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PubMed2006

Rate thresholds determine the precision of temporal integration in principal cells of the ventral cochlear nucleus.

The three types of principal cells of the ventral cochlear nucleus (VCN), bushy, octopus, and T stellate, differ in the detection of coincidence among synaptic inputs. To explore the role of the action-potential-generation mechanism in the detection of coincident inputs, we examined responses to depolarizing currents that increased at varying rates. To fire an action potential, bushy cells, likely of the globular subtype, had to be depolarized faster than 4.8+/-2.8 mV/ms, octopus cells faster than 9.5+/-3.6 mV/ms, and T stellate cells fired irrespective of the rate of depolarization. The threshold rate of depolarization permitted definition of a time window over which depolarization could contribute to generating action potentials. This integration window differed between cell types. It was 5.3+/-1.8 ms for bushy cells and 1.4+/-0.3 ms for octopus cells. T Stellate cells fired action potentials in response to even slow depolarizations, showing that their integration window was unlimited so that temporal summation in these cells is limited by the time course of synaptic potentials. The rate of depolarization threshold in octopus and bushy cells was decreased by alpha-dendrotoxin while T stellate cells were largely insensitive to alpha-dendrotoxin indicating that low-voltage-activated K+ conductances (gKL) are important determinants of the integration window.

Action Potentials↗
PubMed2006

Age-related changes in the response properties of cartwheel cells in rat dorsal cochlear nucleus.

The fusiform cell and deep layers of the dorsal cochlear nucleus (DCN) show neurotransmitter and functional age-related changes suggestive of a downregulation of inhibitory efficacy onto DCN output neurons. Inhibitory circuits implicated in these changes include vertical and D-multipolar cells. Cartwheel cells comprise a large additional population of DCN inhibitory neurons. Cartwheel cells receive excitatory inputs from granule cell parallel fibers and provide a source of glycinergic inhibitory input onto apical dendrites of DCN fusiform cells. The present study compared the response properties from young and aged units meeting cartwheel-cell criteria in anesthetized rats. Single unit recordings from aged cartwheel cells revealed significantly higher thresholds, increased spontaneous activity and significantly altered rate-level functions characterized by hyperexcitability at higher intensities. Aged cartwheel cells showed a significant reduction in off-set suppression. Collectively, these findings suggest a loss of tonic and perhaps response inhibition onto aged DCN cartwheel neurons. These changes likely reflect a compensatory downregulation of synaptic inhibition in response to a loss of excitatory drive from auditory and non-auditory excitatory inputs via granule cells. The impact of increased excitability of cartwheel cells on DCN output neurons is likely to be complex, influenced by loss of glycinergic release and/or subunit receptor changes which would only partially off-set age-related loss of inhibition onto the somata and basal dendrites of fusiform cells.

Age Factors↗
PubMed2001

Temporal representation of iterated rippled noise as a function of delay and sound level in the ventral cochlear nucleus.

The discharge patterns of single units in the ventral cochlear nucleus (VCN) of anesthetized guinea pigs were examined in response to iterated rippled noise (IRN) as a function of the IRN delay (which determines the IRN pitch) and the IRN sound level. Delays were varied over five octaves in half-octave steps, and sound levels were varied over a 30- or 50-dB range in steps of 5 dB. Neural responses were analyzed in terms of first-order and all-order inter-spike intervals (ISIs). The IRN quasi-periodicity was preserved in the all-order ISIs for most units independent of unit type or best frequency (BF). A deterioration of the temporal all-order code was found, however, when the neural response was influenced by inhibition. The IRN quasi-periodicity was also preserved in first-order ISIs for a limited range of IRN delays and levels. Sustained Chopper units (CS) in the VCN responded with very regular ISIs when the IRN delay corresponded to the unit's chopping period; i.e., the unit showed an increased proportion of intervals corresponding to the IRN delay (interval enhancement) relative to an equal-level, white-noise stimulation. This interval enhancement has a band-pass characteristic with a peak corresponding to the chopping period. Moreover, for CS units in rate saturation, the chopping period, and thus the interval enhancement to the IRN, did not vary with level. Units classified as onset-chopper also show a band-pass interval enhancement to the IRN stimuli; however, they show more level-dependent changes than CS units. Primary-like (PL) units also show level-dependent changes in their ability to code the IRN pitch in first-order intervals. The range of delays where PL units showed interval enhancement was broader and extended to shorter delays. Based on these findings, it is suggested that CS units may play an important role in pitch processing in that they transform a higher-order interval code into a first-order interval place code. Their limited dynamic range together with the preservation of the temporal stimulus features in saturation may serve as a physiological basis for the perceived level independence of pitch.

