Fuzessery Zoltan M; Grose Carol D; Wenstrup Jeffrey J
The Journal of neuroscience : the official journal of the Society for Neuroscience
2002
2002-12
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/jneurosci.22-23-10449.2002" target="_blank" rel="noreferrer noopener">10.1523/jneurosci.22-23-10449.2002</a>
Spectral integration in the inferior colliculus: role of glycinergic inhibition in response facilitation.
Animals; Acoustic Stimulation/methods; Neural Inhibition/drug effects/*physiology; Chiroptera; Inferior Colliculi/drug effects/*physiology; Wakefulness/physiology; Auditory Pathways/drug effects/physiology; Echolocation/*physiology; Glycine Agents/administration & dosage; Glycine/*metabolism; Iontophoresis; Pitch Perception/drug effects/*physiology; Strychnine/administration & dosage; Electrodes; Animal/physiology; Vocalization; Implanted
This study examined the contribution of glycinergic inhibition to the time-sensitive spectral integration performed by neurons in the inferior colliculus of the mustached bat (Pteronotus parnellii). These neurons are sometimes called combination-sensitive because they display facilitatory (or inhibitory) responses to the combination of distinct spectral elements in sonar or social vocalizations. Present in a wide range of vertebrates, their temporally and spectrally selective integration is thought to endow them with the ability to discriminate among social vocalizations or to analyze particular cues concerning sonar targets. The mechanisms that underlie these responses or the sites in the auditory system where they are created are not known. We examined combination-sensitive neurons that are facilitated by the presentation of two different harmonic elements of the bat's sonar call and echo. Responses of 24 single units were recorded before and during local application of strychnine, an antagonist of glycinergic inhibition. For each of the 24 units, strychnine application eliminated or greatly reduced temporally sensitive facilitation. There was no difference in this effect for neurons tuned to frequencies associated with the frequency-modulated or the constant-frequency sonar components. These results are unusual because glycine is considered to be an inhibitory neurotransmitter, but here it appears to be essential for the expression of combination-sensitive facilitation. The findings provide strong evidence that facilitatory combination-sensitive response properties present throughout the mustached bat's auditory midbrain, thalamus, and cortex originate through neural interactions in the inferior colliculus.
Wenstrup J J; Leroy S A
The Journal of neuroscience : the official journal of the Society for Neuroscience
2001
2001-02
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/jneurosci.21-03-j0002.2001" target="_blank" rel="noreferrer noopener">10.1523/jneurosci.21-03-j0002.2001</a>
Synaptic Inhibition in Avian Interaural Level Difference Sound Localizing Neurons.
Female; Male; Animals; Acoustic Stimulation/methods; Tissue Culture Techniques; Chick Embryo; Patch-Clamp Techniques; *dorsal nucleus of the lateral lemniscus; *GABAA receptor; *interaural level difference; *reversal potential; *synaptic inhibition; Anions/metabolism; Avian Proteins/metabolism; Brain Stem/cytology/drug effects/*physiology; Chlorides/metabolism; Electric Stimulation; gamma-Aminobutyric Acid/metabolism; Intracellular Space/drug effects/metabolism; Neural Inhibition/drug effects/*physiology; Neurons/cytology/drug effects/*physiology; Sound Localization/drug effects/*physiology; Symporters/metabolism; Synaptic Transmission/drug effects/*physiology; Receptors; GABA-A/metabolism; Glycine/metabolism
Synaptic inhibition plays a fundamental role in the neural computation of the interaural level difference (ILD), an important cue for the localization of high-frequency sound. Here, we studied the inhibitory synaptic currents in the chicken posterior portion of the dorsal nucleus of the lateral lemniscus (LLDp), the first binaural level difference encoder of the avian auditory pathway. Using whole-cell recordings in brain slices, we provide the first evidence confirming a monosynaptic inhibition driven by direct electrical and chemical stimulation of the contralateral LLDp, establishing the reciprocal inhibitory connection between the two LLDps, a long-standing assumption in the field. This inhibition was largely mediated by GABAA receptors; however, functional glycine receptors were also identified. The reversal potential for the Cl(-) channels measured with gramicidin-perforated patch recordings was hyperpolarizing (-88 mV), corresponding to a low intracellular Cl(-) concentration (5.2 mm). Pharmacological manipulations of KCC2 (outwardly Cl(-) transporter) activity demonstrate that LLDp neurons can maintain a low intracellular Cl(-) concentration under a high Cl(-) load, allowing for the maintenance of hyperpolarizing inhibition. We further demonstrate that hyperpolarizing inhibition was more effective at regulating cellular excitability than depolarizing inhibition in LLDp neurons.
