scholarly journals Loose coupling between SK and P/Q-type Ca2+ channels in cartwheel cells of the dorsal cochlear nucleus

2019 ◽  
Vol 122 (4) ◽  
pp. 1721-1727 ◽  
Author(s):  
Tomohiko Irie
Keyword(s):  
Endoplasmic Reticulum ◽  
Cochlear Nucleus ◽  
Brain Slices ◽  
Bk Channels ◽  
Dorsal Cochlear Nucleus ◽  
Loose Coupling ◽  
Sk Channels ◽  
Action Potential Firing ◽  
Small Conductance ◽  
Cartwheel Cells

Small-conductance Ca2+-activated K+ (SK) and large-conductance voltage- and Ca2+-activated K+ (BK) channels are Ca2+-activated K+ channels that control action potential firing in diverse neurons in the brain. In cartwheel cells of the dorsal cochlear nucleus, blockade of either channel type leads to excessive production of spike bursts. In the same cells, P/Q-type Ca2+ channels in plasma membrane and ryanodine receptors in endoplasmic reticulum supply Ca2+ to BK channels through Ca2+ nanodomain signaling. In this study, voltage-clamp experiments were performed in cartwheel cells in mouse brain slices to examine the Ca2+ signaling pathways underlying activation of SK channels. As with BK channels, SK channels required the activity of P/Q-type Ca2+ channels. However, this signaling occurred across Ca2+ micro- rather than nanodomain distances and was independent of Ca2+ release from endoplasmic reticulum. These differential modes of activation may lead to distinct time courses of the two K+ currents and therefore control excitability of auditory neurons across different timescales. NEW & NOTEWORTHY This study has shown for the first time that in cartwheel cells of the dorsal cochlear nucleus, small-conductance Ca2+-activated K+ (SK) channels were triggered by the activation of P/Q-type Ca2+ channels in which SK–P/Q-type coupling is mediated within the Ca2+ microdomains (loose coupling). Although Ca2+-induced Ca2+ release is able to activate large-conductance voltage- and Ca2+-activated K+ (BK) channels in cartwheel cells, it did not contribute to SK activation.

Ion Channels Generating Complex Spikes in Cartwheel Cells of the Dorsal Cochlear Nucleus

2007 ◽  
Vol 97 (2) ◽  
pp. 1705-1725 ◽  
Author(s):  
Yuil Kim ◽  
Laurence O. Trussell
Keyword(s):  
Ion Channels ◽  
Cochlear Nucleus ◽  
Brain Slices ◽  
Bk Channels ◽  
Dorsal Cochlear Nucleus ◽  
Sk Channels ◽  
Negative Membrane Potential ◽  
Patch Technique ◽  
Complex Spikes ◽  
Cartwheel Cells

Cartwheel cells are glycinergic interneurons that modify somatosensory input to the dorsal cochlear nucleus. They are characterized by firing of mixtures of both simple and complex action potentials. To understand what ion channels determine the generation of these two types of spike waveforms, we recorded from cartwheel cells using the gramicidin perforated-patch technique in brain slices of mouse dorsal cochlear nucleus and applied channel-selective blockers. Complex spikes were distinguished by whether they arose directly from a negative membrane potential or later during a long depolarization. Ca2+ channels and Ca2+-dependent K+ channels were major determinants of complex spikes. Onset complex spikes required T-type and possibly R-type Ca2+ channels and were shaped by BK and SK K+ channels. Complex spikes arising later in a depolarization were dependent on P/Q- and L-type Ca2+ channels as well as BK and SK channels. BK channels also contributed to fast repolarization of simple spikes. Simple spikes featured an afterdepolarization that is probably the trigger for complex spiking and is shaped by T/R-type Ca2+ and SK channels. Fast spikes were dependent on Na+ channels; a large persistent Na+ current may provide a depolarizing drive for spontaneous activity in cartwheel cells. Thus the diverse electrical behavior of cartwheel cells is determined by the interaction of a wide variety of ion channels with a prominent role played by Ca2+.

scholarly journals Two Distinct Types of Inhibition Mediated by Cartwheel Cells in the Dorsal Cochlear Nucleus

2009 ◽  
Vol 102 (2) ◽  
pp. 1287-1295 ◽  
Author(s):  
Jaime G. Mancilla ◽  
Paul B. Manis
Keyword(s):  
Cochlear Nucleus ◽  
Reversal Potential ◽  
Dorsal Cochlear Nucleus ◽  
Synaptic Function ◽  
Half Width ◽  
Neonatal Rat ◽  
Projection Neurons ◽  
Paired Pulse ◽  
Dependent Inhibition ◽  
Cartwheel Cells

