Physiological Identification of the Targets of Cartwheel Cells in the Dorsal Cochlear Nucleus

1997 ◽  
Vol 78 (1) ◽  
pp. 248-260 ◽  
Author(s):  
Nace L. Golding ◽  
Donata Oertel

Golding, Nace L. and Donata Oertel. Physiological identification of the targets of cartwheel cells in the dorsal cochlear nucleus. J. Neurophysiol. 78: 248–260, 1997. The integrative contribution of cartwheel cells of the dorsal cochlear nucleus (DCN) was assessed with intracellular recordings from anatomically identified cells. Recordings were made, in slices of the cochlear nuclei of mice, from 58 cartwheel cells, 22 fusiform cells, 3 giant cells, 5 tuberculoventral cells, and 1 cell that is either a superficial stellate or Golgi cell. Cartwheel cells can be distinguished electrophysiologically from other cells of the cochlear nuclei by their complex spikes, which comprised two to four rapid action potentials superimposed on a slower depolarization. The rapid action potentials were blocked by tetrodotoxin ( n = 17) and were therefore mediated by voltage-sensitive sodium currents. The slow spikes were eliminated by the removal of calcium from the extracellular saline ( n = 3) and thus were mediated by voltage-sensitive calcium currents. The spontaneous and evoked firing patterns of cartwheel cells were distinctive. Cartwheel cells usually fired single and complex spikes spontaneously at irregular intervals of between 100 ms and several seconds. Shocks to the DCN elicited firing that lasted tens to hundreds of milliseconds. With the use of these distinctive firing patterns, together with a pharmacological dissection of postsynaptic potentials (PSPs), possible targets of cartwheel cells were identified and the function of the connections was examined. Not only cartwheel and fusiform cells, but also giant cells, received patterns of synaptic input consistent with their having originated from cartwheel cells. These cell types responded to shocks of the DCN with variable trains of PSPs that lasted hundreds of milliseconds. PSPs within these trains appeared both singly and in bursts of two to four, and were blocked by 0.5 or 1 μM strychnine ( n = 4 cartwheel, 4 fusiform, and 2 giant cells), indicating that cartwheel cells are likely to be glycinergic. In contrast with cartwheel cells, which are weakly excited by glycinergic input, glycinergic PSPs consistently inhibited fusiform and giant cells. Tuberculoventral cells and the putative superficial stellate cell received little or no spontaneous synaptic activity. Shocks to the DCN evoked synaptic activity that lasted ∼5 ms. These cells therefore probably do not receive input from cartwheel cells. In addition, the brief firing of tuberculoventral cells and of the putative superficial stellate cell in response to shocks indicates that these cells are unlikely to contribute to the late, glycinergic synaptic potentials observed in cartwheel, fusiform, and giant cells.

1993 ◽  
Vol 69 (5) ◽  
pp. 1384-1397 ◽  
Author(s):  
S. Zhang ◽  
D. Oertel

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.


1995 ◽  
Vol 73 (2) ◽  
pp. 550-561 ◽  
Author(s):  
K. Parham ◽  
D. O. Kim

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.


2003 ◽  
Vol 89 (4) ◽  
pp. 2225-2237 ◽  
Author(s):  
Scott C. Molitor ◽  
Paul B. Manis

Simultaneous fluorescence imaging and electrophysiologic recordings were used to investigate the Ca2+ influx initiated by action potentials (APs) into dorsal cochlear nucleus (DCN) pyramidal cell (PC) and cartwheel cell (CWC) dendrites. Local application of Cd2+blocked Ca2+ transients in PC and CWC dendrites, demonstrating that the Ca2+ influx was initiated by dendritic Ca2+ channels. In PCs, TTX eliminated the dendritic Ca2+ transients when APs were completely blocked. However, the Ca2+ influx could be partially recovered during an incomplete block of APs or when a large depolarization was substituted for the blocked APs. In CWCs, dendritic Ca2+ transients evoked by individual APs, or simple spikes, were blocked by TTX and could be recovered during an incomplete block of APs or by a large depolarization. In contrast, dendritic Ca2+ transients evoked by complex spikes, a burst of APs superimposed on a slow depolarization, were not blocked by TTX, despite eliminating the APs superimposed on the slow depolarization. These results suggest two different mechanisms for the retrograde activation of dendritic Ca2+channels: the first requires fast Na+channel-mediated APs or a large somatic depolarization, whereas the second is independent of Na+ channel activation, requiring only the slow depolarization underlying complex spikes.


