Acoustic and Current-Pulse Responses of Identified Neurons in the Dorsal Cochlear Nucleus of Unanesthetized, Decerebrate Gerbils

1999 ◽  
Vol 82 (6) ◽  
pp. 3434-3457 ◽  
Author(s):  
Jiang Ding ◽  
Thane E. Benson ◽  
Herbert F. Voigt
Keyword(s):  
Cell Morphology ◽  
Giant Cells ◽  
Dorsal Cochlear Nucleus ◽  
Membrane Properties ◽  
Type I ◽  
Fusiform Cell ◽  
Response Properties ◽  
Type Iii ◽  
Acoustic Responses ◽  
Cartwheel Cells

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.

Intracellular Response Properties of Units in the Dorsal Cochlear Nucleus of Unanesthetized Decerebrate Gerbil

1997 ◽  
Vol 77 (5) ◽  
pp. 2549-2572 ◽  
Author(s):  
Jiang Ding ◽  
Herbert F. Voigt
Keyword(s):  
Dorsal Cochlear Nucleus ◽  
Type I ◽  
Type Ii ◽  
Response Properties ◽  
Type Iii ◽  
Type Iv ◽  
Rate Versus ◽  
Lower Maximum ◽  
Intracellular Response ◽  
Acoustic Responses

Ding, Jiang and Herbert F. Voigt. Intracellular response properties of units in the dorsal cochlear nucleus of unanesthetized decerebrate gerbil. J. Neurophysiol. 77: 2549–2572, 1997. Intracellular recording experiments on the dorsal cochlear nuclei of unanesthetized decerebrate gerbils were conducted. Acceptable recordings were those in which resting potentials were −50 mV or less and action potentials (APs) were ≥40 mV. Responses to short-duration tones and noise, and to current pulses delivered via recording electrodes, were acquired. Units were classified according to the response map scheme (types I–IV). Ninety-two acceptable recordings were made. Most units had simple APs (simple-spiking units); nine units had both simple and complex APs, which are bursts of spikes embedded on slow, transient depolarizations (complex-spiking units). Of 83 simple-spiking units, 46 were classified as follows: type I/III (9 units), type II (9 units), type III (25 units), type IV (2 units), and type IV-T (1 unit). One complex-spiking unit was classifiable (a type III unit); six were unclassifiable because of weak acoustic responses. Classifying 39 other simple-spiking units and 2 complex-spiking units was impossible, because they were either injured or lost before sufficient data were acquired. Many simple-spiking units showed depolarization or hyperpolarization (∼5–10 mV) during acoustic stimulation; some were hyperpolarized during the stimulus-off period. Type I/III units were not hyperpolarized during off-best-frequency (off-BF) stimulation. In contrast, many type II units were hyperpolarized by off-BF frequencies, suggesting that they received strong inhibitory sideband inputs. When inhibited, some type III units were hyperpolarized. Type IV units were hyperpolarized during inhibition even at low levels (<60 dB SPL); sustained depolarizations occurred only at higher levels, suggesting that they receive strong inhibitory and weak excitatory inputs. Several intracellular response properties were statistically different from those of extracellularly recorded units. Intracellularly recorded type II units had higher thresholds and lower maximum BF-driven and noise-driven rates than their extracellularly recorded counterparts. Type I/III units recorded intracellularly had lower maximum BF-driven rates. Type III units recorded intracellularly had higher maximum noise rates compared with those recorded extracellularly. Weaker acoustic responses most likely result from membrane disruption, but heightened responses may be related to weakened chloride-channel-dependent inhibition due to altered driving forces resulting from KCl leakage. Firing rates of simple-spiking units increased monotonically with increasing levels of depolarizing current pulses. In contrast, many complex-spiking units responded nonmonotonically to depolarizing current injection. The monotonic rate-versus-current curves and the nonmonotonic rate-versus-sound level curves of type IV and III units suggest that the acoustic behavior is the result of extrinsic inhibitory inputs and not due solely to intrinsic membrane properties.

