Generators of the brainstem auditory evoked potential in cat III: identified cell populations

doi:10.1016/0378-5955(95)00200-6

Hearing Research

Volume 93, Issues 1–2, April 1996, Pages 52-71

https://doi.org/10.1016/0378-5955(95)00200-6 Get rights and content

Abstract

This paper examines the relationship between different brainstem cell populations and the brainstem auditory evoked potential (BAEP). First, we present a mathematical model relating the BAEP to underlying cellular activity. Then, we identify specific cellular generators of the click-evoked BAEP in cats by combining model-derived insights with key experimental data. These data include (a) a correspondence between particular brainstem regions and specific extrema inthe BAEP waveform, determined from lesion experiments, and (b) values for model parameters derived from published physiological and anatomical information. Ultimately, we conclude (with varying degrees of confidence) that: (1) the earliest extrema in the BAEP are generated by spiral ganglion cells, (2) P2 is mainly generated by cochlear nucleus (CN) globular cells, (3) P3 is partly generated by CN spherical cells and partly by cells receiving inputs from globular cells, (4) P4 is predominantly generated by medial superior olive (MSO) principal cells, which are driven by spherical cells, (5) the generators of P5 are driven by MSO principal cells, and (6) the BAEP, as a whole, is generated mainly by cells with characteristic frequencies above 2 kHz. Thus, the BAEP in cats mainly reflects cellular activity in two parallel pathways, one originating with globular cells and the other with spherical cells. Since the globular cell pathway is poorly represented in humans, we suggest that the human BAEP is largely generated by brainstem cells in the spherical cell pathway. Given our conclusions, it should now be possible to relate activity in specific cell populations to psychophysical performance since the BAEP can be recorded in behaving humans and animals.

References (110)

L.J. Achor et al.
Auditory brain stem responses in the rat. II. Effects of lesions
Electroenceph. clin. Neurophysiol.
(1980)
J.C. Adams et al.
Immunocytochemical evidence for inhibitory and disinhibitory circuits in the superior olive
Hear. Res.
(1990)
T.R. Bourk et al.
Tonotopic organization of the anteroventral cochlear nucleus of the cat
Hear. Res.
(1981)
W.E. Brownell
Organization of the cat trapezoid body and the discharge characteristics of its fibers
Brain. Res.
(1975)
W.E. Brownell et al.
Ipsilateral inhibitory responses in the cat lateral superior olive
Brain. Res.
(1979)
D.M. Caird et al.
The effect of inferior colliculus lesions on auditory evoked potentials
Electroenceph. clin. Neurophysiol.
(1987)
N.B. Cant et al.
Organization of the neurons in the anterior division of the anteroventral cochlear nucleus of the cat: light-microscopic observations
Neuroscience
(1979)
N.B. Cant
The fine structure of two types of stellate cells in the anterior division of the anteroventral cochlear nucleus of the cat
Neuroscience
(1981)
N.B. Cant et al.
Projections from the lateral nucleus of the trapezoid body to the medial superior olivary nucleus in the gerbil
Hear. Res.
(1992)
B.C. Fullerton et al.
Comparison of cat and human brain-stem auditory evoked potentials
Electroenceph. clin. Neurophysiol.
(1987)

B.F. Fullerton et al.

The effect of brainstem lesions on brainstem auditory evoked potentials in the cat

Hear. Res.

(1990)

J.J. Guinan et al.

Signal processing in brainstem auditory neurons which receive giant endings (calyces of Held) in the medial nucleus of the trapezoid body of the cat

Hear. Res.

(1990)

C.-M. Huang et al.

Factors that affect the amplitudes and latencies of the vertex short latency acoustic responses in the cat

Electroenceph. clin. Neurophysiol.

(1978)

D.L. Jewett

Volume-conducted potentials in response to auditory stimuli as detected by averaging in the cat

Electroenceph. clin. Neurophysiol.

(1970)

D. Johnson

The relationship of post-stimulus time and interval histograms to the timing characteristics of spike trains

Biophys. J.

(1978)

R.A. Levine et al.

Effects of multiple sclerosis brainstem lesions on sound lateralization and brainstem auditory evoked potentials

Hear. Res.

(1993)

J.R. Melcher et al.

