Physiological studies on neurons in the dorsal cochlear nucleus of cat

Results reported here support the conclusion that an individual neuron in the dorsal cochlear nucleus (DCN) can exhibit pauser, buildup, and chopper patterns in response to tone pips. Fusiform cells have been previously identified as the principal cell exhibiting these patterns. Fusiform cells can also exhibit an onset response followed by suppression of spontaneous activity at their characteristic frequency (CF). Off CF only suppression is seen. These neurons are characterized by a restricted excitatory region near threshold. All these cells can exhibit nonmonotonic rate curves, narrow excitatory regions, and inhibitory sidebands. Nonmonotonicity occurred in 34% of pausers, 52% of buildup, 89% of onsets with a graded response, and 50% overall in the DCN cells. Chopper units occur as often as the other types combined in the DCN. Only 14% show nonmonotonic rate curves. Those with high-spontaneous activity also show inhibitory sidebands. Cells with a predominant buildup pattern occur most frequently in the fusiform cell layer, whereas pausers occur throughout the DCN below the molecular layer. Intracellular potentials often reflect the average response pattern. Sharply delimited response areas indicate that these cells may be useful for performing a spectral analysis. These cells show almost no phase locking suggesting that temporal encoding is an unlikely function. It is suggested that the effects of anesthetic on the function of the DCN is not as marked as previously indicated.

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Vertical Cell Responses to Sound in Cat Dorsal Cochlear Nucleus

Journal of Neurophysiology ◽

10.1152/jn.1999.82.2.1019 ◽

1999 ◽

Vol 82 (2) ◽

pp. 1019-1032 ◽

Cited By ~ 43

Author(s):

William S. Rhode

Keyword(s):

Cochlear Nucleus ◽

Auditory Nerve ◽

Molecular Layer ◽

Broadband Noise ◽

Dorsal Cochlear Nucleus ◽

Type Ii ◽

Fusiform Cell ◽

Sound Sources ◽

Tuning Curves ◽

Axonal Arbors

The dorsal cochlear nucleus receives input from the auditory nerve and relays acoustic information to the inferior colliculus. Its principal cells receive two systems of inputs. One system through the molecular layer carries multimodal information that is processed through a neuronal circuit that resembles the cerebellum. A second system through the deep layer carries primary auditory nerve input, some of which is relayed through interneurons. The present study reveals the morphology of individual interneurons and their local axonal arbors and how these inhibitory interneurons respond to sound. Vertical cells lie beneath the fusiform cell layer. Their dendritic and axonal arbors are limited to an isofrequency lamina. They give rise to pericellular nests around the base of fusiform cells and their proximal basal dendrites. These cells exhibit an onset-graded response to short tones and have response features defined as type II. They have tuning curves that are closed contours (0 shaped), thresholds ∼27 dB SPL, spontaneous firing rates of ∼0 spikes/s, and they respond weakly or not at all to broadband noise, as described for type II units. Their responses are nonmonotonic functions of intensity with peak responses between 30 and 60 dB SPL. They also show a preference for the high-to-low direction of a frequency sweep. It has been suggested that these circuits may be involved in the processing of spectral cues for the localization of sound sources.

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Cartwheel and superficial stellate cells of the dorsal cochlear nucleus of mice: intracellular recordings in slices

Journal of Neurophysiology ◽

10.1152/jn.1993.69.5.1384 ◽

1993 ◽

Vol 69 (5) ◽

pp. 1384-1397 ◽

Cited By ~ 103

Author(s):

S. Zhang ◽

D. Oertel

Keyword(s):

