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S E Shore

Publications and source records attributed to S E Shore.

18 recordsLinked to original sources

Multisensory integration in the dorsal cochlear nucleus: unit responses to acoustic and trigeminal ganglion stimulation.

A necessary requirement for multisensory integration is the convergence of pathways from different senses. The dorsal cochlear nucleus (DCN) receives auditory input directly via the VIIIth nerve and somatosensory input indirectly from the Vth nerve via granule cells. Multisensory integration may occur in DCN cells that receive both trigeminal and auditory nerve input, such as the fusiform cell. We investigated trigeminal system influences on guinea pig DCN cells by stimulating the trigeminal ganglion while recording spontaneous and sound-driven activity from DCN neurons. A bipolar stimulating electrode was placed into the trigeminal ganglion of anesthetized guinea pigs using stereotaxic co-ordinates. Electrical stimuli were applied as bipolar pulses (100 micros per phase) with amplitudes ranging from 10 to 100 microA. Responses from DCN units were obtained using a 16-channel, four-shank electrode. Current pulses were presented alone or preceding 100- or 200-ms broadband noise (BBN) bursts. Thirty percent of DCN units showed either excitatory, inhibitory or excitatory-inhibitory responses to trigeminal ganglion stimulation. When paired with BBN stimulation, trigeminal stimulation suppressed or facilitated the firing rate in response to BBN in 78% of units, reflecting multisensory integration. Pulses preceding the acoustic stimuli by as much as 95 ms were able to alter responses to BBN. Bimodal suppression may play a role in attenuating body-generated sounds, such as vocalization or respiration, whereas bimodal enhancement may serve to direct attention in low signal-to-noise environments.

Acoustic Stimulation↗

Spatial representation of corticofugal input in the inferior colliculus: a multicontact silicon probe approach.

The inferior colliculus (IC) is a well-established target of descending projections from the auditory cortex (AC). However, our understanding of these pathways has been limited by an incomplete picture of their functional influence within the three-dimensional space of the IC. Our goal was to study the properties and spatial representation of corticofugal input in the IC of guinea pigs with a high degree of spatial resolution. We systematically mapped neural activity in the IC using two types of silicon substrate probes that allow for simultaneous recording at multiple neural sites. One probe provided a high resolution in the dorsal-ventral plane and the other provided spatial resolution in the medial-lateral plane. Electrical stimulation of the ipsilateral AC produced excitatory responses in the IC with thresholds usually below 5-10 microA. First spike latencies were predominantly in the 6-20 ms range, although latencies from 3-5 ms were also observed. Broadly distributed unimodal spike patterns with modal latencies greater than 30 ms were occasionally seen. The excitatory responses to cortical stimulation were mostly unimodal and occasionally bimodal with a wide range of spike distribution patterns and response durations. Excitation was often followed by suppression of spontaneous activity. Suppression of acoustic responses was observed even when there was little or no response to electrical stimulation, suggesting spatial-temporal integration. A few of the responding neurons showed purely inhibitory responses to electrical stimulation, suggesting that there are disynaptic routes of corticocollicular inhibition. Detailed spatial mapping revealed that the response patterns and their durations had a characteristic spatial distribution in the IC.

Action Potentials↗

Effects of contralateral sound stimulation on unit activity of ventral cochlear nucleus neurons.

The cochlear nucleus (CN) commissural connection represents the first opportunity for convergence of binaural information in the auditory brainstem. All major neuron types in the ventral CN (VCN) are innervated by a diverse population of cells in the contralateral VCN. This study examined the effect of contralateral sound stimulation on the spontaneous rates (SRs) of neurons in the VCN. Unit activity was recorded with silicon-substrate multichannel probes which allowed recordings from up to 16 sites simultaneously. On average, 30% of units showed short-latency (often only 2 ms greater than the latencies of ipsilateral sound-evoked responses) inhibition of SR by wideband contralateral noise bursts. Fewer units (4.5%) were excited by contralateral noise at sound levels low enough to exclude excitation by acoustic crossover. Both regular and irregular units in the anterior VCN (AVCN) and posterior VCN (PVCN) were inhibited by contralateral sound. Decrements in SR followed a monotonic function with increases in contralateral sound level, except where responses could be attributed to acoustic crossover. Restricting the contralateral noise bandwidth resulted in a frequency-specific inhibition, dominated by frequencies at and below the ipsilateral BF of the unit, consistent with anatomical findings of the tonotopic organization of the CN commissural pathway. The latencies of these effects are compatible with mono, di and tri-synaptic connections reflecting CN commissural pathway effects.

Acoustic Stimulation↗

Effects of trigeminal ganglion stimulation on unit activity of ventral cochlear nucleus neurons.