Generators of the brainstem auditory evoked potential in cat. I. An experimental approach to their identification

Hear. Res.

(1996)

J.R. Melcher et al.

Generators of the brainstem auditory evoked potential in cat. II. Correlating lesion sites with waveform changes

Hear. Res.

(1996)

A.R. Møller et al.

Contributions from the auditory nerve to the brain-stem auditory evoked potentials (BAEPs): results of intracranial recording in man

Electroenceph. clin. Neurophysiol.

(1988)

D.K. Morest

The collateral system of the medial nucleus of the trapezoid body of the cat, its neuronal architecture and relation to the olivo-cochlear bundle

Brain Res.

(1968)

H. Pratt et al.

Effects of myelin or cell body brainstem lesions on 3-channel Lissajous' trajectroies of feline auditory brainstem evoked potentials

Hear. Res.

(1991)

R.L. Saint Marie et al.

Neurotransmitter-specific uptake and retrograde transport of [³H]glycine from the inferior colliculus by ipsilateral projections of the superior olivary complex and nuclei of the lateral lemniscus

Brain Res.

(1990)

R.L. Saint Marie et al.

Glycine immunoreactive projections from the dorsal to the anteroventral cochlear nucleus

Hear. Res.

(1991)

R.K. Shepherd et al.

Progressive ototoxicity of neomycin monitored using derived brainstem response audiometry

Hear. Res.

(1985)

D. Sontheimer et al.

Intra- and extracranially recorded auditory evoked potentials in the cat. II. Effects of interaural time and intensity differences

Electroenceph. clin. Neurophysiol.

(1985)

L.P. Tolbert et al.

The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: golgi and nissl methods

Neuroscience

(1982)

L.P. Tolbert et al.

The neuronal architecture of the anteroventral cochlear nucleus of the cat in the region of the cochlear nerve root: horseradish peroxidase labelling of identified cell types

Neuroscience

(1982)

A.L. Towe et al.

Extracellular microelectrode sampling bias

Exp. Neurol.

(1970)

S.-I. Wada et al.

Generation of auditory brain stem responses (ABRs). I. Effects of injection of a local anesthetic (procaine HCl) into the trapezoid body of guinea pigs and cat

Electroenceph. clin. Neurophysiol.

(1983)

S.-I. Wada et al.

Generation of auditory brain stem responses (ABRs). II. Effects of surgical section of the trapezoid body on the ABR in guinea pigs and cat

Electroenceph. clin. Neurophysiol.

(1983)

W.B. Warr

Fiber degeneration following lesions in the anterior ventral cochlear nucleus of the cat

Exp. Neurol.

(1966)

W.B. Warr

Fiber degeneration following lesions in the posteroventral cochlear nucleus of the cat

Exp. Neurol.

(1969)

J.C. Adams et al.

Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts

J. Comp. Neurol.

(1976)

J.C. Adams

Ascending projections to the inferior colliculus

J. Comp. Neurol.

(1979)

J.C. Adams et al.

Immunostaining of GABA-ergic and glycinergic inputs to the anteroventral cochlear nucleus

Soc. Neurosci. Abstr.

(1987)

F. Antoli-Candela et al.

Unit activity underlying the N1 potential

M.I. Banks et al.

Intracellular recordings from neurobiotin labeled cells in brain slices of the rat medial nucleus of the trapezoid body

J. Neurosci.

(1992)

T.R. Bourk

Electrical Responses of Neural Units in the Anteroventral Cochlear Nucleus of the Cat

J.R. Brawer et al.

The neuronal architecture of the cochlear nucleus of the cat

J. Comp. Neurol.

(1974)

R.H. Britt et al.

Neural generators of brainstem auditory evoked responses. I. Lesion studies

Soc. Neurosci. Abstr.

(1980)

J.S. Buchwald et al.

Far-field acoustic response: origins in the cat

Science

(1975)

R. Burkard et al.

The brain-stem auditory-evoked response in the big brown bat (Eptesicus fuscus) to clicks and frequency-modulated sweeps

J. Acoust. Soc. Am.

(1994)

N.B. Cant

The fine structure of the lateral superior olivary nucleus of the cat

J. Comp. Neurol.

(1984)

N.B. Cant et al.

Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei

J. Comp. Neurol.

(1986)

K.H. Chiappa

Evoked Potentials in Clinical Medicine

(1990)

J.T. Coyle et al.

In situ injection of kainic acid: a new method for selectively lesioning neuronal cell bodies while sparing axons of passage

J. Comp. Neurol.

(1978)

H.H. Elverland

Ascending and intrinsic projection of the superior olivary complex in the cat

Exp. Brain Res.

(1978)

R.R. Fay

A.S. Feng et al.

Functional organization of the cochlear nucleus of rufous horseshoe bats (rhinolophus rouxi): frequencies and internal connections are arranged in slabs

J. Comp. Neurol.

(1985)

C. Fernandez et al.

The course and termination of the striae of Monakow and Held in the cat

J. Comp. Neurol.

(1967)

Cited by (197)

Mechanisms of age-related hearing loss at the auditory nerve central synapses and postsynaptic neurons in the cochlear nucleus
2024, Hearing Research
Sound information is transduced from mechanical vibration to electrical signals in the cochlea, conveyed to and further processed in the brain to form auditory perception. During the process, spiral ganglion neurons (SGNs) are the key cells that connect the peripheral and central auditory systems by receiving information from hair cells in the cochlea and transmitting it to neurons of the cochlear nucleus (CN). Decades of research in the cochlea greatly improved our understanding of SGN function under normal and pathological conditions, especially about the roles of different subtypes of SGNs and their peripheral synapses. However, it remains less clear how SGN central terminals or auditory nerve (AN) synapses connect to CN neurons, and ultimately how peripheral pathology links to structural alterations and functional deficits in the central auditory nervous system. This review discusses recent progress about the morphological and physiological properties of different subtypes of AN synapses and associated postsynaptic CN neurons, their changes during aging, and the potential mechanisms underlying age-related hearing loss.
Sound elicits stereotyped facial movements that provide a sensitive index of hearing abilities in mice
2024, Current Biology
Sound elicits rapid movements of muscles in the face, ears, and eyes that protect the body from injury and trigger brain-wide internal state changes. Here, we performed quantitative facial videography from mice resting atop a piezoelectric force plate and observed that broadband sounds elicited rapid and stereotyped facial twitches. Facial motion energy (FME) adjacent to the whisker array was 30 dB more sensitive than the acoustic startle reflex and offered greater inter-trial and inter-animal reliability than sound-evoked pupil dilations or movement of other facial and body regions. FME tracked the low-frequency envelope of broadband sounds, providing a means to study behavioral discrimination of complex auditory stimuli, such as speech phonemes in noise. Approximately 25% of layer 5–6 units in the auditory cortex (ACtx) exhibited firing rate changes during facial movements. However, FME facilitation during ACtx photoinhibition indicated that sound-evoked facial movements were mediated by a midbrain pathway and modulated by descending corticofugal input. FME and auditory brainstem response (ABR) thresholds were closely aligned after noise-induced sensorineural hearing loss, yet FME growth slopes were disproportionately steep at spared frequencies, reflecting a central plasticity that matched commensurate changes in ABR wave 4. Sound-evoked facial movements were also hypersensitive in Ptchd1 knockout mice, highlighting the use of FME for identifying sensory hyper-reactivity phenotypes after adult-onset hyperacusis and inherited deficiencies in autism risk genes. These findings present a sensitive and integrative measure of hearing while also highlighting that even low-intensity broadband sounds can elicit a complex mixture of auditory, motor, and reafferent somatosensory neural activity.
Auditory brainstem response (ABR) waveform analysis program
2023, MethodsX
Auditory brainstem responses (ABR) are a high-throughput assessment of auditory function. Many studies determine changes to the threshold at frequencies that span the normal hearing range of their test subjects, but fewer studies evaluate changes in waveform morphology. The goal of developing this program was to make a user-friendly semiautomatic peak-detection algorithm to encourage widespread analysis of the amplitudes and latencies of the ABR, which may yield informative details about the integrity of the auditory system with development, aging, genetic manipulations, or damaging conditions. This method incorporates automated peak detection with manual override and inter-rater validation to calculate the amplitude and latency for waves 1–5, as well as interpeak latencies and amplitude ratios between waves. The output includes raw data and calculations in a format compatible with graphical and statistical software.
- •
  The method yields a high-throughput peak-detection algorithm with manual override and inter-rater capabilities to streamline ABR waveform analysis.
- •
  Data output includes amplitudes, latencies, amplitude ratios, and interpeak latencies for generation of input-output curves.
- •