Curry Rebecca J; Lu Yong
eNeuro
2016
2016-12
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/ENEURO.0309-16.2016" target="_blank" rel="noreferrer noopener">10.1523/ENEURO.0309-16.2016</a>
Communication calls produced by electrical stimulation of four structures in the guinea pig brain.
Female; Male; Animals; Acoustic Stimulation/methods; Auditory Perception/physiology; Brain/*physiology; Electric Stimulation/methods; Guinea Pigs; Neurons/physiology; Animal/physiology; Vocalization
One of the main central processes affecting the cortical representation of conspecific vocalizations is the collateral output from the extended motor system for call generation. Before starting to study this interaction we sought to compare the characteristics of calls produced by stimulating four different parts of the brain in guinea pigs (Cavia porcellus). By using anaesthetised animals we were able to reposition electrodes without distressing the animals. Trains of 100 electrical pulses were used to stimulate the midbrain periaqueductal grey (PAG), hypothalamus, amygdala, and anterior cingulate cortex (ACC). Each structure produced a similar range of calls, but in significantly different proportions. Two of the spontaneous calls (chirrup and purr) were never produced by electrical stimulation and although we identified versions of chutter, durr and tooth chatter, they differed significantly from our natural call templates. However, we were routinely able to elicit seven other identifiable calls. All seven calls were produced both during the 1.6 s period of stimulation and subsequently in a period which could last for more than a minute. A single stimulation site could produce four or five different calls, but the amygdala was much less likely to produce a scream, whistle or rising whistle than any of the other structures. These three high-frequency calls were more likely to be produced by females than males. There were also differences in the timing of the call production with the amygdala primarily producing calls during the electrical stimulation and the hypothalamus mainly producing calls after the electrical stimulation. For all four structures a significantly higher stimulation current was required in males than females. We conclude that all four structures can be stimulated to produce fictive vocalizations that should be useful in studying the relationship between the vocal motor system and cortical sensory representation.
Green David B; Shackleton Trevor M; Grimsley Jasmine M S; Zobay Oliver; Palmer Alan R; Wallace Mark N
PloS one
2018
1905-07
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1371/journal.pone.0194091" target="_blank" rel="noreferrer noopener">10.1371/journal.pone.0194091</a>
Temporal features of spectral integration in the inferior colliculus: effects of stimulus duration and rise time.
Acoustic Stimulation/methods; Action Potentials/physiology; Animals; Auditory Perception/*physiology; Auditory Threshold/*physiology; Chiroptera/physiology; Inferior Colliculi/*cytology; Neural Inhibition/physiology; Neurons/*physiology; Predictive Value of Tests; Psycholinguistics; Reaction Time/*physiology; Time Factors; Wakefulness/physiology
This report examines temporal features of facilitation and suppression that underlie spectrally integrative responses to complex vocal signals. Auditory responses were recorded from 160 neurons in the inferior colliculus (IC) of awake mustached bats. Sixty-two neurons showed combination-sensitive facilitation: responses to best frequency (BF) signals were facilitated by well-timed signals at least an octave lower in frequency, in the range 16-31 kHz. Temporal features and strength of facilitation were generally unaffected by changes in duration of facilitating signals from 4 to 31 ms. Changes in stimulus rise time from 0.5 to 5.0 ms had little effect on facilitatory strength. These results suggest that low frequency facilitating inputs to high BF neurons have phasic-on temporal patterns and are responsive to stimulus rise times over the tested range. We also recorded from 98 neurons showing low-frequency (11-32 kHz) suppression of higher BF responses. Effects of changing duration were related to the frequency of suppressive signals. Signals\textless23 kHz usually evoked suppression sustained throughout signal duration. This and other features of such suppression are consistent with a cochlear origin that results in masking of responses to higher, near-BF signal frequencies. Signals in the 23- to 30-kHz range-frequencies in the first sonar harmonic-generally evoked phasic suppression of BF responses. This may result from neural inhibitory interactions within and below IC. In many neurons, we observed two or more forms of the spectral interactions described here. Thus IC neurons display temporally and spectrally complex responses to sound that result from multiple spectral interactions at different levels of the ascending auditory pathway.