Individual neurons have been shown to exhibit target cell-specific synaptic function in several brain areas. The time course of the postsynaptic conductances (PSCs) strongly influences the dynamics of local neural networks. Cartwheel cells (CWCs) are the most numerous inhibitory interneurons in the dorsal cochlear nucleus (DCN). They are excited by parallel fiber synapses, which carry polysensory information, and in turn inhibit other CWCs and the main projection neurons of the DCN, pyramidal cells (PCs). CWCs have been implicated in “context-dependent” inhibition, producing either depolarizing (other CWCs) or hyperpolarizing (PCs) post synaptic potentials. In the present study, we used paired whole cell recordings to examine target-dependent inhibition from CWCs in neonatal rat DCN slices. We found that CWC inhibitory postsynaptic potentials (IPSPs) onto PCs are large (1.3 mV) and brief (half-width = 11.8 ms), whereas CWC IPSPs onto other CWCs are small (0.2 mV) and slow (half-width = 36.8 ms). Evoked IPSPs between CWCs exhibit paired-pulse facilitation, while CWC IPSPs onto PCs exhibit paired-pulse depression. Perforated-patch recordings showed that spontaneous IPSPs in CWCs are hyperpolarizing at rest with a mean estimated reversal potential of −67 mV. Spontaneous IPSCs were smaller and lasted longer in CWCs than in PCs, suggesting that the kinetics of the receptors are different in the two cell types. These results reveal that CWCs play a dual role in the DCN. The CWC-CWC network interactions are slow and sensitive to the average rate of CWC firing, whereas the CWC-PC network is fast and sensitive to transient changes in CWC firing.

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

2010 ◽  
Vol 104 (5) ◽  
pp. 2462-2473 ◽  
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.

Metabolism of the dorsal cochlear nucleus in rat brain slices

2000 ◽  
Vol 143 (1-2) ◽  
pp. 115-129 ◽  
Author(s):  
Li Zheng ◽  
Donald A Godfrey ◽  
Hardress J Waller ◽  
Timothy G Godfrey ◽  
Kejian Chen ◽  
...  
Keyword(s):  
Rat Brain ◽  
Cochlear Nucleus ◽  
Brain Slices ◽  
Dorsal Cochlear Nucleus

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

1993 ◽  
Vol 69 (5) ◽  
pp. 1384-1397 ◽  
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.

Spontaneous and sound-evoked discharge characteristics of complex-spiking neurons in the dorsal cochlear nucleus of the unanesthetized decerebrate cat

1995 ◽  
Vol 73 (2) ◽  
pp. 550-561 ◽  
Author(s):  
K. Parham ◽  
D. O. Kim
Keyword(s):  
Cochlear Nucleus ◽  
Pure Tone ◽  
Broadband Noise ◽  
Dorsal Cochlear Nucleus ◽  
Projection Neurons ◽  
Response Latencies ◽  
Discharge Characteristics ◽  
Decerebrate Cat ◽  
Complex Spikes ◽  
Cartwheel Cells

1. We examined the spontaneous and sound-evoked discharge characteristics of 20 complex-spiking units recorded in the dorsal cochlear nucleus (DCN) of 15 unanesthetized, decerebrate cats. 2. The extracellularly recorded complex spikes consisted of bursts of two to five action potentials whose size gradually decreased during the burst. Complex spikes were observed both in the spontaneous and sound-evoked activity of the units in our sample. 3. The spontaneous rates (SRs) of DCN complex-spiking units ranged from 0 to 30 spikes/s. Spontaneous activity consisted of complex and simple (i.e., the common single neuronal action potential) spikes. Comparison of the SR distributions of the DCN complex-spiking units with that of a total sample of 194 DCN units (from 9 cats) suggests that the complex-spiking units tended to be in the lower half of the DCN SR distribution. 4. Sound-evoked discharges could consist of both complex and simple spikes. On the basis of their sound-driven responses, we divided the DCN complex-spiking units into two groups. The majority (15 of 20, 75%) were weakly driven by pure tones and inhibited by broadband noise. They tended to have broad response areas. Their response latencies to pure tone and noise stimuli were relatively long (10-20 ms). The recording depths of these units tended to be superficial (i.e., 10 of 15 units were located within 400 microns of the dorsal surface of the DCN). A minority (5 of 20, 25%) of the complex-spiking units were strongly driven by pure tone and broadband noise stimuli. These units had more clearly defined excitatory regions of response areas than the weakly driven units. Their response latencies to pure tone and noise stimuli were short (< 10 ms). The recording depths of these units tended to be deeper (i.e., 4 of 5 units were located at 400-700 microns) than those of the weakly driven units. 5. Intracellular recording and labeling studies of in vitro DCN slice preparations have correlated complex spikes with the superficially located cartwheel cells. Given the complex spikes of the units, many of which were located superficially, we suggest that our sample, particularly the weakly driven group of neurons, corresponds to the cartwheel cells. 6. Cartwheel cells are putative inhibitory interneurons whose axons primarily contact on the main projection neurons of DCN, the fusiform cells. The present finding of sound-evoked discharges by the superficially located complex-spiking units suggests that cartwheel cells should play a role in modifying the sound-evoked responses of the fusiform cells.