  While complete automation of peak detection with this tool is dependent on good signal-to-noise ratios, relevant amplitude and latency calculations are fully automated, and manual spot-checking is simplified to significantly reduce the time to analyze waveforms.
Runx1 controls auditory sensory neuron diversity in mice
2023, Developmental Cell
Sound stimulus is encoded in mice by three molecularly and physiologically diverse subtypes of sensory neurons, called Ia, Ib, and Ic spiral ganglion neurons (SGNs). Here, we show that the transcription factor Runx1 controls SGN subtype composition in the murine cochlea. Runx1 is enriched in Ib/Ic precursors by late embryogenesis. Upon the loss of Runx1 from embryonic SGNs, more SGNs take on Ia rather than Ib or Ic identities. This conversion was more complete for genes linked to neuronal function than to connectivity. Accordingly, synapses in the Ib/Ic location acquired Ia properties. Suprathreshold SGN responses to sound were enhanced in Runx1^CKO mice, confirming the expansion of neurons with Ia-like functional properties. Runx1 deletion after birth also redirected Ib/Ic SGNs toward Ia identity, indicating that SGN identities are plastic postnatally. Altogether, these findings show that diverse neuronal identities essential for normal auditory stimulus coding arise hierarchically and remain malleable during postnatal development.
Role of GluA4 in the acoustic and tactile startle responses
2022, Hearing Research
The primary startle response (SR) is an innate reaction evoked by sudden and intense acoustic, tactile or visual stimuli. In rodents and humans the SR involves reflexive contractions of the face, neck and limb muscles. The acoustic startle response (ASR) pathway consists of auditory nerve fibers (AN), cochlear root neurons (CRNs) and giant neurons of the caudal pontine reticular nucleus (PnC), which synapse on cranial and spinal motor neurons. The tactile startle response (TSR) is transmitted by primary sensory neurons to the principal sensory (Pr5) and spinal (Sp5) trigeminal nuclei. The ventral part of Pr5 projects directly to the PnC neurons. The SR requires rapid transmission of sensory information to initiate a fast motor response. Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors (AMPAR) are necessary to transmit auditory information to the PnC neurons and elicit the SR. AMPARs containing the glutamate AMPAR subunit 4 (GluA4) have fast kinetics, which makes them ideal candidates to transmit the SR signal. This study examined the role of GluA4 within the primary SR pathway by using GluA4 knockout (GluA4-KO) mice. Deletion of GluA4 considerably decreased the amplitude and probability of successful ASR and TSR, indicating that the presence of this subunit is critical at a common station within the startle pathway. We conclude that deletion of GluA4 affects the transmission of sensory signals from acoustic and tactile pathways to the motor component of the startle reflex. Therefore, GluA4 is required for the full response and for reliable elicitation of the startle response.
Auditory brainstem response test results in normal hearing adolescents with subjective tinnitus
2021, International Journal of Pediatric Otorhinolaryngology
Citation Excerpt :
Current studies on adolescents with tinnitus have focused more on risk factors, prevalence, and characteristics of tinnitus or the effect of tinnitus on psychomotor symptoms [8–11]. Meanwhile, the auditory brainstem response (ABR) test measures acoustically stimulated signals that represent activation of neural pathways between the cochlear nerve and up to the inferior colliculus of the midbrain [12]. Individuals with normal hearing thresholds in conventional pure tone audiometry (PTA) may show abnormal findings in ABR, such as delayed latency or smaller amplitudes.
The objective of the study was to analyze the auditory brainstem response (ABR) test results of adolescents with normal hearing threshold who have subjective tinnitus in an effort to determine the probable site of origin of tinnitus.
Among the patients who visited the outpatient clinic of the Department of Otolaryngology at our tertiary hospital from January 2016 to December 2019, adolescents aged 13–18 years with the chief complaint of unilateral subjective tinnitus and pure tone audiometry (PTA) within 25 dB HL were enrolled and retrospectively reviewed. The ABR test parameters (amplitudes and latencies of waves I, III, and V and interpeak latencies [IPLs] of waves I–III, III–V, and I–V) were analyzed and compared between tinnitus ears and contralateral ears without tinnitus. Study participants were divided into the chronic tinnitus (tinnitus duration ≥6 months) and non-chronic tinnitus (tinnitus duration <6 months) groups, and the difference between the two groups was analyzed.
Ten adolescents were included in the study, and their ABR test results were reviewed. IPL III–V was significantly prolonged in tinnitus ears compared to non-tinnitus ears (p = 0.035). Although other parameters were found to be statistically non-significant, there was preponderance in ABR wave I amplitude; it was smaller in tinnitus ears of chronic tinnitus adolescents than in those of non-chronic tinnitus adolescents (p = 0.114).
The probable site of origin of tinnitus in adolescents with normal hearing might be in the upper brainstem of the auditory pathway. Further analysis of ABR test results in adolescents with tinnitus and normal hearing can help clarify the pathophysiology of tinnitus in adolescents.