Cochlear Nucleus ◽

Nerve Root ◽

Action Potentials ◽

Stellate Cell ◽

Molecular Layer ◽

Dorsal Cochlear Nucleus ◽

Fusiform Cell ◽

Parasagittal Plane ◽

Axonal Arbors ◽

Cartwheel Cells

1. Intracellular recordings were made from identified cartwheel and stellate cells in the molecular and fusiform cell layers of the murine dorsal cochlear nucleus (DCN). The aim of the study was to identify and characterize their synaptic inputs and to learn how synaptic inputs and intrinsic electrical properties interact to generate firing patterns. 2. Eight cells labeled by the intracellular injection of biocytin were cartwheel cells. Their axon terminals extended from the deep part of the molecular layer through the fusiform cell layer. Their dendrites extended through the molecular layer and had spines. Both the dendritic and axonal arbors were small, having diameters of approximately 150 microns in the parasagittal plane. 3. When depolarized, cartwheel cells often fired bursts of rapid action potentials superimposed on a slow depolarization. The peaks of action potentials were usually overshooting. Individually occurring action potentials were followed by two afterhyperpolarizations, as in other cells of the DCN. During bursts, action potentials did not have two distinct repolarizing phases. 4. Excitatory postsynaptic potentials (EPSPs) were recorded from cartwheel cells spontaneously and after shocks to the nerve root or to the ventral cochlear nucleus (VCN). The EPSPs rose slowly. When they were suprathreshold they evoked action potentials singly or in bursts. EPSPs evoked by shocks to the nerve root or to the VCN had long latencies, the rise of EPSPs beginning between 5 and 10 ms after the shock. No inhibitory synaptic potentials, either spontaneous or driven with electrical stimulation, were detected in cells whose resting potentials were between -50 and -70 mV. 5. The locations from which excitatory input can be driven electrically are consistent with cartwheel cells receiving excitatory synaptic input from granule cells. 6. One labeled cell was a superficial stellate cell. It had smooth, straight dendrites that radiated parallel to the layers of the DCN; its axonal arbor was also planar and was restricted to the molecular layer. Both the dendritic and axonal arbors of this stellate cell were large, > 500 microns diam in the parasagittal plane. 7. The superficial stellate cell fired trains of action potentials at regular intervals that, like other cells of the DCN, were overshooting and were followed by double undershoots. 8. Shocks to the nerve root and to the surface of the VCN evoked EPSPs after 3.5 and 2 ms, respectively, in the superficial stellate cell. Chemical stimulation of the VCN also evoked excitation. No inhibitory synaptic input, spontaneous or driven, was detected.

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Muscarinic acetylcholine receptors control baseline activity and Hebbian stimulus timing-dependent plasticity in fusiform cells of the dorsal cochlear nucleus

Journal of Neurophysiology ◽

10.1152/jn.00270.2016 ◽

2017 ◽

Vol 117 (3) ◽

pp. 1229-1238 ◽

Cited By ~ 11

Author(s):

Roxana A. Stefanescu ◽

Susan E. Shore

Keyword(s):

Spontaneous Activity ◽

Cochlear Nucleus ◽

Acetylcholine Receptors ◽

Dorsal Cochlear Nucleus ◽

Muscarinic Acetylcholine Receptors ◽

Fusiform Cell ◽

Baseline Activity ◽

Stimulus Timing

Cholinergic modulation contributes to adaptive sensory processing by controlling spontaneous and stimulus-evoked neural activity and long-term synaptic plasticity. In the dorsal cochlear nucleus (DCN), in vitro activation of muscarinic acetylcholine receptors (mAChRs) alters the spontaneous activity of DCN neurons and interacts with N-methyl-d-aspartate (NMDA) and endocannabinoid receptors to modulate the plasticity of parallel fiber synapses onto fusiform cells by converting Hebbian long-term potentiation to anti-Hebbian long-term depression. Because noise exposure and tinnitus are known to increase spontaneous activity in fusiform cells as well as alter stimulus timing-dependent plasticity (StTDP), it is important to understand the contribution of mAChRs to in vivo spontaneous activity and plasticity in fusiform cells. In the present study, we blocked mAChRs actions by infusing atropine, a mAChR antagonist, into the DCN fusiform cell layer in normal hearing guinea pigs. Atropine delivery leads to decreased spontaneous firing rates and increased synchronization of fusiform cell spiking activity. Consistent with StTDP alterations observed in tinnitus animals, atropine infusion induced a dominant pattern of inversion of StTDP mean population learning rule from a Hebbian to an anti-Hebbian profile. Units preserving their initial Hebbian learning rules shifted toward more excitatory changes in StTDP, whereas units with initial suppressive learning rules transitioned toward a Hebbian profile. Together, these results implicate muscarinic cholinergic modulation as a factor in controlling in vivo fusiform cell baseline activity and plasticity, suggesting a central role in the maladaptive plasticity associated with tinnitus pathology. NEW & NOTEWORTHY This study is the first to use a novel method of atropine infusion directly into the fusiform cell layer of the dorsal cochlear nucleus coupled with simultaneous recordings of neural activity to clarify the contribution of muscarinic acetylcholine receptors (mAChRs) to in vivo fusiform cell baseline activity and auditory-somatosensory plasticity. We have determined that blocking the mAChRs increases the synchronization of spiking activity across the fusiform cell population and induces a dominant pattern of inversion in their stimulus timing-dependent plasticity. These modifications are consistent with similar changes established in previous tinnitus studies, suggesting that mAChRs might have a critical contribution in mediating the maladaptive alterations associated with tinnitus pathology. Blocking mAChRs also resulted in decreased fusiform cell spontaneous firing rates, which is in contrast with their tinnitus hyperactivity, suggesting that changes in the interactions between the cholinergic and GABAergic systems might also be an underlying factor in tinnitus pathology.