Immunocytochemical localization of glycine in a subset of cartwheel cells of the dorsal cochlear nucleus in rats

1996 ◽  
Vol 96 (1-2) ◽  
pp. 157-166 ◽  
Author(s):  
Troy S. Gates ◽  
Diana L. Weedman ◽  
Tan Pongstaporn ◽  
David K. Ryugo
Keyword(s):  
Cochlear Nucleus ◽  
Dorsal Cochlear Nucleus ◽  
Immunocytochemical Localization ◽  
Cartwheel Cells

scholarly journals Development of spontaneous firing of fusiform neurons from the dorsal cochlear nucleus of mice occurs after hearing onset

2021 ◽  
Author(s):  
Nikollas M. Benites ◽  
Beatriz Rodrigues ◽  
Carlos H. Silveira ◽  
Ricardo M. Leão
Keyword(s):  
Action Potential ◽  
Cochlear Nucleus ◽  
Sodium Current ◽  
Dorsal Cochlear Nucleus ◽  
Active State ◽  
Membrane Properties ◽  
Action Potential Firing ◽  
Electrophysiological Properties ◽  
Somatosensory Information ◽  
Potential Firing

AbstractThe dorsal cochlear nucleus (DCN) in the auditory brainstem integrates auditory and somatosensory information. Mature fusiform neurons express two qualitative intrinsic states in equal proportions: quiet, with no spontaneous regular action potential firing, or active, with regular spontaneous action potential firing. However, how these firing states and other electrophysiological properties of fusiform neurons develop during early postnatal days to adulthood is not known. Thus, we recorded fusiform neurons from mice from P4 to P21 and analyzed their electrophysiological properties. In the pre-hearing phase (P4-P13), we found that fusiform neurons are mostly quiet, with the active state emerging after hearing onset at P14. Subthreshold properties present more variations before hearing onset, while action potential properties vary more after P14, developing bigger, shorter, and faster action potentials. Interestingly, the activity threshold is more depolarized in pre-hearing cells suggesting that persistent sodium current (INaP) increases its expression after hearing. In fact, INaP increases its expression after hearing, accordingly with the development of active neurons. Thus, we suggest that the post-hearing expression of INaP creates the active state of the fusiform neuron. At the same time, other changes refine the passive membrane properties and increase the speed of action potential firing of fusiform neurons.

scholarly journals Classification of Neurons in the Adult Mouse Cochlear Nucleus: Linear Discriminant Analysis

2019 ◽  
Author(s):  
Paul B. Manis ◽  
Michael R. Kasten ◽  
Ruili Xie
Keyword(s):  
Discriminant Analysis ◽  
Linear Discriminant Analysis ◽  
Time Constant ◽  
Cochlear Nucleus ◽  
Brain Slices ◽  
Stellate Cells ◽  
Dorsal Cochlear Nucleus ◽  
Morphological Identification ◽  
Linear Discriminant ◽  
Principal Axes

AbstractThe cochlear nucleus (CN) transforms the spike trains of spiral ganglion cells into a new set of sensory representations that are essential for auditory discriminations and perception. These transformations require the coordinated activity of different classes of neurons that are embryologically derived from distinct sets of precursors. Decades of investigation have shown that the neurons of the CN are differentiated by their ion channel expression and intrinsic excitability. In the present study we have used linear discriminant analysis (LDA) to perform an unbiased analysis of measures of the responses of CN neurons to current injections to mathematically separate cells on the basis of both morphology and physiology. Recordings were made from cells in brain slices from CBA mice and a transgenic mouse line, NF107, crossed against the Ai32 line. For each cell, responses to current injections were analyzed for spike rate, spike shape (action potential height, afterhyperpolarization depth, first spike half-width), input resistance, resting membrane potential, membrane time constant, hyperpolarization-activated sag and time constant. Cells were filled with dye for morphological classification, and visually classified according to published accounts. The different morphological classes of cells were separated with the LDA. Ventral cochlear nucleus (VCN) bushy cells, planar multipolar (T-stellate) cells, and radiate multipolar (D-stellate) cells were in separate clusters, and were also separated from all of the neurons from the dorsal cochlear nucleus (DCN). Within the DCN, the pyramidal cells and tuberculoventral cells were largely separated from a distinct clusters of cartwheel cells. DCN cells fell largely within a plane in the first 3 principal axes, whereas VCN cells were in 3 clouds approximately orthogonal to this plane. VCN neurons from the two mouse strains were slightly separated, indicating either a strain dependence or the differences in slice preparation methods. We conclude that cochlear nucleus neurons can be objectively distinguished based on their intrinsic electrical properties, but that such distinctions are still best aided by morphological identification.

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