Roles of inhibition in complex auditory responses in the inferior colliculus: inhibited combination-sensitive neurons.
Acoustic Stimulation; Action Potentials/drug effects/physiology; Afferent/drug effects/*physiology; Animals; Auditory; Auditory Pathways/drug effects/*physiology; Bicuculline/pharmacology; Brain Stem/drug effects/*physiology; Chiroptera; Electrophysiology; Evoked Potentials; GABA-A Receptor Antagonists; GABA-A/physiology; Glycine/antagonists & inhibitors/physiology; Inferior Colliculi/*physiology; Neural Inhibition/drug effects/*physiology; Neurons; Receptors; Strychnine/pharmacology
We studied the functional properties and underlying neural mechanisms associated with inhibitory combination-sensitive neurons in the mustached bat's inferior colliculus (IC). In these neurons, the excitatory response to best frequency tones was suppressed by lower frequency signals (usually in the range of 12-30 kHz) in a time-dependant manner. Of 143 inhibitory units, the majority (71%) were type I, in which low-frequency sounds evoked inhibition only. In the remainder, however, the low-frequency inhibitory signal also evoked excitation. Of these, excitation preceded the inhibition in type E/I units (16%), whereas in type I/E units (13%), excitation followed the inhibition. Type E/I and I/E units were distinct in the tuning and threshold sensitivity of low-frequency responses, whereas type I units overlapped the other types in these features. In 71 neurons, antagonists to receptors for glycine [strychnine (STRY)] or GABA [bicuculline (BIC)] were applied microiontophoretically. These antagonists failed to eliminate combination-sensitive inhibition in 92% (STRY), 93% (BIC), and 87% (BIC + STRY) of the type I units tested. However, inhibition was reduced in many neurons. Results were similar for type E/I and I/E inhibitory neurons. The results indicate that there are distinct populations of combination-sensitive inhibited neurons in the IC and that these populations are at least partly independent of glycine or GABAA receptors in the IC. We propose that these populations originate in different brain stem auditory nuclei, that they may be modified by interactions within the IC, and that they may perform different spectrotemporal analyses of vocal signals.
Nataraj Kiran; Wenstrup Jeffrey J
Journal of neurophysiology
2006
2006-04
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/10.1152/jn.01148.2005" target="_blank" rel="noreferrer noopener">10.1152/jn.01148.2005</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>
Glycinergic inhibition creates a form of auditory spectral integration in nuclei of the lateral lemniscus.
Acoustic Stimulation; Action Potentials/drug effects; Animals; Auditory Perception/drug effects/*physiology; Bicuculline/pharmacology; Brain Stem/drug effects/*physiology; Chiroptera; GABA Antagonists/pharmacology; GABA-A Receptor Antagonists; GABA-A/metabolism; gamma-Aminobutyric Acid/metabolism; Glycine Agents/pharmacology; Glycine/*physiology; Glycine/antagonists & inhibitors/metabolism; Microelectrodes; Neural Inhibition/drug effects/*physiology; Neurons/drug effects/*physiology; Receptors; Strychnine/pharmacology
For analyses of complex sounds, many neurons integrate information across different spectral elements via suppressive effects that are distant from the neurons' excitatory tuning. In the mustached bat, suppression evoked by sounds within the first sonar harmonic (23-30 kHz) or in the subsonar band (\textless23 kHz) alters responsiveness to the higher best frequencies of many neurons. This study examined features and mechanisms associated with low-frequency (LF) suppression among neurons of the lateral lemniscal nuclei (NLL). We obtained extracellular recordings from neurons in the intermediate and ventral nuclei of the lateral lemniscus, observing different forms of LF suppression related to the two above-cited frequency bands. To understand the mechanisms underlying this suppression in NLL neurons, we examined the roles of glycinergic and GABAergic input through local microiontophoretic application of strychnine, an antagonist to glycine receptors (GlyRs), or bicuculline, an antagonist to gamma-aminobutyric acid type A receptors (GABA(A)Rs). With blockade of GABA(A)Rs, neurons showed an increase in firing rate to best frequency (BF) and/or LF tones but retained LF suppression of BF sounds. For neurons that displayed LF suppression tuned to
Peterson Diana Coomes; Nataraj Kiran; Wenstrup Jeffrey
Journal of neurophysiology
2009
2009-08
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.00040.2009" target="_blank" rel="noreferrer noopener">10.1152/jn.00040.2009</a>