Roles of Inhibition in Creating Complex Auditory Responses in the Inferior Colliculus: Facilitated Combination-Sensitive Neurons

2005 ◽  
Vol 93 (6) ◽  
pp. 3294-3312 ◽  
Author(s):  
Kiran Nataraj ◽  
Jeffrey J. Wenstrup
Keyword(s):  
Brain Stem ◽  
Inferior Colliculus ◽  
Low Frequency ◽  
Auditory Responses ◽  
Auditory Brain Stem ◽  
Neural Interactions ◽  
Lower Brain Stem ◽  
Excitatory Responses ◽  
Sonar Echoes ◽  
Inhibitory Interactions

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 γ-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.

scholarly journals Temporal Features of Spectral Integration in the Inferior Colliculus: Effects of Stimulus Duration and Rise Time

2009 ◽  
Vol 102 (1) ◽  
pp. 167-180 ◽  
Author(s):  
Donald Gans ◽  
Kianoush Sheykholeslami ◽  
Diana Coomes Peterson ◽  
Jeffrey Wenstrup
Keyword(s):  
Inferior Colliculus ◽  
Rise Time ◽  
Low Frequency ◽  
Auditory Pathway ◽  
Spectral Integration ◽  
Auditory Responses ◽  
Temporal Features ◽  
Vocal Signals ◽  
Inhibitory Interactions ◽  
Different Levels

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 <23 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.

Influence of cold and warm acclimation on neuronal responses in the lower brain stem

1987 ◽  
Vol 65 (6) ◽  
pp. 1281-1289 ◽  
Author(s):  
P. Hinckel ◽  
W. T. Perschel
Keyword(s):  
Brain Stem ◽  
Guinea Pigs ◽  
Metabolic Activation ◽  
Maximum Activity ◽  
Descending Pathways ◽  
Nucleus Raphe Magnus ◽  
Average Maximum ◽  
Raphe Magnus ◽  
Lower Brain Stem ◽  
Excitatory Responses

Neurons in two lower brain stem areas, the nucleus raphe magnus and the subcoeruleus region, have been shown to be part of the thermoafferent system. It is concluded from microcut experiments in unanaesthetized guinea pigs that inhibition of shivering caused by nucleus raphe magnus stimulation is mediated partly by ascending and partly by descending efferents of the nucleus raphe magnus. Electrical stimulation of the subcoeruleus area caused excitatory metabolic responses. Interruption of the ascending efferents of the subcoeruleus area did not prevent the metabolic activation. It is concluded that the excitatory responses are partly mediated by descending efferents of the subcoeruleus area. The descending pathways project mainly to motoneurone pools and to dorsal horn cells. In cold-acclimated guinea pigs, the average maximum activity of bell-shaped subcoeruleus cold-responsive units was reduced significantly in comparison with cold-responsive neurons in animals acclimated to normal room temperature. Furthermore, peak activity of warm-responsive units in the nucleus raphe magnus was larger in cold-acclimated animals than in animals acclimated to normal room termperature. These neuronal changes may contribute via descending lower loops and via ascending upper loops to long-term slope reduction of metabolic cold defence and shivering threshold displacements.

Effects of intracochlear factors on spiral ganglion cells and auditory brain stem response after long-term electrical stimulation in deafened kittens

2000 ◽  
Vol 122 (3) ◽  
pp. 425-433
Author(s):  
Eugene N. Myers ◽  
Susumu Araki ◽  
Atsushi Kawano ◽  
H. Lee Seldon ◽  
Robert K. Shepherd ◽  
...  
Keyword(s):  
Brain Stem ◽  
Inferior Colliculus ◽  
Negative Correlation ◽  
Volume Fraction ◽  
Spiral Ganglion ◽  
Organ Of Corti ◽  
Scala Tympani ◽  
Auditory Brain Stem Response ◽  
Spiral Ganglion Cell ◽  
Auditory Brain Stem

Using an animal model, we have studied the response of the auditory brain stem to cochlear implantation and the effect of intracochlear factors on this response. Neonatally, pharmacologically deafened cats (100 to more than 180 days old) were implanted with a 4-electrode array in both cochleas. Then, the left cochlea of each cat was electrically stimulated for total periods of up to 1000 hours. After a terminal 14C-2-deoxyglucose (2DG) experiment, the fraction of the right inferior colliculus with a significant accumulation of 2DG label was calculated. Using 3-dimensional computer-aided reconstruction, we examined the cochleas of these animals for spiral ganglion cell (SGC) survival and intracochlear factors such as electrode positions, degeneration of the organ of Corti, and the degree of fibrosis of the scala tympani. The distribution of each parameter was calculated along the organ of Corti from the basal end. There was a positive correlation between SGC survival and the level of fibrosis in the scala tympani, and a negative correlation between SGC survival and the degree of organ of Corti degeneration. Finally, there was a negative correlation between the 2DG-labeled inferior colliculus volume fraction and the degree of fibrosis, particularly in the 1-mm region nearest the pair of electrodes, and presumably in the basal turn.