The trigeminal ganglion sends a projection to the granule and magnocellular regions of the ventral cochlear nucleus (VCN; [J Comp Neurol 419 (2000) 271]), as well as to the cochlea ([Neuroscience 79 (1997) 605; Neuroscience 84 (1998a) 559]). We investigated the effects of electrically stimulating the trigeminal ganglion on unit responses in the guinea-pig VCN. Responses consisted of one, two or more phases of excitation, sometimes followed by a longer inhibitory phase. The latencies to the first excitation peak ranged between 5 and 17 ms from the onset of stimulation. These responses were preceded by a slow wave potential evoked by the stimulation. Applying kainic acid, which eliminates VIIIth nerve responses, diminished the firing rates of VCN units to trigeminal stimulation, and increased their first spike latencies. Cochlear destruction had a similar effect. The responses in VCN evoked by trigeminal ganglion stimulation therefore appear to result from direct stimulation of the trigeminal ganglion-cochlear nucleus pathway, as well as modulation by the trigeminal ganglion-cochlear pathway. Alternatively, a reduction in spontaneous rate of VCN neurons by removal of VIIIth nerve input could explain the decreased response to trigeminal stimulation after cochlear manipulations. The modulation of firing rate in second order auditory neurons by first order somatosensory neurons could influence central auditory targets and may be involved in generating or modulating perceptions of phantom sounds which can be modified by manipulations of somatic regions of the head and neck ("somatic tinnitus").

Action Potentials↗

Trigeminal ganglion innervates the auditory brainstem.

A neural connection between the trigeminal ganglion and the auditory brainstem was investigated by using retrograde and anterograde tract tracing methods: iontophoretic injections of biocytin or biotinylated dextran-amine (BDA) were made into the guinea pig trigeminal ganglion, and anterograde labeling was examined in the cochlear nucleus and superior olivary complex. Terminal labeling after biocytin and BDA injections into the ganglion was found to be most dense in the marginal cell area and secondarily in the magnocellular area of the ventral cochlear nucleus (VCN). Anterograde and retrograde labeling was also seen in the shell regions of the lateral superior olivary complex and in periolivary regions. The labeling was seen in the neuropil, on neuronal somata, and in regions surrounding blood vessels. Retrograde labeling was investigated using either wheatgerm agglutinin-horseradish peroxidase (WGA-HRP), BDA, or a fluorescent tracer, iontophoretically injected into the VCN. Cells filled by retrograde labeling were found in the ophthalmic and mandibular divisions of the trigeminal ganglion. We have previously shown that these divisions project to the cochlea and middle ear, respectively. This study provides the first evidence that the trigeminal ganglion innervates the cochlear nucleus and superior olivary complex. This projection from a predominantly somatosensory ganglion may be related to integration mechanisms involving the auditory end organ and its central targets.

Animals↗

Endolymphatic hydrops reduces retrograde labeling of trigeminal innervation to the cochlea.

This paper reports that endolymphatic hydrops causes a significant reduction of retrogradely labeled cell bodies of the ipsilateral trigeminal ganglion following application of horseradish peroxidase in the cochlea. We previously showed that the trigeminal ganglion is a source of primary sensory innervation to the cochlear blood vessels. The innervation of the cochlea from the trigeminal ganglion may provide the basis of an alternative mechanism for Ménière's syndrome (imbalance, hearing loss, tinnitus, and a sensation of fullness in the ear) for which a central neural basis has been speculated. Innervation patterns of sensory nerves from the trigeminal ganglion to the cochlear blood vessels were studied using retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). Healthy and hydropic guinea pigs were unilaterally implanted with an osmotic pump and a cannula for cochlear delivery of 2% WGA-HRP or vehicle alone. In other guinea pigs the cochlea was pretreated with 100 micromol capsaicin before administering 2% WGA-HRP. Histological sections of the ipsi- and contralateral trigeminal ganglia were obtained 48 h after WGA-HRP infusion. In the hydropic guinea pig, the number of labeled nerve cell bodies observed in the anteriomedial portion of the trigeminal ganglion at the origin of the ophthalmic nerve was reduced by 70% relative to normal animals. Capsaicin pretreatment nearly eliminated the labeled sensory fibers as expected. These data indicate that the trigeminal innervation to the cochlea could be involved in inner ear homeostatic disturbances, including the hydrops that is symptomatic of Ménière's disease.

Animals↗

Direct evidence of trigeminal innervation of the cochlear blood vessels.

