High concentrations of divalent cations isolate monosynaptic inputs from local circuits in the auditory midbrain.
inferior colliculus; Animals; Mice; Acoustic Stimulation; Neural Inhibition/drug effects/*physiology; high divalents; local circuits; monosynaptic; first spike latency; Inferior Colliculi/drug effects/*physiology; Reaction Time/drug effects/physiology; Synapses/drug effects/*physiology; Cations; Divalent/*pharmacology
Hierarchical processing of sensory information occurs at multiple levels between the peripheral and central pathway. Different extents of convergence and divergence in top down and bottom up projections makes it difficult to separate the various components activated by a sensory input. In particular, hierarchical processing at sub-cortical levels is little understood. Here we have developed a method to isolate extrinsic inputs to the inferior colliculus (IC), a nucleus in the midbrain region of the auditory system, with extensive ascending and descending convergence. By applying a high concentration of divalent cations (HiDi) locally within the IC, we isolate a HiDi-sensitive from a HiDi-insensitive component of responses evoked by afferent input in brain slices and in vivo during a sound stimulus. Our results suggest that the HiDi-sensitive component is a monosynaptic input to the IC, while the HiDi-insensitive component is a local polysynaptic circuit. Monosynaptic inputs have short latencies, rapid rise times, and underlie first spike latencies. Local inputs have variable delays and evoke long-lasting excitation. In vivo, local circuits have variable onset times and temporal profiles. Our results suggest that high concentrations of divalent cations should prove to be a widely useful method of isolating extrinsic monosynaptic inputs from local circuits in vivo.
Sivaramakrishnan Shobhana; Sanchez Jason Tait; Grimsley Calum Alex
Frontiers in neural circuits
2013
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/10.3389/fncir.2013.00175" target="_blank" rel="noreferrer noopener">10.3389/fncir.2013.00175</a>
Midbrain local circuits shape sound intensity codes.
inferior colliculus; Animals; Mice; Neurons/physiology; Acoustic Stimulation; Auditory Perception/*physiology; Inferior Colliculi/*physiology; Auditory Pathways/*physiology; Auditory Threshold/physiology; high divalents; local circuits; monosynaptic; Neural Inhibition/*physiology; sound intensity
Hierarchical processing of sensory information requires interaction at multiple levels along the peripheral to central pathway. Recent evidence suggests that interaction between driving and modulating components can shape both top down and bottom up processing of sensory information. Here we show that a component inherited from extrinsic sources combines with local components to code sound intensity. By applying high concentrations of divalent cations to neurons in the nucleus of the inferior colliculus in the auditory midbrain, we show that as sound intensity increases, the source of synaptic efficacy changes from inherited inputs to local circuits. In neurons with a wide dynamic range response to intensity, inherited inputs increase firing rates at low sound intensities but saturate at mid-to-high intensities. Local circuits activate at high sound intensities and widen dynamic range by continuously increasing their output gain with intensity. Inherited inputs are necessary and sufficient to evoke tuned responses, however local circuits change peak output. Push-pull driving inhibition and excitation create net excitatory drive to intensity-variant neurons and tune neurons to intensity. Our results reveal that dynamic range and tuning re-emerge in the auditory midbrain through local circuits that are themselves variable or tuned.
Grimsley Calum Alex; Sanchez Jason Tait; 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.2013.00174" target="_blank" rel="noreferrer noopener">10.3389/fncir.2013.00174</a>
Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus.
lateral lemniscus; biosonar; combination sensitivity; combination-sensitive; echolocation; facilitation; glycinergic; medial nucleus of trapezoid body
This review describes mechanisms and circuitry underlying combination-sensitive response properties in the auditory brainstem and midbrain. Combination-sensitive neurons, performing a type of auditory spectro-temporal integration, respond to specific, properly timed combinations of spectral elements in vocal signals and other acoustic stimuli. While these neurons are known to occur in the auditory forebrain of many vertebrate species, the work described here establishes their origin in the auditory brainstem and midbrain. Focusing on the mustached bat, we review several major findings: (1) Combination-sensitive responses involve facilitatory interactions, inhibitory interactions, or both when activated by distinct spectral elements in complex sounds. (2) Combination-sensitive responses are created in distinct stages: inhibition arises mainly in lateral lemniscal nuclei of the auditory brainstem, while facilitation arises in the inferior colliculus (IC) of the midbrain. (3) Spectral integration underlying combination-sensitive responses requires a low-frequency input tuned well below a neuron's characteristic frequency (ChF). Low-ChF neurons in the auditory brainstem project to high-ChF regions in brainstem or IC to create combination sensitivity. (4) At their sites of origin, both facilitatory and inhibitory combination-sensitive interactions depend on glycinergic inputs and are eliminated by glycine receptor blockade. Surprisingly, facilitatory interactions in IC depend almost exclusively on glycinergic inputs and are largely independent of glutamatergic and GABAergic inputs. (5) The medial nucleus of the trapezoid body (MNTB), the lateral lemniscal nuclei, and the IC play critical roles in creating combination-sensitive responses. We propose that these mechanisms, based on work in the mustached bat, apply to a broad range of mammals and other vertebrates that depend on temporally sensitive integration of information across the audible spectrum.
Wenstrup Jeffrey James; Nataraj Kiran; Sanchez Jason Tait
Frontiers in neural circuits
2012
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/10.3389/fncir.2012.00075" target="_blank" rel="noreferrer noopener">10.3389/fncir.2012.00075</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>
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>
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>