An in vivo investigation of inferior colliculus single neuron responses to cochlear nucleus pulse train stimulation

2012 ◽  
Vol 108 (11) ◽  
pp. 2999-3008 ◽  
Author(s):  
Stefan J. Mauger ◽  
Mohit N. Shivdasani ◽  
Graeme D. Rathbone ◽  
Antonio G. Paolini
Keyword(s):  
Speech Perception ◽  
Brain Stem ◽  
Inferior Colliculus ◽  
Cochlear Nucleus ◽  
Acoustic Stimulation ◽  
Neural Firing ◽  
Response Properties ◽  
Stimulus Rate ◽  
Auditory Brain Stem

The auditory brain stem implant (ABI) is being used clinically to restore hearing to patients unable to benefit from a cochlear implant (CI). Speech perception outcomes for ABI users are typically poor compared with most CI users. The ABI is implanted either on the surface of or penetrating through the cochlear nucleus in the auditory brain stem and uses stimulation strategies developed for auditory nerve stimulation with a CI. Although the stimulus rate may affect speech perception outcomes with current stimulation strategies, no studies have systematically investigated the effect of stimulus rate electrophysiologically or clinically. We therefore investigated rate response properties and temporal response properties of single inferior colliculus (IC) neurons from penetrating ABI stimulation using stimulus rates ranging from 100 to 1,600 pulses/s in the rat. We found that the stimulus rate affected the proportion of response types, thresholds, and dynamic ranges of IC activation. The stimulus rate was also found to affect the temporal properties of IC responses, with higher rates providing more temporally similar responses to acoustic stimulation. Suppression of neural firing and inhibition in IC neurons was also found, with response properties varying with the stimulus rate. This study demonstrated that changes in the ABI stimulus rate results in significant differences in IC neuron response properties. Due to electrophysiological differences, the stimulus rate may also change perceptual properties. We suggest that clinical evaluation of the ABI stimulus rate should be performed.

scholarly journals Roles of Inhibition in Complex Auditory Responses in the Inferior Colliculus: Inhibited Combination-Sensitive Neurons

2006 ◽  
Vol 95 (4) ◽  
pp. 2179-2192 ◽  
Author(s):  
Kiran Nataraj ◽  
Jeffrey J. Wenstrup
Keyword(s):  
Inferior Colliculus ◽  
Low Frequency ◽  
Neural Mechanisms ◽  
The Other ◽  
Inhibitory Neurons ◽  
Type I ◽  
Excitatory Response ◽  
Frequency Responses ◽  
Auditory Responses ◽  
Vocal Signals

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.

scholarly journals Systematic mapping of the monkey inferior colliculus reveals enhanced low frequency sound representation

2011 ◽  
Vol 105 (4) ◽  
pp. 1785-1797 ◽  
Author(s):  
David A. Bulkin ◽  
Jennifer M. Groh
Keyword(s):  
Inferior Colliculus ◽  
Rhesus Monkeys ◽  
Rhesus Macaques ◽  
Low Frequency ◽  
Large Mass ◽  
Surrounding Tissue ◽  
Systematic Mapping ◽  
Prosthetic Devices ◽  
Auditory Responses ◽  
Tonal Stimuli

We investigated the functional architecture of the inferior colliculus (IC) in rhesus monkeys. We systematically mapped multiunit responses to tonal stimuli and noise in the IC and surrounding tissue of six rhesus macaques, collecting data at evenly placed locations and recording nonresponsive locations to define boundaries. The results show a modest tonotopically organized region (17 of 100 recording penetration locations in 4 of 6 monkeys) surrounded by a large mass of tissue that, although vigorously responsive, showed no clear topographic arrangement (68 of 100 penetration locations). Rather, most cells in these recordings responded best to frequencies at the low end of the macaque auditory range. The remaining 15 (of 100) locations exhibited auditory responses that were not sensitive to sound frequency. Potential anatomical correlates of functionally defined regions and implications for midbrain auditory prosthetic devices are discussed.

scholarly journals Activity-dependent formation and location of voltage-gated sodium channel clusters at a CNS nerve terminal during postnatal development

2017 ◽  
Vol 117 (2) ◽  
pp. 582-593 ◽  
Author(s):  
Jie Xu ◽  
Emmanuelle Berret ◽  
Jun Hee Kim
Keyword(s):  
Brain Stem ◽  
Nerve Terminal ◽  
Low Frequency ◽  
Presynaptic Terminal ◽  
Scaffolding Protein ◽  
Unmyelinated Axon ◽  
Voltage Gated ◽  
Medial Nucleus ◽  
Auditory Brain Stem ◽  
Activity Dependent