Gans Donald; Sheykholeslami Kianoush; Peterson Diana Coomes; Wenstrup Jeffrey
Journal of neurophysiology
2009
2009-07
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.91300.2008" target="_blank" rel="noreferrer noopener">10.1152/jn.91300.2008</a>
Intracellular recordings from combination-sensitive neurons in the inferior colliculus.
Acoustic Stimulation/methods; Afferent/classification/*physiology; Animals; Auditory/physiology; Biological; Chiroptera; Evoked Potentials; Inferior Colliculi/*cytology; Membrane Potentials/physiology/radiation effects; Models; Neural Inhibition/*physiology; Neural Pathways/physiology; Neurons; Psychophysics; Reaction Time; Wakefulness
In vertebrate auditory systems, specialized combination-sensitive neurons analyze complex vocal signals by integrating information across multiple frequency bands. We studied combination-sensitive interactions in neurons of the inferior colliculus (IC) of awake mustached bats, using intracellular somatic recording with sharp electrodes. Facilitated combinatorial neurons are coincidence detectors, showing maximum facilitation when excitation from low- and high-frequency stimuli coincide. Previous work showed that facilitatory interactions originate in the IC, require both low and high frequency-tuned glycinergic inputs, and are independent of glutamatergic inputs. These results suggest that glycinergic inputs evoke facilitation through either postinhibitory rebound or direct depolarizing mechanisms. However, in 35 of 36 facilitated neurons, we observed no evidence of low frequency-evoked transient hyperpolarization or depolarization that was closely related to response facilitation. Furthermore, we observed no evidence of shunting inhibition that might conceal inhibitory inputs. Since these facilitatory interactions originate in IC neurons, the results suggest that inputs underlying facilitation are electrically segregated from the soma. We also recorded inhibitory combinatorial interactions, in which low frequency sounds suppress responses to higher frequency signals. In 43% of 118 neurons, we observed low frequency-evoked hyperpolarizations associated with combinatorial inhibition. For these neurons, we conclude that low frequency-tuned inhibitory inputs terminate on neurons primarily excited by high-frequency signals; these inhibitory inputs may create or enhance inhibitory combinatorial interactions. In the remainder of inhibited combinatorial neurons (57%), we observed no evidence of low frequency-evoked hyperpolarizations, consistent with observations that inhibitory combinatorial responses may originate in lateral lemniscal nuclei.
Peterson Diana Coomes; Voytenko Sergiy; Gans Donald; Galazyuk Alexander; Wenstrup Jeffrey
Journal of neurophysiology
2008
2008-08
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.90390.2008" target="_blank" rel="noreferrer noopener">10.1152/jn.90390.2008</a>
Roles of inhibition in creating complex auditory responses in the inferior colliculus: facilitated combination-sensitive neurons.
Acoustic Stimulation/methods; Action Potentials/*physiology; Animals; Auditory Pathways/physiology; Bicuculline/pharmacology; Cell Count; Drug Interactions; GABA Antagonists/pharmacology; Glycine Agents/pharmacology; Inferior Colliculi/*cytology; Iontophoresis/methods; Models; Neural Inhibition/drug effects/*physiology; Neurological; Neurons/classification/drug effects/*physiology/radiation effects; Otters; Reaction Time/*physiology/radiation effects; Regression Analysis; Strychnine/pharmacology; Time Factors; Wakefulness/physiology
We studied roles of inhibition on temporally sensitive facilitation in combination-sensitive neurons from the mustached bat's inferior colliculus (IC). In these integrative neurons, excitatory responses to best frequency (BF) tones are enhanced by much lower frequency signals presented in a specific temporal relationship. Most facilitated neurons (76%) showed inhibition at delays earlier than or later than the delays causing facilitation. The timing of inhibition at earlier delays was closely related to the best delay of facilitation, but the inhibition had little influence on the duration or strength of the facilitatory interaction. Local iontophoretic application of antagonists to receptors for glycine (strychnine, STRY) and gamma-aminobutyric acid (GABA) (bicuculline, BIC) showed that STRY abolished facilitation in 96% of tested units, but BIC eliminated facilitation in only 28%. This suggests that facilitatory interactions are created in IC and reveals a differential role for these neurotransmitters. The facilitation may be created by coincidence of a postinhibitory rebound excitation activated by the low-frequency signal with the BF-evoked excitation. Unlike facilitation, inhibition at earlier delays was not eliminated by application of antagonists, suggesting an origin in lower brain stem nuclei. However, inhibition at delays later than facilitation, like facilitation itself, appears to originate within IC and to be more dependent on glycinergic than GABAergic mechanisms. Facilitatory and inhibitory interactions displayed by these combination-sensitive neurons encode information within sonar echoes and social vocalizations. The results indicate that these complex response properties arise through a series of neural interactions in the auditory brain stem and midbrain.