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Somatosensory effects on neurons in dorsal cochlear nucleus

Journal of Neurophysiology ◽

10.1152/jn.1995.73.2.743 ◽

1995 ◽

Vol 73 (2) ◽

pp. 743-765 ◽

Cited By ~ 129

Author(s):

E. D. Young ◽

I. Nelken ◽

R. A. Conley

Keyword(s):

Electrical Stimulation ◽

Evoked Potentials ◽

Cochlear Nucleus ◽

Evoked Potential ◽

Deep Layer ◽

Molecular Layer ◽

Dorsal Cochlear Nucleus ◽

Fusiform Cell ◽

Principal Cells ◽

Type Iv

1. Single units and evoked potentials were recorded in dorsal cochlear nucleus (DCN) in response to electrical stimulation of the somatosensory dorsal column and spinal trigeminal nuclei (together called MSN for medullary somatosensory nuclei) and for tactile somatosensory stimuli. Recordings were from paralyzed decerebrate cats. 2. DCN principal cells (type IV units) were strongly inhibited by electrical stimulation (single 50-microA bipolar pulse) in MSN or by somatosensory stimulation. Units recorded in the fusiform cell and deep layers of DCN were inhibited, suggesting that the inhibition affects both types of principal cells (i.e., both fusiform and giant cells). 3. Interneurons (type II units) that inhibit principal cells were only weakly inhibited by electrical stimulation and were never excited, demonstrating that the inhibitory effect on principal cells does not pass through the type II circuit. In the vicinity of the DCN/PVCN (posteroventral cochlear nucleus) boundary, units were encountered that were excited by electrical stimulation in MSN; some of these neurons responded to sound, and some did not. Their response properties are consistent with the hypothesis that they are deep-layer inhibitory interneurons conveying somatosensory information to the DCN. 4. Analysis of the evoked potentials produced by electrical stimulation in MSN suggests that the somatosensory inputs activate the granule cell system of the DCN molecular layer. A model based on previous work by Klee and Rall was used to show that the distribution of evoked potentials in DCN can be explained as resulting from radial currents produced in the DCN molecular and fusiform-cell layers by synchronous activation of granule cells inputs to fusiform and cartwheel cells. Current-source density analysis of the evoked potentials is consistent with this model. Thus molecular layer interneurons (cartwheel and stellate cells) are a second possible source of inhibition to principal cells. 5. With lower stimulus levels (20 microA) and pulse-pair stimuli (50- to 100-ms interstimulus interval), three components of the inhibitory response can be recognized in both fusiform cell layer and deep layer type IV units: a short-latency inhibition that begins before the start of the evoked potential; a longer-latency inhibition whose timing corresponds to the evoked potential; and an excitatory component that occurs on the rising phase of the evoked potential. The excitatory component is usually overwhelmed by the inhibitory components and could be derived from granule cell inputs; the long-latency inhibitory component could be derived from cartwheel cells or the hypothesized deep-layer inhibitory interneurons.(ABSTRACT TRUNCATED AT 400 WORDS)

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Mechanisms of Onset Responses in Octopus Cells of the Cochlear Nucleus: Implications of a Model

Journal of Neurophysiology ◽

10.1152/jn.1997.78.2.872 ◽

1997 ◽

Vol 78 (2) ◽

pp. 872-883 ◽

Cited By ~ 15

Author(s):