Action Potentials↗
PubMed1990

Psychophysical measures from electrical stimulation of the human cochlear nucleus.

Auditory performance on basic psychophysical tasks was measured in ten deaf patients with electrodes positioned near their cochlear nucleus. The device is called the auditory brainstem implant (ABI). Electrodes were placed during surgery to remove an acoustic neuroma, which results in the removal of the VIII nerve and, thus deafness. In patients who received auditory sensation from electrical stimulation we measured auditory performance on standard psychophysical tasks: thresholds, loudness growth, intensity discrimination, temporal integration, temporal modulation detection, gap detection, and forward masking. Plots of threshold as a function of frequency or biphasic pulse duration were markedly different from those of patients with cochlear implants. The difference in threshold functions is probably partly due to the biophysical difference in the neural elements stimulated. Another possibility is that part of the difference is due to the highly abnormal spatial pattern of activation in the cochlear nucleus from electrical stimulation, which prevents normal spatial integration of activity. The usable range of electrical amplitudes above threshold is comparable with that of cochlear implants, typically 10-15 dB. Little temporal integration occurs over a range of stimulus durations from 2-1000 ms. When compared at equivalent loudness levels, gap detection thresholds are similar to, or a bit longer than, gap thresholds in normal-hearing listeners and cochlear implant patients. Forward masking recovery functions are similar to those of normal listeners and cochlear implant patients. Patients' ability to detect amplitude modulation as a function of modulation frequency is similar to that of cochlear implant patients and normal listeners. Thus, direct electrical stimulation of the brainstem produces temporal resolution that does not significantly differ from that of normal listeners when compared in equivalent amplitude units. This implies that the limiting factors for these tasks are more centrally located, and not directly related to threshold mechanisms. Thus, a properly designed speech processor could preserve the important temporal features of speech for these patients.

Adolescent↗
PubMed1976

Descending inputs to caudal cochlear nucleus in cats: a horseradish peroxidase (HRP) study.

After HRP injections into the octopus cell area of the cat cochlear nucleus, only periolivary neurons of the superior olivary complex (SOC) reacted. Elongate neurons in the lateral periolivary nuclei (ipsilateral to the injection) and multipolar neurons in ventromedial periolivary regions (contralateral to the injection) contained granules. No neurons in the main SOC nuclei or higher auditory nuclei reacted, despite a wide range of HRP concentrations. Thus, neurons from the SOC to the octopus cell area of the cochlear nucleus seem to be entirely periolivary and not entirely equivalent to neurons providing collaterals to the olivocochlear bundle.

Animals↗
PubMed1994

Cholinergic modulation of spontaneous activity in rat dorsal cochlear nucleus.

Extracellular recordings were made from brain stem slices to test the effects of bath application of cholinergic agonists and antagonists on the firing rates of spontaneously active dorsal cochlear nucleus neurons. About 90% of neurons responded to carbachol. A higher proportion responded to muscarine than to nicotine. Muscarine elicited larger responses at lower concentrations than nicotine. Responses to either carbachol or muscarine were always blocked by atropine or scopolamine. The nicotinic antagonists d-tubocurarine, hexamethonium, and mecamylamine blocked the responses to nicotine, but did not decrease the responses to carbachol. Regularly firing neurons showed only increases of firing rate during exposure to cholinergic agonists. About half of responsive bursting neurons showed increased firing; half showed increased followed by decreased firing to 10 microM carbachol or muscarine. All phases of the responses of most bursting neurons were greatly decreased or abolished in low calcium, high magnesium medium, while responses of regular neurons were not detectably affected. Thus, cholinergic agonists appear to act directly on regularly firing neurons, while their actions on bursting neurons may require synaptic activity. The data suggest that cholinergic transmission in the dorsal cochlear nucleus is predominantly muscarinic, and that most regularly firing spontaneously active neurons have muscarinic receptors.