Nataraj Kiran; Wenstrup Jeffrey J
Journal of neurophysiology
2005
2005-06
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.01152.2004" target="_blank" rel="noreferrer noopener">10.1152/jn.01152.2004</a>
Auditory responses in the cochlear nucleus of awake mustached bats: precursors to spectral integration in the auditory midbrain.
Acoustic Stimulation/methods; Action Potentials/*physiology; Animals; Auditory; Brain Mapping; Brain Stem/*physiology; Chiroptera/*physiology; Cochlear Nucleus/*physiology; Evoked Potentials; Mesencephalon/physiology; Nerve Net/*physiology; Pitch Perception/*physiology; Wakefulness/physiology
In the cochlear nucleus (CN) of awake mustached bats, single- and two-tone stimuli were used to examine how responses in major CN subdivisions contribute to spectrotemporal integrative features in the inferior colliculus (IC). Across CN subdivisions, the proportional representation of frequencies differed. A striking result was the substantial number of units tuned to frequencies \textless23 kHz. Across frequency bands, temporal response patterns, latency, and spontaneous discharge differed. For example, the 23- to 30-kHz representation, which comprises the fundamental of the sonar call, had an unusually high proportion of units with onset responses (39%) and low spontaneous rates (53%). Units tuned to 58-59 kHz, corresponding to the sharply tuned cochlear resonance, had slightly but significantly longer latencies than other bands. In units tuned to frequencies \textgreater30 kHz, 31% displayed a secondary excitatory peak, usually between 10 and 22 kHz. The secondary peak may originate in cochlear mechanisms for some units, but in others it may result from convergent input onto CN neurons. In 20% of units tested with two-tone stimuli, suppression of best frequency (BF) responses was tuned at least an octave below BF. These properties may underlie similar IC responses. However, other forms of spectral interaction present in IC were absent in CN: we found no facilitatory combination-sensitive interactions and very few combination-sensitive inhibitory interactions of the dominant IC type in which inhibition was tuned to 23-30 kHz. Such interactions arise above CN. Distinct forms of spectral integration thus originate at different levels of the ascending auditory pathway.
Marsh Robert A; Nataraj Kiran; Gans Donald; Portfors Christine V; Wenstrup Jeffrey J
Journal of neurophysiology
2006
2006-01
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.00634.2005" target="_blank" rel="noreferrer noopener">10.1152/jn.00634.2005</a>
Leading inhibition to neural oscillation is important for time-domain processing in the auditory midbrain.
*Periodicity; Acoustic Stimulation/methods; Action Potentials/drug effects/physiology; Animals; Anura; Auditory Pathways/physiology; Bicuculline/pharmacology; Chiroptera; Dose-Response Relationship; Echolocation/*physiology; GABA Antagonists/pharmacology; Mesencephalon/*cytology/physiology; Neural Inhibition/drug effects/*physiology; Neurons/drug effects/*physiology; Newborn; Radiation; Reaction Time/drug effects/*physiology; Sound; Species Specificity; Time Factors
A number of central auditory neurons exhibit paradoxical latency shift (PLS), a response characterized by longer response latencies at higher sound levels. PLS neurons are known to play a role in target ranging for echolocating bats that emit frequency-modulated sounds. We recently reported that early inhibition of unit's oscillatory discharges is critical for PLS in the inferior colliculus (IC) of little brown bats. The goal of this study was to determine in echolocating bats and in non-echolocating animals (frogs): 1) the detailed characteristics of PLS and whether PLS was dependent on sound level, frequency, and duration; 2) the time course of inhibition underlying PLS using a paired-pulse paradigm. We found that 22% of IC neurons in bats and 15% in frogs exhibited periodic discharge patterns in response to tone pulses at high sound levels. The firing periodicity was unit specific and independent of sound level and duration. Other IC neurons (28% in bats; 14% in frogs) exhibited PLS. These PLS neurons shared several response characteristics: 1) PLS was largely independent of sound frequency and 2) the magnitude of shift in first-spike latency was either duration dependent or duration tolerant. For PLS neurons, application of bicuculline abolished PLS and unmasked the unit's periodical firing pattern that served as the building block for PLS. In response to paired sound pulses, PLS neurons exhibited delay-dependent response suppression, confirming that high-threshold leading inhibition was responsible for PLS. Results also revealed the timing of excitatory and inhibitory inputs underlying PLS and its role in time-domain processing.