This paper provides the first detailed description of the trigeminal innervation of the inner ear vasculature. This system provides a newly discovered neural substrate for rapid vasodilatatory responses of the inner ear to high levels of activity and sensory input. Moreover, this discovery may provide an alternative mechanism for a set of clinical disturbances (imbalance, hearing loss, tinnitus and headache) for which a central neural basis has been speculated. Iontophoretic injections of biocytin were made via a glass microelectrode into the trigeminal ganglion in guinea-pigs. Tissue for histological sections was obtained 24 h later. Labeled fibers from the injection site were observed as bundles around the ipsilateral spiral modiolar blood vessels, as individual labeled fibers in the interscala septae, and in the ipsilateral stria vascularis. The dark cell region of the cristae ampullaris in the vestibular labyrinth was also intensively labeled. No labeled fibers were observed in the neuroepithelium of the cristae ampullaris or the semicircular canals. These results confirm and localize an earlier indirect observation of the trigeminal ganglion projection to the cochlea. This innervation may play a role in normal vascular tone and in some inner ear disturbances, e.g., sudden hearing loss may reflect an abnormal activity of trigeminal ganglion projections to the cochlear blood vessels.

Animals↗

Sources of input to the cochlear granule cell region in the guinea pig.

Anterograde and retrograde transport of fluorogold was used to trace input to the superficial granule cell layer of the ventral cochlear nucleus in the guinea pig. Infusion of fluorogold into the labyrinth resulted in heavy labeling of eighth nerve axons and their terminals in the ventral cochlear nucleus, but only a few labeled axons entered the granule cell layer. Injections of fluorogold restricted to the granule cell layer retrogradely labeled neurons in the ipsilateral lateral superior olivary nucleus, in the periolivary region predominantly contralaterally, and in the inferior colliculus predominantly ipsilaterally. Labeled neurons were also present in the ipsilateral ventral cochlear nucleus, but this may be due to interruption of axons of passage in the lateral ventrotubercular tract. Overall this study demonstrates very restricted direct cochlear input to the granule cell region, but provides evidence for projections from several brainstem auditory nuclei.

Animals↗

Influence of centrifugal pathways on forward masking of ventral cochlear nucleus neurons.

When responses to one part of a sequence of auditory signals reduce the responses to a subsequent portion of the signal, "forward masking" results. Although forward masking occurs in the auditory nerve, that observed in the ventral cochlear nucleus (VCN) more closely resembles psychophysical forward masking. In contrast to the auditory nerve in which the amount of forward masking is proportional to the amount of excitation produced by the masker, most VCN neurons show a poor correlation between forward masking and excitation produced by the masker, indicating a more complex interaction between responses to adjacent signals. This study tested the hypothesis that one component of forward masking is produced by inputs from centrifugal neural connections to the VCN. The centrifugal pathways were interrupted with knife-cut lesions medial to the CN. Responses of single units obtained 60 minutes after the lesions were compared to those obtained before the lesions. In primarylike, sustained chopper and on units the lesions resulted in a reduction in forward masking and enhanced recovery. In contrast, lesions resulted in increased masking in primarylike-notch and low-intensity chopper units. The relationship between masker-elicited excitation and forward masking became more monotonic for transient choppers and on units, approaching that observed for auditory nerve fibers. These effects are probably the result of removal of both inhibitory and excitatory inputs, ultimately reflecting a balance of excitation and inhibition to each neural population in the VCN.

Animals↗

Trigeminal ganglion innervation of the cochlea--a retrograde transport study.

Innervation patterns of sensory nerves from the trigeminal ganglion to the cochlear blood vessels were studied using retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Guinea-pigs (n=7) were unilaterally implanted with an osmotic pump and a cannula for cochlear delivery of 2% or 20% wheat germ agglutinin horseradish peroxidase (Group 1), 2% wheat germ agglutinin-horseradish peroxidase followed by 100 micromol capsaicin (Group 2), or vehicle alone. Histological sections of the trigeminal ganglia, the C1 and C2 dorsal ganglia, the superior and inferior ganglia of the glossopharyngeal nerve bilaterally, the midbrain and the brainstem were obtained after 48 h of infusion. In Group 1, a large number of labeled nerve cell bodies were observed in the anteromedial portion of the trigeminal ganglion and at the origin of the ophthalmic nerve. Some labeled cells were also found on the lateral side of the ophthalmic nerve, as well as on the medial side of the maxillary nerve root. Capsaicin pretreatment significantly reduced the density of labeled neurons in the trigeminal ganglion. A few labeled neurons were also found in the trigeminal brainstem nucleus complex and in certain auditory brainstem nuclei. No wheat germ agglutinin horseradish peroxidase-positive cells were observed in the spinal C1 or C2 cervical ganglia or in the superior or inferior glossopharyngeal ganglia. In contrast, wheat germ agglutinin-horseradish peroxidase application to the middle ear resulted in labeled cells in the middle posterolateral portion of the trigeminal ganglia and in the superior ganglia of the glossopharyngeal nerve. These results provide the first direct evidence that the trigeminal ganglion sends projections to the cochlea.