Action Potentials↗
PubMed2000

Effects of high-potassium-induced depolarization on amino acid chemistry of the dorsal cochlear nucleus in rat brain slices.

High K+ was used to depolarize glia and neurons in order to study the effects on amino acid release from and concentrations within the dorsal cochlear nucleus (DCN) of brain slices. The release of glutamate, gamma-aminobutyrate (GABA) and glycine increased significantly during exposure to 50 mM K+, while glutamine and serine release decreased significantly during and/or after exposure, respectively. After 10 min of exposure to 50 mM K+, glutamine concentrations increased in all three layers of DCN slices, to more than 5 times the values in unexposed slices. In the presence of a glutamate uptake blocker, L-trans-pyrrolidine-2,4-dicarboxylic acid (PDC), glutamine concentrations in all layers did not increase as much during 50 mM K+. Similar but smaller changes occurred for serine. Mean ATP concentrations were lower in 50 mM K(+)-exposed slices compared to control. The results suggest that depolarization, such as during increased neural activity, can greatly affect amino acid metabolism in the cochlear nucleus.

Adenosine Triphosphate↗
PubMed1992

Rapid and reversible astrocytic reaction to afferent activity blockade in chick cochlear nucleus.

We describe here rapid proliferation of astrocytic processes immunoreactive for glial fibrillary acidic protein (GFAP) in the chick cochlear nucleus following blockade of action potentials in the afferent nerve. Unilateral eighth nerve activity blockade was achieved through intralabyrinthine injection of TTX. Within 1 hr of activity blockade, a 56% increase in area density of GFAP-immunoreactive processes was found in the ipsilateral cochlear nucleus as compared to the contralateral side of the brain. This increase reached 152% by 3 hr. When eighth nerve activity was allowed to recover and animals were studied 1 week after TTX injection, no difference was found in GFAP immunoreactivity between the ipsilateral and contralateral cochlear nuclei. This is the first report of a glial reaction to documented neuronal inactivity in the absence of neuropathology. These results indicate that neuronal activity may regulate the structure of astrocytic processes.

Animals↗
PubMed1996

N-methyl-D-aspartate receptors at parallel fiber synapses in the dorsal cochlear nucleus.

1. N-methyl-D-aspartate (NMDA) binding and NMDA-receptors immunolocalization experiments have revealed an enhanced expression of these receptors in the outer two layers of the dorsal cochlear nucleus (DCN). The distribution of the receptors is congruent with the distribution of synapses produced by the granule cell-parallel fiber system. To determine the functional distribution and contribution of NMDA receptors at parallel fiber synapses, synaptic responses to parallel fiber stimulation were studied in in vitro brain slice preparations of the guinea pig and rat dorsal cochlear nucleus. 2. The field potential response to parallel fiber stimulation in guinea pigs includes three postsynaptic components. The short latency components (the P3(2) and N2(2)) are blocked by general excitatory receptor antagonists, including the non-NMDA-receptor blockers 6,7-dinitroquinoxaline-2,3-dione (DNQX) and 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), but are insensitive to NMDA-receptor antagonists. 3. A slower component (P4(2)) is revealed when the slices are washed with a low magnesium solution to eliminate the magnesium block of currents through NMDA receptors. This slow component is reduced by D- or DL-2-amino-5-phosphonovaleric acid (D-APV, DL-APV) and 3-[(+/-)-2-carboxypiperazine-4-yl] propyl-1-phosphonate, but is not blocked by DNQX or CNQX. Eliminating the voltage dependence of the NMDA receptors also results in a complex oscillatory response in some slices. This response exhibits the same pharmacological sensitivity as the slow potential. The pharmacologic sensitivity to NMDA-receptor antagonists suggest that the slow component (P4(2)) and the associated oscillatory response are mediated through activation of NMDA receptors. 4. Current source-density analysis of the parallel fiber-evoked field potentials was carried out to determine the relative spatial distributions of the fast and slow synaptic currents. Both synaptic components were associated with a superficial current sink and a deeper current source, localized within the superficial 250 microM of the nucleus. The slow (APV-sensitive) current was slightly shifted in depth relative to the fast (DNQX-sensitive) current in three of five slices with the maximum current sink and source occurring approximately 16 microns further from the surface of the DCN. These data suggest that either the NMDA receptors are not present at all of the synapses that generate the fast non-NMDA currents or that postsynaptic cells with different dendritic distributions have different densities of NMDA receptors. 5. The types of cells in layers 1 and 2 exhibiting NMDA-receptor-mediated synaptic potentials were investigated. Intracellular recordings with sharp electrodes in guinea pig slices showed that eliminating the voltage dependence of the NMDA receptors in low magnesium revealed a slow excitatory postsynaptic potential (EPSP) in both simple and complex spiking cells. The late phase of the EPSP could be reduced by APV in both cell types. These results could be explained by NMDA receptors on the postsynaptic cells or by NMDA receptors on excitatory interneurons. Attempts to demonstrate an appropriate voltage dependence of the parallel fiber synaptic response in normal magnesium medium under current clamp were confounded by the intrinsic voltage-dependent conductances of the cells. 6. To determine whether NMDA receptors were present on postsynaptic cells, the direct sensitivity of DCN cells to NMDA application was examined during intracellular recording. Both simple spiking and complex spiking cells responded to NMDA with depolarization. The response to NMDA persisted when non-NMDA receptors were blocked with CNQX or DNQX. However in all cells tested, the response to NMDA was blocked by APV. These experiments further support the postsynaptic localization of NMDA receptors on both simple and complex spiking cells. (ABSTRACT TRUNCATED)