Yidao Cai ◽

Edward J. Walsh ◽

JoAnn McGee

Keyword(s):

Cochlear Nucleus ◽

Response Pattern ◽

Compartment Model ◽

Ionic Channels ◽

Nerve Fibers ◽

Threshold Channel ◽

Slow Kinetics ◽

Low Threshold ◽

Onset Response ◽

Onset Responses

Cai, Yidao, Edward J. Walsh, and JoAnn McGee. Mechanisms of onset responses in octopus cells of the cochlear nucleus: implications of a model. J. Neurophysiol. 78: 872–883, 1997. The octopus cells of the posteroventral cochlear nucleus receive inputs from auditory-nerve fibers and form one of the major ascending auditory pathways. They respond to acoustic and electrical stimulation transiently and are believed to carry temporal information in the precise timing of their action potentials. The mechanism whereby onset responses are generated is not clear. Proposals aimed at elucidating the mechanism range from neural circuitry and/or inhibition, “depolarization block” (or inactivation of Na+ channels), and the involvement of a 4-aminopyridine (4-AP)–sensitive, low-threshold channel (KLT). In the present study, we used a compartment model to investigate possible mechanisms. The model cell contains a soma, an axon, and four passive dendrites. Four kinds of ionic channels were included in the soma compartment: the Hodgkin-Huxley–like Na+ and K+ channels, a 4-AP–sensitive, low-threshold channel, KLT, and a Cs+-sensitive, hyperpolarization-activated inward rectifier, I h . DC currents and half-wave–rectified sinewaves were used as stimuli. Our results showed that an onset response can be generated in the absence of neuronal circuitry of any form, thus suggesting that the onset response in octopus cells is regulated intrinsically. Among the many factors involved, low-input impedance, partly contributed by I h , appears to be essential to the basic onset response pattern; also, the KLT conductance plays a major role, whereas the inactivation of Na+ channels probably plays only a secondary role. The dynamics of I h also can modify the response pattern, but due to its slow kinetics, its role is probably limited to longer-term regulation under the conditions simulated in this study.

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Molecular Layer Inhibitory Interneurons Provide Feedforward and Lateral Inhibition in the Dorsal Cochlear Nucleus

Journal of Neurophysiology ◽

10.1152/jn.00312.2010 ◽

2010 ◽

Vol 104 (5) ◽

pp. 2462-2473 ◽

Cited By ~ 24

Author(s):

Michael T. Roberts ◽

Laurence O. Trussell

Keyword(s):

Brain Stem ◽

Lateral Inhibition ◽

Cochlear Nucleus ◽

Molecular Layer ◽

Dorsal Cochlear Nucleus ◽

Inhibitory Input ◽

Auditory Information ◽

Parallel Fibers ◽

Sensory Inputs ◽

Cartwheel Cells

In the outer layers of the dorsal cochlear nucleus, a cerebellum-like structure in the auditory brain stem, multimodal sensory inputs drive parallel fibers to excite both principal (fusiform) cells and inhibitory cartwheel cells. Cartwheel cells, in turn, inhibit fusiform cells and other cartwheel cells. At the microcircuit level, it is unknown how these circuit components interact to modulate the activity of fusiform cells and thereby shape the processing of auditory information. Using a variety of approaches in mouse brain stem slices, we investigated the synaptic connectivity and synaptic strength among parallel fibers, cartwheel cells, and fusiform cells. In paired recordings of spontaneous and evoked activity, we found little overlap in parallel fiber input to neighboring neurons, and activation of multiple parallel fibers was required to evoke or alter action potential firing in cartwheel and fusiform cells. Thus neighboring neurons likely respond best to distinct subsets of sensory inputs. In contrast, there was significant overlap in inhibitory input to neighboring neurons. In recordings from synaptically coupled pairs, cartwheel cells had a high probability of synapsing onto nearby fusiform cells or other nearby cartwheel cells. Moreover, single cartwheel cells strongly inhibited spontaneous firing in single fusiform cells. These synaptic relationships suggest that the set of parallel fibers activated by a particular sensory stimulus determines whether cartwheel cells provide feedforward or lateral inhibition to their postsynaptic targets.

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