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>
Contribution of NMDA and AMPA receptors to temporal patterning of auditory responses in the inferior colliculus.
Animals; Chiroptera/*physiology; Neurons/physiology; Action Potentials/drug effects; Excitatory Amino Acid Antagonists/pharmacology; Quinoxalines/pharmacology; Inferior Colliculi/cytology/drug effects/*physiology; Piperazines/pharmacology; *Acoustic Stimulation; Reaction Time/drug effects/*physiology; N-Methyl-D-Aspartate/*physiology; Receptors; AMPA/*physiology
Although NMDA receptors (NMDARs) are associated with synaptic plasticity, they form an essential part of responses to sensory stimuli. We compared contributions of glutamatergic NMDARs and AMPA receptors (AMPARs) to auditory responses in the inferior colliculus (IC) of awake, adult mustached bats. We examined the magnitude and temporal pattern of responses to tonal signals in single units before, during, and after local micro-iontophoretic application of selective antagonists to AMPARs [NBQX (1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide)] and NMDARs [CPP ((+/-)3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid)]. Combined blockade of AMPARs and NMDARs eliminated excitatory responses in nearly all neurons, whereas separate blockade of each receptor was quantitatively similar, causing substantial (\textgreater 50%) spike reductions in approximately 75% of units. The major result was that effects of receptor blockade were most closely related to the first-spike latency of a unit. Thus, AMPAR blockade substantially reduced spikes in all short-latency units (\textless 12 ms) but never in long-latency units (\textgreater or = 12 ms). NMDAR blockade had variable effects on short-latency units but reduced spikes substantially for all long-latency units. There were no distinct contributions of AMPARs and NMDARs to early and late elements of responses. Thus, AMPAR blockade reduced early (onset) spikes somewhat more effectively than NMDAR blockade in short-latency units, but NMDAR blockade reduced onset spikes more effectively in long-latency units. AMPAR and NMDAR blockade were equally effective in reducing later elements of sustained responses in short-latency units, whereas NMDAR blockade was much more effective in long-latency units. These results indicate that NMDARs play multiple roles for signal processing in adult IC neurons.
Sanchez Jason Tait; Gans Donald; Wenstrup Jeffrey J
The Journal of neuroscience : the official journal of the Society for Neuroscience
2007
2007-02
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.2894-06.2007" target="_blank" rel="noreferrer noopener">10.1523/JNEUROSCI.2894-06.2007</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>
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>
Effects of artifact rejection and bayesian weighting on the auditory brainstem response during quiet and active behavioral conditions.
*Artifacts; *Bayes Theorem; Adult; Auditory; Brain Stem/*physiology; Evoked Potentials; Female; Humans; Male; Motor Activity/*physiology; Noise; Rest/physiology
PURPOSE: To evaluate the effects of 2 noise reduction techniques on the auditory brainstem response (ABR). METHOD: ABRs of 20 normal hearing adults were recorded during quiet and active behavioral conditions using 2 stimulus intensity levels. Wave V amplitudes and residual noise root-mean-square values were measured following the offline application of artifact rejection and Bayesian weighting. Repeated measures analysis of variance and Bonferroni adjusted pairwise t tests were utilized to evaluate significant main effects and interactions between the 2 noise reduction techniques. RESULTS: ABRs recorded during the quiet behavioral condition resulted in minimal differences in wave V amplitude and noise reduction improvement, suggesting that the 2 techniques were equally effective under ideal recording situations. During the active behavioral condition, however, the techniques differed significantly in the ability to preserve the evoked potential and reduce noise. Consequently, strict artifact rejection levels resulted in an inherent underestimation of wave V amplitudes when compared with the Bayesian approach. CONCLUSION: Artifact rejection had a detrimental effect on waveform morphology of the ABR. This could lead to difficulty in ABR interpretation when patients are active and ultimately result in diagnostic errors.
Sanchez Jason Tait; Gans Donald
American Journal of Audiology
2006
2006-12
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/10.1044/1059-0889(2006/019)" target="_blank" rel="noreferrer noopener">10.1044/1059-0889(2006/019)</a>