Animals↗
PubMed2006

Oscillating neurons in the cochlear nucleus: I. Experimental basis of a simulation paradigm.

Anatomical and physiological auditory data and pitch measurements are presented including some additional analysis. The data provide the basis for a new computer model of sustained chopper neurons in the ventral cochlear nucleus. New and old evidence indicating a preference for multiples of 0.4 ms in oscillations of chopper neurons in the cochlear nucleus of different species such as man, cats, and Guinea fowls, is summarized. Our hypothesis is that the time constant of 0.4 ms is due to the minimum synaptic delay of chopper neuron connections. Anatomical findings show that chopper neurons are indeed connected and can excite each other; a model of a circular network of neurons that are connected via synapses with a delay of 0.4 ms is thus plausible. Results concerning frequency tuning and dynamical properties of periodicity encoding of chopper neurons are reviewed. It is concluded that chopper neurons receive input both from auditory nerve fibres and onset neurons.

Acoustic Stimulation↗
PubMed2005

Developmental time course of potassium channel expression in the rat cochlear nucleus.

Voltage gated potassium channels play critical roles in determining the responses of auditory brainstem neurons to acoustic stimuli. In the present study, we examined the developmental expression of potassium channels in rat cochlear nucleus. Quantitative RT-PCR revealed that Kv1.1 , Kv1.2 and Kv3.1 showed a monotonic increase in mRNA levels from postnatal days 3-28 (P3-P28), after which mRNA level was relatively constant until P56. In contrast, Kv4.2 mRNA levels were lower on average by a factor of 2 after P28 than before P28. Relative to Kv1.1, Kv3.1 and Kv1.2 mRNA were more abundant before P10 and less abundant thereafter. To address the relationship between message and protein levels, we performed semi-quantitative Western blotting for Kv1.2. The message for Kv1.2 increased earlier in development than the protein levels. Immunocytochemistry revealed a broad expression of Kv1.1 and Kv1.2 in the VCN. Staining intensity increased from 7-28 days postnatal. Kv1.2 immunostaining was less variable across cells than Kv1.1 staining. We conclude that maturation of potassium channel expression in the rat cochlear nucleus continues until at least 4 weeks postnatal.

Age Factors↗
PubMed1995

Sound induced expression of c-Fos in GABA positive neurones of the gerbil cochlear nucleus.

To characterize c-Fos-expressing neurones in more detail, a double labelling technique was developed to simultaneously demonstrate the presence of GABA-like and c-Fos-like immunoreactivity in cryostat sections of the gerbil cochlear nucleus. The animals were exposed to a wide-band noise stimulus for the induction of c-Fos expression. The distribution of c-Fos-positive cells and GABA-positive somata was consistent with previous reports. Our double labelling approach revealed the presence of GABA-positive cells that showed c-Fos expression after noise stimulation. One interpretation of this finding is that a prolonged acoustic exposure induces long term changes in inhibitory interneurones to adjust the output of the cochlear nucleus.

