Development of Sound Localization Mechanisms in the Mongolian Gerbil Is Shaped by Early Acoustic Experience

2005 ◽  
Vol 94 (2) ◽  
pp. 1028-1036 ◽  
Author(s):  
Armin H. Seidl ◽  
Benedikt Grothe
Keyword(s):  
Brain Stem ◽  
Sound Localization ◽  
Low Frequency ◽  
Mammalian Brain ◽  
Medial Superior Olive ◽  
Visual Inputs ◽  
Auditory Brain Stem ◽  
Barn Owls ◽  
Neuronal Representation ◽  
Acoustic Experience

Sound localization is one of the most important tasks performed by the auditory system. Differences in the arrival time of sound at the two ears are the main cue to localize low-frequency sound in the azimuth. In the mammalian brain, such interaural time differences (ITDs) are encoded in the auditory brain stem; first by the medial superior olive (MSO) and then transferred to higher centers, such as the dorsal nucleus of the lateral lemniscus (DNLL), a brain stem nucleus that gets a direct input from the MSO. Here we demonstrate for the first time that ITD sensitivity in gerbils undergoes a developmental maturation after hearing onset. We further show that this development can be disrupted by altering the animal's acoustic experience during a critical period. In animals that had been exposed to omnidirectional white noise during a restricted time period right after hearing onset, ITD tuning did not develop normally. Instead, it was similar to that of juvenile animals 3 days after hearing onset, with the ITD functions not adjusted to the physiological range. Animals that had been exposed to omnidirectional noise as adults did not show equivalent abnormal ITD tuning. The development presented here is in contrast to that of the development of neuronal representation of ITDs in the midbrain of barn owls and interaural intensity differences in ferrets, where the representations are adjusted by an interaction of auditory and visual inputs. The development of ITD tuning presented here most likely depends on normal acoustic experience and may be related to the maturation of inhibitory inputs to the ITD detector itself.

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.

Midline and lateral field sound localization in the ferret (Mustela putorius): contribution of the superior olivary complex

1992 ◽  
Vol 67 (6) ◽  
pp. 1643-1658 ◽  
Author(s):  
G. L. Kavanagh ◽  
J. B. Kelly
Keyword(s):  
Brain Stem ◽  
Kainic Acid ◽  
Sound Localization ◽  
Retrograde Transport ◽  
Superior Olivary Complex ◽  
Motor Impairments ◽  
Lateral Field ◽  
Superior Olive ◽  
Auditory Brain Stem ◽  
Bilateral Lesions

1. The ability of ferrets to localize sound in space was determined before and after unilateral or bilateral lesions of the superior olivary complex (SOC). Lesions were made by pressure injection of kainic acid into the SOC through a stereotaxically positioned glass micropipette. The lesions destroyed the cell bodies in the superior olive without disrupting fibers of passage in the trapezoid body or other pathways in the auditory brain stem. The integrity of fibers was demonstrated by protargol staining of axonal processes and by the retrograde transport of horseradish peroxidase (HRP) from the inferior colliculus to other auditory brain stem nuclei. Behavioral tests were carried out separately for sound localization at midline and lateral field positions. Minimum audible angles were determined for single 45-ms noise bursts presented through paired loudspeakers positioned symmetrically around 0, -60, and +60 degrees azimuth. 2. Four ferrets received complete lesions of the left SOC, and two received complete lesions of the right SOC. In general, unilateral destruction of the superior olive resulted in impairments in sound localization in both left and right lateral fields. In some cases, deficits were also apparent on midline. Four additional animals received unilateral lesions that spared cells within the SOC. In most cases, deficits were apparent despite incomplete lesions of the SOC. The pattern of deficits was generally consistent with that found in animals with complete lesions. Most animals had difficulty localizing sounds in the lateral fields. 3. Four animals received bilateral lesions of the SOC. Three had complete or near-complete destruction of the superior olive on one side of the brain with relatively minor damage on the other side. Each of these animals exhibited behavioral deficits that were particularly severe ipsilateral to the more extensively damaged superior olive. One animal with complete bilateral destruction of the SOC was incapable of sound localization, even with 2-s noise bursts. This animal, however, suffered severe motor impairments after surgery that might have contributed to the apparent inability to localize sound. 4. Two animals with kainic acid lesions that caused little or no damage to the SOC were still capable of high levels of performance in tests of sound localization and had no elevation in minimum audible angles. These cases served as controls for the possible effects of nonspecific brain damage and demonstrated that kainic acid injections per se resulted in no obvious deficits in our test situation.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Neuronal coupling by endogenous electric fields: cable theory and applications to coincidence detector neurons in the auditory brain stem

2016 ◽  
Vol 115 (4) ◽  
pp. 2033-2051 ◽  
Author(s):  
Joshua H. Goldwyn ◽  
John Rinzel
Keyword(s):  
Membrane Potential ◽  
Brain Stem ◽  
Coincidence Detection ◽  
Neural Population ◽  
Medial Superior Olive ◽  
Cable Theory ◽  
Auditory Brain Stem ◽  
Neuronal Computation ◽  
Ephaptic Coupling