Animals↗

Recovery of forward-masked responses in ventral cochlear nucleus neurons.

Single unit responses were obtained from 8 classes of cells in the ventral cochlear nucleus: Primarylike, Primarylike with characteristic frequencies below 1 kHz, Primarylike-Notch, Sustained Chopper, Transient-Chopper, Low-intensity Chopper; Onset with later activity and On-Chopper. Stimuli were paired tonebursts, a masker preceding a probe, separated by time delta t ms. The decrement in discharge rate to the probe was measured as a function of delta t and constituted the forward-masking recovery function. The recovery functions of primarylike units were similar to those reported for auditory nerve fibers, but recovered more slowly than all other classes of units in the ventral cochlear nucleus. Some units, such as onset units, were completely masked at short masker-probe intervals, while others, such as the low-intensity choppers, were less affected by the masker. More masking occurred in the first 2 ms of the response (onset rate) than in the overall response (average rate). Using shorter maskers and measuring the onset rate produced greater differences in masking functions between unit classes. Units with high spontaneous activity were more resistant to the effects of the masker than units with low and medium spontaneous activity. This was especially evident at high masker levels and short masker-probe intervals. Units other than primarylike often showed non-monotonic relationships between the firing rate evoked by the masker and the firing rate decrement in response to the probe, suggesting that both adaptation and inhibition are operating to produce the observed effects.

Acoustic Stimulation↗

Connections between the cochlear nuclei in guinea pig.

This study provides a detailed analysis of the appearances and distributions of neurons projecting from one cochlear nucleus to the other. Injections of wheatgerm agglutinin conjugated to horseradish peroxidase were made into ventral or dorsal cochlear nucleus of the guinea pig. Retrogradely labeled cells in the opposite cochlear nucleus were examined and quantified. Three major categories of labeled cells were discerned on the basis of their soma shape: elongate, round-to-oval, and polygonal. All injections resulted in widespread labeling of cells in all of these categories, but especially round-to-oval cells, in the opposite ventral cochlear nucleus and sparse labeling in the dorsal cochlear nucleus. The results suggest that there is a significant cochlear nucleus commissural projection involving heterogeneous cell types which could have diverse functions in binaural auditory signal processing.

Animals↗

Descending projections to the dorsal and ventral divisions of the cochlear nucleus in guinea pig.

The origins of extrinsic projections to the guinea pig dorsal and ventral cochlear nuclei were identified by examining the retrograde transport of horseradish peroxidase conjugated to wheatgerm agglutinin following its injection into each of these divisions. Major projections originated in periolivary regions of the superior olivary complex, the contralateral cochlear nucleus and the inferior colliculus. There was no contribution from the nuclei of the lateral lemniscus to these pathways. The heaviest projection from the periolivary regions to both divisions of the cochlear nucleus arose bilaterally in the ventral nucleus of the trapezoid body. The ipsilateral lateral nucleus of the trapezoid body also projected heavily to dorsal and ventral cochlear nucleus. In addition, the ventral cochlear nucleus received a substantial projection from the dorsal aspect of the ipsilateral dorsomedial periolivary nucleus. Projections originating bilaterally in the central nucleus of the inferior colliculus terminated in the deep layers of dorsal cochlear nucleus. These projections appear to be more strongly ipsilateral and specific than those reported in the cat.

Animals↗

Evoked vertex and inferior colliculus responses to electrical stimulation of the cochlear nucleus.

Evoked potentials were recorded from the vertex and the inferior colliculus in guinea pigs in response to electrical stimulation of the cochlear nucleus complex. The stimuli consisted of 80-microseconds biphasic pulses, ranging from 20 to 5,000 microA. The effect of electrode location (nerve root area, surface, and in-depth dorsal cochlear nucleus) on the evoked response was assessed by measuring amplitudes, latencies, and thresholds as a function of stimulating current levels. Stimulation of the nerve root area resulted in the shortest latencies, the largest amplitudes, and the lowest thresholds, whereas the surface of the dorsal cochlear nucleus was the least effective stimulating site.

Amplifiers, Electronic↗

Unit responses in ventral cochlear nucleus reflect cochlear coding of rapid frequency sweeps.