Acoustic Stimulation↗
PubMed2005

Developmental regulation and adult maintenance of potassium channel proteins (Kv 1.1 and Kv 1.2) in the cochlear nucleus of the rat.

The development and maintenance of the adult expression and distribution of Kv 1.1 and Kv 1.2, two voltage-dependent potassium channel subunits, were investigated in the anteroventral cochlear nucleus (AVCN) of the rat. Both Kv 1.1 and Kv 1.2 were found in AVCN neuronal cell bodies at birth, as detected by in situ hybridization and immunocytochemistry. However, Kv 1.1 and Kv 1.2 were not seen in axons until the end of the third postnatal week. From postnatal day 21 through adulthood, labeling for both potassium channels was in axonal processes, whereas the number of cell bodies labeled for Kv 1.1 decreased and there were no cell bodies labeled for Kv 1.2. Therefore, these two potassium channel proteins are targeted to their final subcellular destinations in axons well after hearing onset. Once the adult distribution pattern of Kv 1.1 and Kv 1.2 is attained, its maintenance does not depend on signals from auditory nerve synapses. Eliminating auditory nerve input to the cochlear nucleus by means of bilateral cochleotomy did not change Kv 1.1 or Kv 1.2 expression or distribution, as seen by in situ hybridization, immunocytochemistry and Western blot. Thus, normal excitatory synaptic input in adult animals is not a requirement to regulate the expression and cellular and subcellular distribution of these potassium channel proteins.

Age Factors↗
PubMed1996

Three classes of inhibitory amino acid terminals in the cochlear nucleus of the guinea pig.

Electron microscopic postembedding immunocytochemistry was used to analyze and assess the synaptic distribution of glycine (GLY) and gamma-amino butyric acid (GABA) immunoreactivities in the guinea pig cochlear nucleus (CN). Three classes of endings were identified containing immunolabeling for glycine, GABA, or both glycine and GABA (GLY/GABA). All classes were similar in that the terminals contained pleomorphic vesicles and formed symmetric synapses with their postsynaptic targets. A fourth class, which labeled with neither antibody, contained round vesicles and formed asymmetric synapses. Glycine endings predominated in the ventral CN, while GLY/GABA endings were prevalent in the dorsal CN. GABA endings were the least common and smallest in size. Glycine, GLY/GABA, and GABA endings differed in their proportions and patterns of distribution on the different classes of projection neurons in the CN, including spherical bushy, type I stellate/multipolar, and octopus cells in the ventral CN and fusiform cells in the dorsal CN. The vast majority of anatomically-defined, putative inhibitory endings contain GLY, GABA, or both, suggesting that most of the inhibition in the cochlear nucleus is mediated by these three cytochemically and, probably, functionally distinct classes of endings. The results of this study also suggest that a large proportion of the GABA available for inhibition in the CN coexists in terminals with glycine.

Animals↗
PubMed1996

Synaptic input to cochlear nucleus dendrites that receive medial olivocochlear synapses.

Axons of olivocochlear neurons originate in the superior olivary complex and project to the cochlea. Along their course, medial olivocochlear axons give off branches to the cochlear nucleus. We labeled these branches with horseradish peroxidase and used electron microscopy to determine their target dendrites. Target dendrites were of two classes: "large" dendrites and "varicose" dendrites. Using serial sections, we reconstructed the dendrites and, in addition to the labeled olivocochlear input, we determined the synaptic profile of unlabeled inputs onto the dendrites. We classified the terminals on the basis of the shape and size of their synaptic vesicles. On large dendrites, the predominant type of unlabeled terminal had small round (SmRnd) vesicles. These terminals are likely to be excitatory, and some of them may originate from unlabeled medial olivocochlear branches. On varicose dendrites, the predominant type of terminal had pleomorphic vesicles. These terminals are likely to be inhibitory. They may be from descending inputs that arise in higher centers. A final type of terminal onto large dendrites exhibited signs of neuronal degeneration, possibly because the cell body of origin was damaged during the injection procedure. These terminals often had long, perforated synaptic densities and may originate from type II primary afferents. Thus, medial olivocochlear efferents and type II afferents, which both contact outer hair cells in the periphery, appear to synapse onto the same targets in the cochlear nucleus. In contrast, where examined, the target dendrites did not receive terminals with large vesicles from afferents that contact inner hair cells. Thus, target neurons appear to function in a neural circuit associated more closely with outer than with inner hair cells.