1993 ◽  
Vol 69 (5) ◽  
pp. 1398-1408 ◽  
Author(s):  
S. Zhang ◽  
D. Oertel

1. In slices of the murine cochlear nuclear complex, intracellular recordings were made from five giant cells that were identified by intracellular labeling with biocytin. Giant cells form one of the two output pathways of the dorsal cochlear nucleus (DCN). Understanding how neuronal circuits and intrinsic electrical properties interact to control the firing of giant cells is a step toward understanding what acoustic information is conveyed through these cells. 2. Cell bodies of the labeled giant cells lay in the deep layer of the DCN. Dendrites, widespread both along the isofrequency axis and along the tonotopic axis, occupied mainly the deep layer, but some distal ends strayed into the molecular layer. Axons of giant cells were large, varying between 1 and 2 microns diam, and left through the dorsal acoustic stria. They were not observed to branch in the cochlear nuclei. 3. Giant cells fired large, overshooting action potentials that were followed by two afterhyperpolarizations. The first brought the membrane potential below rest, independent of the strength of injected current. The more variable second one produced either an undershoot or an inflection in the membrane potential between action potentials. 4. In each of the five labeled giant cells, shocks to the nerve root or to the anteroventral cochlear nucleus (AVCN) evoked a monosynaptic excitatory postsynaptic potential and two tandem inhibitory postsynaptic potentials (IPSPs) in the first 10 ms. Later IPSPs followed after latencies of between 10 and 50 ms. Monosynaptic excitation was usually cut short by the inhibition. 5. Strychnine, at 1 microM, blocked all IPSPs in the one giant cell tested, indicating that inhibitory input to this giant cell from circuits intrinsic to the cochlear nuclear complex was glycinergic. 6. The location of afferents was mapped for two giant cells. Both excitatory and inhibitory inputs to giant cells could be driven by the local application of glutamate to many loci in the AVCN and posteroventral cochlear nucleus, indicating that the ventral cochlear nucleus VCN contains interneurons that are monosynaptically or polysynaptically connected to giant cells. 7. An interpretation consistent with the results is that giant cells are excited by auditory nerve fibers and are inhibited by tuberculoventral cells. Giant cells may also be excited by granule or T stellate cells.


2007 ◽  
Vol 97 (2) ◽  
pp. 1705-1725 ◽  
Author(s):  
Yuil Kim ◽  
Laurence O. Trussell

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+.


2009 ◽  
Vol 102 (2) ◽  
pp. 1287-1295 ◽  
Author(s):  
Jaime G. Mancilla ◽  
Paul B. Manis

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.


2010 ◽  
Vol 104 (5) ◽  
pp. 2462-2473 ◽  
Author(s):  
Michael T. Roberts ◽  
Laurence O. Trussell

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.


1994 ◽  
Vol 71 (2) ◽  
pp. 467-478 ◽  
Author(s):  
H. J. Waller ◽  
D. A. Godfrey