Response properties of units in the dorsal cochlear nucleus of unanesthetized decerebrate gerbil

1996 ◽  
Vol 75 (4) ◽  
pp. 1411-1431 ◽  
Author(s):  
K. A. Davis ◽  
J. Ding ◽  
T. E. Benson ◽  
H. F. Voigt
Keyword(s):  
Dorsal Cochlear Nucleus ◽  
Type I ◽  
Type Ii ◽  
Decerebrate Cat ◽  
Excitatory Response ◽  
Type Iii ◽  
Type Iv ◽  
Noise Type ◽  
Rate Versus ◽  
Excitatory Responses

1. The electrophysiological responses of single units in the dorsal cochlear nucleus of unanesthetized decerebrate Mongolian gerbil (Meriones unguiculatus) were recorded. Units were classified according to the response map scheme of Evans and Nelson as modified by Young and Brownell, Young and Voigt, and Shofner and Young. Type II units have a V-shaped excitatory response map similar to typical auditory nerve tuning curves but little or no spontaneous activity (SpAc < 2.5 spikes/s) and little or no response to noise. Type I/III units also have a V-shaped excitatory map and SpAc < 2.5 spikes/s, but have an excitatory response to noise. Type III units have a V-shaped excitatory map with inhibitory sidebands, SpAc > 2.5 spikes/s, and an excitatory response to noise. Type IV-T units typically also have a V-shaped excitatory map with inhibitory sidebands, but have a highly nonmonotonic rate versus level response to best frequency (BF) tones like type IV units, SpAc > 2.5 spikes/s, and an excitatory response to noise. Type IV units have a predominantly inhibitory response map above an island of excitation of BF, SpAc > 2.5 spikes/s, and an excitatory response to noise. We present results for 133 units recorded with glass micropipette electrodes. The purpose of this study was to establish a normative response map data base in this species for ongoing structure/function and correlation studies. 2. The major types of units (type II, type I/III, type III, type IV-T, and type IV) found in decerebrate cat are found in decerebrate gerbil. However, the percentage of type II (7.5%) and type IV (11.3%) units encountered are smaller and the percentage of type III (62.4%) units is larger in decerebrate gerbil than in decerebrate cat. In comparison, Shofner and Young found 18.5% type II units, 30.6% type IV units, and 23.1% type III units using metal electrodes. 3. Two new unit subtypes are described in gerbil: type III-i and type IV-i units. Type III-i units are similar to type III units except that type III-i units are inhibited by low levels of noise and excited by high levels of noise whereas type III units have strictly excitatory responses to noise. Type IV-i units are similar to type IV units except that type IV-i units are excited by low levels of noise and become inhibited by high levels of noise whereas type IV units have strictly excitatory responses to noise. Type III-i units are approximately 30% of the type III population and type IV-i units are approximately 50% of the type IV population. 4. On the basis of the paucity of classic type II units and the reciprocal responses to broadband noise of type III-i and type IV-i units, we postulate that some gerbil type III-i units are the same cell type and have similar synaptic connections as cat type II units. 5. Type II and type I/III units are distinguished from one another on the basis of both their relative noise response, rho, and the normalized slope of the BF tone rate versus level functions beyond the first maximum. Previously, type II units were defined to be those nonspontaneously active units with rho values < 0.3 where rho is defined as the ratio of the maximum noise response minus spontaneous rate to the maximum BF tone response minus spontaneous rate. In the gerbil, the average rho value for type II units is 0.25, although a few values are > 0.3, and the rate-level curves are consistently nonmonotonic with normalized slopes steeper than than -0.007/dB. The average rho value for type I/III units is 0.54, although a few values are < 0.3, and the rate-level curves tend to saturate with slopes shallower than -0.006/dB. In general, the response properties of type II units recorded in gerbil are similar to those recorded in decerebrate cat. 6. In comparison to decerebrate cat, the lower percentage of type IV units recorded in decerebrate gerbil may be due to a species difference (a reduced number of type II units in gerbil) or an electrode bias.

Neural repetitive firing: a comparative study of membrane properties of crustacean walking leg axons

1975 ◽  
Vol 38 (4) ◽  
pp. 922-932 ◽  
Author(s):  
J. A. Connor
Keyword(s):  
Membrane Conductance ◽  
Firing Frequency ◽  
Membrane Properties ◽  
Constant Current ◽  
Repetitive Firing ◽  
Type I ◽  
Frequency Range ◽  
Type Iii ◽  
Range Type ◽  
Sucrose Gap

1. Repetitive activity and membrane conductance parameters of crab walking leg axons have been studied in the double sucrose gap. 2. The responses to constant current stimulus could be classified into three catagories; highly repetitive with wide firing frequency range, type I; highly repetitive with narrow frequency range, type II; and nonrepetitive or repetitive to only a limited degree, type III. The minimum firing frequency for type I axons was much greater than for other recording techniques. 3. Voltage-clamp currents in type III axons were qualitatively similar to those of squid or lobster axon. 4. The outward membrane currents of type I and II axons showed a transient phase in addition to the usual delayed current. The magnitude of this transient was a function of both the holding and test voltages. 5. The direction of the transient current reversed in potassium-rich saline. 6. The type I repetitive response in the walking leg axons appears to be generated by the same types of conductance changes that have been demonstrated in molluscan central neurons.