Animals↗
PubMed2003

Morphology of neurons cultured from subdivisions of the mouse cochlear nucleus.

This study was designed to characterize the dendritic organization of cochlear nucleus (CN) cells grown in primary cell culture and to assess differences among cultures grown from different regions of CN. Cultures were prepared from postnatal mice and processed using microtubule-associated protein 2 (MAP2) or gamma-aminobutyric acid (GABA) immunohistochemistry. CN neurons were successfully cultured from preparations grown from either the anteroventral subdivision of the nucleus (AVCN), the posterior region [posteroventral (PVCN) and dorsal (DCN) subnuclei], or the whole CN, although the cultured neurons did not exhibit complex dendritic patterns characteristic of CN neurons in vivo. Neurons cultured from the entire nucleus exhibited an increased rate of survival compared to those cultured from either the anterior or posterior regions, although similar types of cells were observed in all preparations. The majority of cultured CN neurons were GABA-positive and had soma areas that were similar to the areas of immature GABAergic neurons measured in CN sections. Small cells (soma areas or=120 microm(2)) were also present in significant numbers. Overall, CN cultures consisted of a heterogeneous population of neurons that had less elaborate dendritic organizations than cells of corresponding size that have been described in adult animals in vivo.

Animals↗
PubMed2006

Cochlear damage induces GAP-43 expression in cholinergic synapses of the cochlear nucleus in the adult rat: a light and electron microscopic study.

Recent studies suggest a potential for activity-dependent reconstruction in the adult mammalian brainstem that exceeds previous expectations. We found that a unilateral cochlear lesion led within 1 week to a rise of choline acetyltransferase (ChAT) immunoreactivity in the ventral cochlear nucleus of the affected side, matching the lesion-induced expression of growth-associated protein 43 (GAP-43) previously described. The rise of both ChAT and GAP-43 immunoreactivity was reflected in the average density of the staining. Moreover, the number of light-microscopically identifiable boutons increased in both stains. GAP-43-positive boutons could, by distinct ultrastructural features, regularly be identified as presynaptic endings. However, GAP-43 immunoreactivity was not only found in presynaptic endings with a classical morphology, but also in profiles that suggest morphological dynamic structures by showing filopodia, assemblages of pleomorphic vesicles, large vesicles (diameter up to 200 nm) fusing with the presynaptic plasma membrane close to synaptic contacts, small dense-core vesicles (diameter about 80 nm) and presynaptic ribosomes. Moreover, we observed perforated synapses as well as GAP-43 immunoreactivity condensed in rafts, both indicative of growing or changing neuronal connections. Classical and untypical ultrastructural profiles that contained GAP-43 also contained ChAT. We conclude that there is extensive deafness-induced GAP-43-mediated synaptic plasticity in the cochlear nucleus, and that this plasticity is predominantly, if not exclusively, based on cholinergic afferents.

Acetylcholine↗
PubMed1997

Intracellular responses of the rat cochlear nucleus to sound and its role in temporal coding.

The anteroventral cochlear nucleus (AVCN), the first centre of the central auditory pathway, contains globular bushy cells, which are unique in their ability to produce fast excitatory post-synaptic potentials (EPSPs). Using in vivo intracellular recordings in the rat AVCN we examined these fast EPSPs in relation to temporal coding. At frequencies up to 2.5 kHz, EPSPs were evoked on successive sine waves of the stimulus with EPSP summation limited. This one-to-one relationship between the EPSPs and the sound wave period was present at higher frequencies and over a greater intensity range than for action potentials. These results suggest that temporal coding is possible in globular bushy neurones by their ability to extract temporal information through fast processing of convergent presynaptic input.

Acoustic Stimulation↗