This study examines the encoding of rapid frequency sweeps in single units of the ventral cochlear nucleus (VCN). Sweeps were designed to explore the role of cochlear mechanics in shaping the temporal responses across cells in the VCN. The time course of frequency change for rapidly rising frequency sweeps theoretically produced simultaneous displacement maxima by cancelling travel time along the cochlear partition. Rising sweeps with longer time courses only partially canceled travel time, while falling sweeps had time courses of frequency change equal to or greater than travel time. Falling sweeps thus augmented normal travel time. Latency of unit firing to sweeps across unit characteristic frequency (CF) reflected cochlear delay-line mechanics. The latency-CF functions agreed with predictions from travel-time estimates for rising-frequency sweeps, but responses to falling sweeps were less predictable.

Acoustic Stimulation↗

The effects of cochlear hypothermia on compound action potential tuning.

The effects of lowered cochlear temperature on eighth-nerve tuning were assessed by using forward masking of whole nerve action potential (AP) responses to generate AP tuning curves (APTCs) at cochlear temperatures ranging from 38.5 degrees to 30 degrees C for probe frequencies from 8 to 36 kHz. The data indicate that subnormal cochlear temperatures result in: broadened APTCs for probe frequencies above 10 kHz which are interpreted as resulting from reduced hair-cell frequency selectivity, lowered or more sensitive APTC tips where tone-burst thresholds are unchanged, and raised or less sensitive tips where thresholds to tone bursts were elevated. Increased tip sensitivity is explained in terms of enhanced eighth-nerve adaptation which occurred during hypothermia. Experiments directly addressing adaptation were performed, in which the masker-probe interval (delta t) was systematically lengthened. The normalized AP decrement versus delta t functions indicate an enhancement of both the amount and duration of adaptation during hypothermia. Functions relating the growth of response to the masker (AP decrement versus masker intensity functions) were reduced at low temperatures.

Acclimatization↗

High-synchrony cochlear compound action potentials evoked by rising frequency-swept tone bursts.

The auditory compound action potential (CAP) represents synchronous VIIIth nerve activity. Clicks or impulses have been used in the past to produce this synchrony under the assumption that the wide spectral spread inherent in transient signals will activate a large portion of the cochlear partition. However, the observation that only auditory nerve units tuned above 3 kHz contribute to synchronous activity in the N1P1 complex of the CAP [Dolan et al., J. Acoust. Soc. Am. 73, 580-591 (1983)] suggests that temporal delays imposed by the traveling wave result in an asynchronous pattern of VIIIth nerve activation. In order to determine if units tuned below 3 kHz could be recruited into the CAP response, the present study uses tone bursts of exponentially rising frequency to hypothetically activate synchronous discharges of VIIIth nerve fibers along the length of the cochlear partition. The equations defining the frequency sweeps are calculated to be the inverse of the delay-line characteristics of the guinea pig cochlear partition. The resultant sweeps theoretically cause a constant phase displacement of a large portion of the cochlear partition at one time. Compound action potentials recorded in response to the rising frequency sweeps were compared to CAPs evoked by corresponding falling frequency sweeps and clicks. Analysis of the CAP waveforms showed narrower N1 widths and larger N1 and P1 amplitudes for rising sweeps when compared to falling sweeps. This is consistent with the hypothesis of increased synchrony. A further test of the hypothesis was made by using high-pass masking noise to evaluate the contributions of discrete cochlear locations to the CAP ("derived" CAP). Latency functions of the derived CAPs for clicks and falling frequency sweeps showed progressive increases in latency as the cutoff frequency of the high-pass filter was lowered. The latency of the derived CAP for these stimulus conditions reflects traveling wave delays [Aran and Cazals, "Electrocochleography: Animal studies," in Evoked Electrical Activity in The Auditory Nervous System (Academic, New York, 1978)]. In contrast, derived CAPs obtained from rising sweeps showed no change in latency for any cutoff frequencies, indicating a constant delay of response for fibers with different characteristic frequencies (CFs). These results support the theoretical premise underlying the derivation of the rising sweep: Spectral energy with the appropriate temporal organization, dictated by basilar membrane traveling wave properties, will increase CAP synchrony.

Acoustic Stimulation↗

Cochlear microphonic responses of the peripheral auditory system to frequency-varying signals.

Cochlear partition displacement responses to rising and falling frequency sweeps were inferred from cochlear microphonic potentials recorded from three basal turn locations in the guinea pig cochlea. Relative phase measures of microphonic potentials recorded from the three locations suggested that displacements of the partition toward either scala vestibuli or scala tympani occurred closely together in time for rising sweeps and were dispersed in time for falling sweeps. These differences in peripheral response patterns to sweeps may explain, in part, asymmetric neural discharges elicited from higher neural centers.

Animals↗