In auditory pathways, the precision of action potential (AP) propagation depends on axon myelination and high densities of voltage-gated Na (Nav) channels clustered at nodes of Ranvier. Changes in Nav channel expression at the heminode, the final node before the nerve terminal, can alter AP invasion into the presynaptic terminal. We studied the activity-dependent formation of Nav channel clusters before and after hearing onset at postnatal day 12 in the rat and mouse auditory brain stem. In rats, the Nav channel cluster at the heminode formed progressively during the second postnatal week, around hearing onset, whereas the Nav channel cluster at the nodes was present before hearing onset. Initiation of heminodal Nav channel clustering was correlated with the expression of scaffolding protein ankyrinG and paranodal protein Caspr. However, in whirler mice with congenital deafness, heminodal Nav channels did not form clusters and maintained broad expression, but Nav channel clustering was normal at the nodes. In addition, a clear difference in the distance from the heminodal Nav channel to the calyx across the mediolateral axis of the medial nucleus of the trapezoid body (MNTB) developed after hearing onset. In the medial MNTB, where neurons respond best to high-frequency sounds, the heminodal Nav channel cluster was located closer to the terminal than in the lateral MNTB, where neurons respond best to low-frequency sounds. Thus sound-mediated neuronal activities are potentially associated with the refinement of the heminode adjacent to the presynaptic terminal in the auditory brain stem. NEW & NOTEWORTHY Clustering of voltage-gated sodium (Nav) channels and their distribution along the axon, specifically at the unmyelinated axon segment next to the nerve terminal, are essential for tuning propagated action potentials. Nav channel clusters near the nerve terminal and their location as a function of neuronal position along the mediolateral axis are controlled by auditory inputs after hearing onset. Thus sound-mediated neuronal activity influences the tonotopic organization of Nav channels at the nerve terminal in the auditory brain stem.

Acute intracranial hypertension and auditory brain-stem responses

1979 ◽  
Vol 51 (6) ◽  
pp. 846-851 ◽  
Author(s):  
Seigo Nagao ◽  
Peter Roccaforte ◽  
Robert A. Moody
Keyword(s):  
Brain Stem ◽  
Inferior Colliculus ◽  
Complete Suppression ◽  
Content Type ◽  
Transtentorial Herniation ◽  
Auditory Brain Stem Responses ◽  
Auditory Brain Stem ◽  
The Brain ◽  
Marked Suppression

✓ Movement of the upper brain stem (inferior colliculus) was correlated with the alterations in the amplitude of wave V of the auditory brain-stem responses (BER's) during supratentorial brain compression in cats. In vivo observation of the brain stem and postmortem inspection show that suppression of the amplitude of BER wave V reflects the extent of caudal displacement of the inferior colliculus. Marked suppression of the amplitude of BER wave V (approximately 30% of control) correlates with the beginning of transtentorial herniation, and complete suppression of the wave V indicates complete transtentorial herniation of the brain-stem and supratentorial structures. The BER wave V is thought to be a sensitive index of caudal movement of the upper brain stem due to transtentorial herniation.

Acute intracranial hypertension and auditory brain-stem responses

1980 ◽  
Vol 52 (3) ◽  
pp. 351-358 ◽  
Author(s):  
Seigo Nagao ◽  
Peter Roccaforte ◽  
Robert A. Moody
Keyword(s):  
Brain Stem ◽  
Posterior Fossa ◽  
Systemic Blood Pressure ◽  
Postmortem Brain ◽  
Content Type ◽  
Transtentorial Herniation ◽  
Auditory Brain Stem Responses ◽  
Auditory Brain Stem ◽  
Lower Brain Stem

✓ The auditory brain-stem responses (BER's), infratentorial intracranial pressure (ICP), systemic blood pressure (BP), and heart rate were recorded before, during and after expansion of an infratentorial epidural mass in anesthetized cats. Two types of BER's to increasing posterior fossa pressure were noted. In Type 1, there was predominantly suppression of the electrical activity of the auditory nuclei of the upper brain stem (Waves V and IV) and upward transtentorial herniation of the midbrain. In Type 2, the neural activity of the lower brain-stem nuclei (Waves III and II) was affected as well as that of the upper brain stem. There was upward and foraminal impaction of the brain stem and cerebellum which was confirmed by the postmortem brain sections. The change in the amplitudes of BER Waves V and III proved useful in detecting upward transtentorial herniation of the midbrain and foraminal herniation of the cerebellum in acute expanding lesions of the posterior fossa. Medullary paralysis was also detected by observing Wave III.

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