The ongoing activity of neurons generates a spatially and time-varying field of extracellular voltage ( Ve). This Ve field reflects population-level neural activity, but does it modulate neural dynamics and the function of neural circuits? We provide a cable theory framework to study how a bundle of model neurons generates Ve and how this Ve feeds back and influences membrane potential ( Vm). We find that these “ephaptic interactions” are small but not negligible. The model neural population can generate Ve with millivolt-scale amplitude, and this Ve perturbs the Vm of “nearby” cables and effectively increases their electrotonic length. After using passive cable theory to systematically study ephaptic coupling, we explore a test case: the medial superior olive (MSO) in the auditory brain stem. The MSO is a possible locus of ephaptic interactions: sounds evoke large (millivolt scale) Ve in vivo in this nucleus. The Ve response is thought to be generated by MSO neurons that perform a known neuronal computation with submillisecond temporal precision (coincidence detection to encode sound source location). Using a biophysically based model of MSO neurons, we find millivolt-scale ephaptic interactions consistent with the passive cable theory results. These subtle membrane potential perturbations induce changes in spike initiation threshold, spike time synchrony, and time difference sensitivity. These results suggest that ephaptic coupling may influence MSO function.

scholarly journals Physiology and anatomy of neurons in the medial superior olive of the mouse

2016 ◽  
Vol 116 (6) ◽  
pp. 2676-2688 ◽  
Author(s):  
Matthew J. Fischl ◽  
R. Michael Burger ◽  
Myriam Schmidt-Pauly ◽  
Olga Alexandrova ◽  
James L. Sinclair ◽  
...  
Keyword(s):  
Sound Localization ◽  
Molecular Mechanisms ◽  
Low Frequency ◽  
Acoustic Stimulation ◽  
Medial Superior Olive ◽  
Temporal Acuity ◽  
Low Frequencies ◽  
Superior Olive

In mammals with good low-frequency hearing, the medial superior olive (MSO) computes sound location by comparing differences in the arrival time of a sound at each ear, called interaural time disparities (ITDs). Low-frequency sounds are not reflected by the head, and therefore level differences and spectral cues are minimal or absent, leaving ITDs as the only cue for sound localization. Although mammals with high-frequency hearing and small heads (e.g., bats, mice) barely experience ITDs, the MSO is still present in these animals. Yet, aside from studies in specialized bats, in which the MSO appears to serve functions other than ITD processing, it has not been studied in small mammals that do not hear low frequencies. Here we describe neurons in the mouse brain stem that share prominent anatomical, morphological, and physiological properties with the MSO in species known to use ITDs for sound localization. However, these neurons also deviate in some important aspects from the typical MSO, including a less refined arrangement of cell bodies, dendrites, and synaptic inputs. In vitro, the vast majority of neurons exhibited a single, onset action potential in response to suprathreshold depolarization. This spiking pattern is typical of MSO neurons in other species and is generated from a complement of Kv1, Kv3, and IH currents. In vivo, mouse MSO neurons show bilateral excitatory and inhibitory tuning as well as an improvement in temporal acuity of spiking during bilateral acoustic stimulation. The combination of classical MSO features like those observed in gerbils with more unique features similar to those observed in bats and opossums make the mouse MSO an interesting model for exploiting genetic tools to test hypotheses about the molecular mechanisms and evolution of ITD processing.

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.

scholarly journals Stochastic Model Explains the Role of Excitation and Inhibition in Binaural Sound Localization in Mammals

2011 ◽  
pp. 573-583 ◽  
Author(s):  
M. DRAPAL ◽  
P. MARSALEK
Keyword(s):  
Sound Localization ◽  
Arrival Time ◽  
Neural Circuit ◽  
Low Frequency ◽  
Spike Timing ◽  
Inhibitory Input ◽  
Medial Superior Olive ◽  
Interaural Time Differences ◽  
Stochastic Description

Interaural time differences (ITDs), the differences of arrival time of the sound at the two ears, provide a major cue for low-frequency sound localization in the horizontal plane. The first nucleus involved in the computation of ITDs is the medial superior olive (MSO). We have modeled the neural circuit of the MSO using a stochastic description of spike timing. The inputs to the circuit are stochastic spike trains with a spike timing distribution described by a given probability density function (beta density). The outputs of the circuit reproduce the empirical firing rates found in experiment in response to the varying ITD. The outputs of the computational model are calculated numerically and these numerical simulations are also supported by analytical calculations. We formulate a simple hypothesis concerning how sound localization works in mammals. According to this hypothesis, there is no array of delay lines as in the Jeffress’ model, but the inhibitory input is shifted in time as a whole. This is consistent with experimental observations in mammals.

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