Membrane properties of mesopontine cholinergic neurons studied with the whole-cell patch-clamp technique: implications for behavioral state control

1992 ◽  
Vol 68 (4) ◽  
pp. 1359-1372 ◽  
Author(s):  
A. Kamondi ◽  
J. A. Williams ◽  
B. Hutcheon ◽  
P. B. Reiner
Keyword(s):  
Patch Clamp ◽  
Cholinergic Neurons ◽  
Membrane Properties ◽  
Type I ◽  
Type Ii ◽  
Patch Clamp Technique ◽  
Whole Cell ◽  
Type Iii ◽  
Clamp Technique ◽  
Whole Cell Patch Clamp

1. The whole-cell patch-clamp technique was used to study the membrane properties of identified cholinergic and noncholinergic laterodorsal tegmental neurons in slices of rat brain maintained in vitro. 2. On the basis of their expression of the transient outward potassium current IA and the transient inward calcium current IT, three classes of neurons were observed: type I neurons exhibited a large IT; type II neurons exhibited a prominent IA; and type III neurons exhibited both IA and IT. 3. Combining intracellular deposition of biocytin with NADPH diaphorase histochemistry revealed that the vast majority of type III neurons were cholinergic, whereas only a minority of type I and type II neurons were cholinergic. Thus mesopontine cholinergic neurons possess intrinsic ionic currents capable of inducing burst firing. 4. Delineation of the intrinsic membrane properties of identified mesopontine cholinergic neurons, in concert with recent results regarding the responses of these neurons to neurotransmitter agents, has led us to present a unifying and mechanistic hypothesis of brain stem cholinergic function in the control of behavioral states.

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.

scholarly journals Oxytocin selectively excites interneurons and inhibits output neurons of the bed nucleus of the stria terminalis (BNST)

2020 ◽  
Author(s):  
Walter Francesconi ◽  
Fulvia Berton ◽  
Valentina Olivera-Pasilio ◽  
Joanna Dabrowska
Keyword(s):  
Male Rats ◽  
Membrane Properties ◽  
Projection Neurons ◽  
Type I ◽  
Stria Terminalis ◽  
Type Ii ◽  
Spontaneous Firing ◽  
Bed Nucleus ◽  
Type Iii ◽  
Output Neurons

AbstractThe dorsolateral bed nucleus of the stria terminalis (BNSTDL) has high expression of oxytocin receptors, but their role in the modulation of BNSTDL activity remains elusive. BNSTDL contains GABA-ergic neurons classified based on intrinsic membrane properties into three types. Using in vitro patch-clamp and cell-attached recordings in male rats, we demonstrate that oxytocin excites and increases spontaneous firing of Type I, putative BNSTDL interneurons. As a consequence, oxytocin increases the frequency of spontaneous inhibitory post-synaptic currents (sIPSCs) (tetrodotoxin-sensitive) and reduces spontaneous firing of Type II neurons. In contrast, in Type III neurons, oxytocin reduces the amplitude of both sIPSCs and evoked IPSCs, suggesting a direct postsynaptic inhibitory effect. As Type II and Type III are the BNSTDL projection neurons, we present a model of fine-tuned modulation by oxytocin, which selectively excites Type I BNSTDL interneurons and inhibits Type II and Type III output neurons, via an indirect and direct mechanism, respectively.

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

2006 ◽  
Vol 216-217 ◽  
pp. 207-215 ◽  
Author(s):  
Donald M. Caspary ◽  
Larry F. Hughes ◽  
Tracy A. Schatteman ◽  
Jeremy G. Turner
Keyword(s):  
Cochlear Nucleus ◽  
Dorsal Cochlear Nucleus ◽  
Response Properties ◽  
Age Related ◽  
Age Related Changes ◽  
Cartwheel Cells

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
Keyword(s):  
Cochlear Nucleus ◽  
Action Potentials ◽  
Stellate Cell ◽  
Giant Cells ◽  
Dorsal Cochlear Nucleus ◽  
Synaptic Activity ◽  
Cochlear Nuclei ◽  
Rapid Action ◽  
Complex Spikes ◽  
Cartwheel Cells

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.

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