Galazyuk Alexander V; Lin Wenyu; Llano Daniel; Feng Albert S
Journal of neurophysiology
2005
2005-07
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1152/jn.00056.2005" target="_blank" rel="noreferrer noopener">10.1152/jn.00056.2005</a>
Intrinsic plasticity induced by group II metabotropic glutamate receptors via enhancement of high-threshold KV currents in sound localizing neurons.
Acoustic Stimulation/methods; Action Potentials/drug effects/physiology; Animals; Auditory Pathways/drug effects/*physiology; Brain/drug effects/physiology; Chick Embryo; Glutamic Acid/metabolism; metabotropic glutamate receptor; Metabotropic Glutamate/agonists/*metabolism; neuromodulation; Neuronal Plasticity/drug effects/*physiology; Neurons/drug effects/*physiology; nucleus laminaris; Patch-Clamp Techniques; Potassium Channels; Potassium/metabolism; Protein Kinase C/metabolism; Receptors; Sound Localization/drug effects/*physiology; Tissue Culture Techniques; Type C Phospholipases/metabolism; voltage-gated potassium channel; Voltage-Gated/*metabolism
Intrinsic plasticity has emerged as an important mechanism regulating neuronal excitability and output under physiological and pathological conditions. Here, we report a novel form of intrinsic plasticity. Using perforated patch clamp recordings, we examined the modulatory effects of group II metabotropic glutamate receptors (mGluR II) on voltage-gated potassium (KV) currents and the firing properties of neurons in the chicken nucleus laminaris (NL), the first central auditory station where interaural time cues are analyzed for sound localization. We found that activation of mGluR II by synthetic agonists resulted in a selective increase of the high-threshold KV currents. More importantly, synaptically released glutamate (with reuptake blocked) also enhanced the high-threshold KV currents. The enhancement was frequency-coding region dependent, being more pronounced in low-frequency neurons compared to middle- and high-frequency neurons. The intracellular mechanism involved the Gbetagamma signaling pathway associated with phospholipase C and protein kinase C. The modulation strengthened membrane outward rectification, sharpened action potentials, and improved the ability of NL neurons to follow high-frequency inputs. These data suggest that mGluR II provides a feedforward modulatory mechanism that may regulate temporal processing under the condition of heightened synaptic inputs.
Hamlet W R; Lu Y
Neuroscience
2016
2016-06
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/j.neuroscience.2016.03.010" target="_blank" rel="noreferrer noopener">10.1016/j.neuroscience.2016.03.010</a>
mGluRs modulate neuronal firing in the auditory midbrain.
Acoustic Stimulation/methods; Action Potentials/drug effects/*physiology; Animals; Auditory Perception/drug effects/physiology; Excitatory Amino Acid Agonists/pharmacology; Excitatory Amino Acid Antagonists/pharmacology; Glutamic Acid/physiology; Inbred CBA; Inferior Colliculi/drug effects/metabolism/*physiology; Metabotropic Glutamate/agonists/antagonists & inhibitors/*physiology; Mice; Neural Inhibition/drug effects/physiology; Neurons/drug effects/*physiology; Perceptual Masking/physiology; Receptors; Synaptic Transmission/drug effects/physiology
The mechanisms underlying sound-evoked suppression of neuronal firing in the auditory system are poorly understood. To explore these mechanisms in the inferior colliculus (IC), agonists and antagonists targeting different groups of metabotropic glutamate receptors (mGluRs) were applied iontophoretically to IC neurons in awake mice. We found that a group I-specific mGluR agonist predominantly increased neuronal firing in 52% of neurons, whereas group I antagonist had the opposite effect in 51% of neurons. A group II specific agonist showed no effect on neuronal firing but an antagonist increased firing rate in 48% of neurons. Neither a group III-specific mGluR agonist nor an antagonist had an effect on neuronal firing in the IC. We also found that sound stimuli triggered suppression of spontaneous firing in 70% of IC neurons. This suppression was reversibly blocked by group I mGluR antagonists. There is a possible link between this suppression and two perceptual phenomena: forward masking and "residual inhibition," the brief reduction/elimination of tinnitus following an appropriate masking sound.
Voytenko S V; Galazyuk A V
Neuroscience letters
2011
2011-04
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/j.neulet.2011.01.075" target="_blank" rel="noreferrer noopener">10.1016/j.neulet.2011.01.075</a>
An improved approach to separating startle data from noise.
