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>
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>