View all citing articles on Scopus

^☆: Portions of this work were presented at the annual meeting of the Society for Neuroscience (1990), at the annual midwinter meeting of the Association for Research in Otolaryngology (1993), and in J.R.M.'s doctoral thesis (Massachusetts Institute of Technology, 1993).

View full text

Research paperGenerators of the brainstem auditory evoked potential in cat III: identified cell populations☆

Abstract

Electroenceph. clin. Neurophysiol.

Hear. Res.

Hear. Res.

Brain. Res.

Brain. Res.

Electroenceph. clin. Neurophysiol.

Neuroscience

Neuroscience

Hear. Res.

Electroenceph. clin. Neurophysiol.

Hear. Res.

Hear. Res.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Biophys. J.

Hear. Res.

Hear. Res.

Hear. Res.

Electroenceph. clin. Neurophysiol.

Brain Res.

Hear. Res.

Brain Res.

Hear. Res.

Hear. Res.

Electroenceph. clin. Neurophysiol.

Neuroscience

Neuroscience

Exp. Neurol.

Electroenceph. clin. Neurophysiol.

Electroenceph. clin. Neurophysiol.

Exp. Neurol.

Exp. Neurol.

Origins of axons in the cat's acoustic striae determined by injection of horseradish peroxidase into severed tracts

J. Comp. Neurol.

Ascending projections to the inferior colliculus

J. Comp. Neurol.

Immunostaining of GABA-ergic and glycinergic inputs to the anteroventral cochlear nucleus

Soc. Neurosci. Abstr.

Unit activity underlying the N1 potential

Intracellular recordings from neurobiotin labeled cells in brain slices of the rat medial nucleus of the trapezoid body

J. Neurosci.

Electrical Responses of Neural Units in the Anteroventral Cochlear Nucleus of the Cat

The neuronal architecture of the cochlear nucleus of the cat

J. Comp. Neurol.

Neural generators of brainstem auditory evoked responses. I. Lesion studies

Soc. Neurosci. Abstr.

Far-field acoustic response: origins in the cat

Science

The brain-stem auditory-evoked response in the big brown bat (Eptesicus fuscus) to clicks and frequency-modulated sweeps

J. Acoust. Soc. Am.

The fine structure of the lateral superior olivary nucleus of the cat

J. Comp. Neurol.

Projections from the anteroventral cochlear nucleus to the lateral and medial superior olivary nuclei

J. Comp. Neurol.

Evoked Potentials in Clinical Medicine

In situ injection of kainic acid: a new method for selectively lesioning neuronal cell bodies while sparing axons of passage

J. Comp. Neurol.

Ascending and intrinsic projection of the superior olivary complex in the cat

Exp. Brain Res.

Functional organization of the cochlear nucleus of rufous horseshoe bats (rhinolophus rouxi): frequencies and internal connections are arranged in slabs

J. Comp. Neurol.

The course and termination of the striae of Monakow and Held in the cat

J. Comp. Neurol.

Research paper
Generators of the brainstem auditory evoked potential in cat III: identified cell populations☆