*Electronic Data Processing; *Noise; Acoustic startle reflex; Acoustic Stimulation/methods; Analysis of Variance; Animal locomotion; Animals; Auditory/*physiology; Automated classification; Evoked Potentials; Inbred CBA; Male; Mice; Reflex; Startle waveform analysis; Startle/*physiology; Time Factors; Video Recording
BACKGROUND: The acoustic startle reflex (ASR) is a rapid, involuntary movement to sound, found in many species. The ASR can be modulated by external stimuli and internal state, making it a useful tool in many disciplines. ASR data collection and interpretation varies greatly across laboratories making comparisons a challenge. NEW METHOD: Here we investigate the animal movement associated with a startle in mouse (CBA/CaJ). Movements were simultaneously captured with high-speed video and a piezoelectric startle plate. We also use simple mathematical extrapolations to convert startle data (force) into center of mass displacement ("height"), which incorporates the animal's mass. RESULTS: Startle plate force data revealed a stereotype waveform associated with a startle that contained three distinct peaks. This waveform allowed researchers to separate trials into 'startles' and 'no-startles' (termed 'manual classification). Fleiss' kappa and Krippendorff"s alpha (0.865 for both) indicate very good levels of agreement between researchers. Further work uses this waveform to develop an automated startle classifier. The automated classifier compares favorably with manual classification. A two-way ANOVA reveals no significant difference in the magnitude of the 3 peaks as classified by the manual and automated methods (P1: p=0.526, N1: p=0.488, P2: p=0.529). COMPARISON WITH EXISTING METHOD(S): The ability of the automated classifier was compared with three other commonly used classification methods; the automated classifier far outperformed these methods. CONCLUSIONS: The improvements made allow researchers to automatically separate startle data from noise, and normalize for an individual animal's mass. These steps ease inter-animal and inter-laboratory comparisons of startle data.
Grimsley Calum A; Longenecker Ryan J; Rosen Merri J; Young Jesse W; Grimsley Jasmine M S; Galazyuk Alexander V
Journal of neuroscience methods
2015
2015-09
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/j.jneumeth.2015.07.001" target="_blank" rel="noreferrer noopener">10.1016/j.jneumeth.2015.07.001</a>
Responses to combinations of tones in the nuclei of the lateral lemniscus.
Acoustic Stimulation/methods; Animals; Auditory Pathways/*physiology; Brain Stem/*physiology; Chiroptera; Electrophysiology; Neurons/physiology; Reaction Time/physiology
Combination-sensitive neurons integrate specific spectral and temporal elements in biologically important sounds, and they may underlie the analysis of biosonar and social vocalizations. Combination-sensitive neurons are found in the forebrain of a variety of vertebrates. In the mustached bat, they also occur in the central nucleus of the inferior colliculus (ICC). However, it is not known where combination-sensitive response properties emerge. To address this question, we used a two-tone paradigm to examine responses of single units to combination stimuli in a brainstem structure, the nuclei of the lateral lemniscus (NLL). We recorded and histologically localized 101 single units in the NLL. The majority (82%) of units had a single excitatory frequency tuning curve. Seven units had two separate excitatory frequency tuning curves but displayed no combinatorial interaction. Twelve units were combination-sensitive. Of these, three units were facilitated by the combination of two separate frequency bands and nine units were inhibited by combinatorial stimuli. The three facilitatory neurons had excitatory responses tuned to the second harmonic constant frequency (CF2, 57-60 kHz) component of the biosonar signal and were facilitated by a second signal within the first harmonic (Hl, 24-30 kHz) of the biosonar call. Most of the inhibitory interactions occurred between signals in the frequency bands associated with the frequency-modulated (FM) components of the biosonar call. The strongest combinatorial effects (facilitatory and inhibitory) were elicited by simultaneous onset of the two signals (i.e., 0 ms delay). All combination-sensitive units were in the intermediate nucleus of the NLL (INLL), which in bats is a hypertrophied structure that projects strongly to combination-sensitive neurons in the ICC. Thus, the combination-sensitive neurons in the INLL may impart their response properties onto ICC neurons. However, the small number of facilitatory combination-sensitive neurons in the NLL suggests that the majority of these combinatorial responses originate in the ICC.
Portfors C V; Wenstrup J J
Journal of the Association for Research in Otolaryngology : JARO
2001
2001-06
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1007/s101620010057" target="_blank" rel="noreferrer noopener">10.1007/s101620010057</a>