1. The cochlear nucleus of rat brain stem slices was explored with extracellular microelectrodes to determine the distribution and characteristics of spontaneously active neurons. 2. In mapping experiments few spontaneously active neurons were found in anteroventral or posteroventral divisions of the cochlear nucleus. In contrast, spontaneously active neurons (N = 648) were widely distributed in the dorsal cochlear nucleus (DCN), especially its more superficial part. The density (neurons per penetration) was greatest 100-400 microns from the lateral surface of DCN, corresponding approximately to the fusiform soma layer and closely adjacent portions of the molecular and deeper regions. In penetrations with active neurons as many as 13 were found, with a mean of 4.3 neurons per penetration. Activity was found along the entire dorsomedial-ventrolateral extent of the nucleus, across the tonotopic representation. 3. Most neurons were readily categorized according to the spike interval pattern as regular (40%), bursting (30%), or irregular (30%). Regular and bursting patterns were highly stable, but few bursting neurons were found in relatively inactive slices. Although there was extensive overlap in location, bursting neurons were significantly closer to the lateral edge of the slice. Also, they were more likely to have initially negative action potentials than regular or irregular neurons. 4. A high density of spontaneous firing, including regular, bursting, and irregular patterns, was observed in slices containing only DCN and adjacent fiber tracts, with other nuclear structures trimmed away. 5. When the K+ concentration of the perfusion medium was decreased from 6.25 to 3.25 mM firing rates of regular neurons decreased moderately without changes in pattern. In contrast, firing rates of most bursting and irregular neurons showed large increases, and bursts were prolonged. 6. When the K+ concentration was increased from 6.25 to 9.25 or 12.25 mM regular neurons showed moderate increases in rate without changes in pattern. Effects on firing rates differed among bursting and irregular neurons, but bursts usually increased in frequency and decreased in duration, and irregular neurons showed some burst firing. 7. When Ca2+ was decreased to 0.2 mM and Mg2+ increased to 3.8 or 7.8 mM regular neurons did not change in pattern of firing although firing rates increased or decreased moderately. Bursting neurons showed large increases in the durations of the bursts. Firing rates of bursting neurons usually increased during 0.2 mM Ca2+ -3.8 mM Mg2+ but typically decreased, after an initial rise, during 0.2 mM Ca2+ -7.8 mM Mg2+.(ABSTRACT TRUNCATED AT 400 WORDS)


2012 ◽  
Vol 107 (3) ◽  
pp. 824-835 ◽  
Author(s):  
Wei-Li Diana Ma ◽  
Stephan D. Brenowitz

Because of the availability of disease and genetic models, the mouse has become a valuable species for auditory neuroscience that will facilitate long-term goals of understanding neuronal mechanisms underlying the perception and processing of sounds. The goal of this study was to define the basic sound-evoked response properties of single neurons in the mouse dorsal cochlear nucleus (DCN). Neurons producing complex spikes were distinguished as cartwheel cells (CWCs), and other neurons were classified according to the response map scheme previously developed in DCN. Similar to observations in other rodent species, neurons of the mouse DCN exhibit relatively little sound-driven inhibition. As a result, type III was the most commonly observed response. Our findings are generally consistent with the model of DCN function that has been developed in the cat and the gerbil, suggesting that this in vivo mouse preparation will be a useful tool for future studies of auditory physiology.


1999 ◽  
Vol 82 (6) ◽  
pp. 3434-3457 ◽  
Author(s):  
Jiang Ding ◽  
Thane E. Benson ◽  
Herbert F. Voigt

In an effort to establish relationships between cell physiology and morphology in the dorsal cochlear nucleus (DCN), intracellular single-unit recording and marking experiments were conducted on decerebrate gerbils using horseradish peroxidase (HRP)- or neurobiotin-filled micropipettes. Intracellular responses to acoustic (tone and broadband noise bursts) and electric current-pulse stimuli were recorded and associated with cell morphology. Units were classified according to the response map scheme (type I to type V). Results from 19 identified neurons, including 13 fusiform cells, 2 giant cells, and 4 cartwheel cells, reveal correlations between cell morphology of these neurons and their acoustic responses. Most fusiform cells (8/13) are associated with type III unit response properties. A subset of fusiform cells was type I/III units (2), type III-i units (2), and a type IV-T unit. The giant cells were associated with type IV-i unit response properties. Cartwheel cells all had weak acoustic responses that were difficult to classify. Some measures of membrane properties also were correlated with cell morphology but to a lesser degree. Giant cells and all but one fusiform cell fired only simple action potentials (APs), whereas all cartwheel cells discharged complex APs. Giant and fusiform cells all had monotonic rate versus current level curves, whereas cartwheel cells had nonmonotonic curves. This implies that inhibitory acoustic responses, resulting in nonmonotonic rate versus sound level curves, are due to local inhibitory interactions rather than strictly to membrane properties. A complex-spiking fusiform cell with type III unit properties suggests that cartwheel cells are not the only complex-spiking cells in DCN. The diverse response properties of the DCN′s fusiform cells suggests that they are very sensitive to the specific complement of excitatory and inhibitory inputs they receive.


Sign in / Sign up

Export Citation Format

Share Document