Postnatal Changes in Membrane Properties of Mice Trigeminal Ganglion Neurons

2002 ◽  
Vol 87 (5) ◽  
pp. 2398-2407 ◽  
Author(s):  
Carmen Cabanes ◽  
Mikel López de Armentia ◽  
Félix Viana ◽  
Carlos Belmonte

Intracellular recordings from neurons in the mouse trigeminal ganglion (TG) in vitro were used to characterize changes in membrane properties that take place from early postnatal stages (P0–P7) to adulthood (>P21). All neonatal TG neurons had uniformly slow conduction velocities, whereas adult neurons could be separated according to their conduction velocity into Aδ and C neurons. Based on the presence or absence of a marked inflection or hump in the repolarization phase of the action potential (AP), neonatal neurons were divided into S- (slow) and F-type (fast) neurons. Their passive and subthreshold properties (resting membrane potential, input resistance, membrane capacitance, and inward rectification) were nearly identical, but they showed marked differences in AP amplitude, AP overshoot, AP duration, rate of AP depolarization, rate of AP repolarization, and afterhyperpolarization (AHP) duration. Adult TG neurons also segregated into S- and F-type groups. Differences in their mean AP amplitude, AP overshoot, AP duration, rate of AP depolarization, rate of AP repolarization, and AHP duration were also prominent. In addition, axons of 90% of F-type neurons and 60% of S-type neurons became faster conducting in their central and peripheral branch, suggestive of axonal myelination. The proportion of S- and F-type neurons did not vary during postnatal development, suggesting that these phenotypes were established early in development. Membrane properties of both types of TG neurons evolved differently during postnatal development. The nature of many of these changes was linked to the process of myelination. Thus myelination was accompanied by a decrease in AP duration, input resistance ( R in), and increase in membrane capacitance (C). These properties remained constant in unmyelinated neurons (both F- and S-type). In adult TG, all F-type neurons with inward rectification were also fast-conducting Aδ, suggesting that those F-type neurons showing inward rectification at birth will evolve to F-type Aδ neurons with age. The percentage of F-type neurons showing inward rectification also increased with age. Both F- and S-type neurons displayed changes in the sensitivity of the AP to reductions in extracellular Ca2+ or substitution with Co2+ during the process of maturation.

1993 ◽  
Vol 70 (3) ◽  
pp. 1244-1248 ◽  
Author(s):  
D. Mattia ◽  
G. G. Hwa ◽  
M. Avoli

1. Conventional intracellular recordings were performed in rat hippocampal slices to investigate the electrophysiological properties of subicular neurons. These cells had a resting membrane potential (RMP) of -66 +/- 7.2 mV (mean +/- SD; n = 50), input resistance of 23.6 +/- 8.2 M omega (n = 51), time constant of 7.1 +/- 1.9 ms (n = 51), action potential amplitude of 85.8 +/- 13.8 mV (n = 50), and duration of 2.9 +/- 1.2 ms (n = 48). Analysis of the current-voltage relationship revealed membrane inward rectification in both depolarizing and hyperpolarizing direction. The latter type was readily abolished by Cs+ (3 mM; n = 6 cells). 2. Injection of depolarizing current pulses of threshold intensity induced in all subicular neurons (n = 51) recorded at RMP a burst of two to three fast action potentials (frequency = 212.7 +/- 90 Hz, n = 13 cells). This burst rode on a slow depolarizing envelope and was followed by an afterhyperpolarization and later by regular spiking mode once the pulse was prolonged. Similar bursts were also generated upon termination of a hyperpolarizing current pulse. 3. The slow depolarization underlying the burst resembled a low-threshold response, which in thalamic cells is caused by a Ca2+ conductance and is contributed by the Cs(+)-sensitive inward rectifier. However, bursts in subicular cells persisted in medium containing the Ca(2+)-channel blockers Co2+ (2 mM) and Cd2+ (1 mM) (n = 5 cells) but disappeared during application of TTX (1 microM; n = 3 cells). Hence they were mediated by Na+. Blockade of the hyperpolarizing inward rectification by Cs+ did not prevent the rebound response (n = 3 cells). 4. Our findings demonstrate that intrinsic bursts, presumably related to a "low-threshold" Na+ conductance are present in rat subicular neurons. Similar intrinsic characteristics have been suggested to underlie the rhythmic activity described in other neuronal networks, although in most cases the low-threshold electrogenesis was caused by Ca2+. We propose that the bursting mechanism might play a role in modulating incoming signals from the classical hippocampal circuit within the limbic system.


2003 ◽  
Vol 90 (4) ◽  
pp. 2219-2231 ◽  
Author(s):  
C. Cabanes ◽  
F. Viana ◽  
C. Belmonte

Intracellular recordings were employed to study the effects of temperature on membrane properties and excitability in sensory neurons of the intact guinea pig trigeminal ganglion (TG) maintained in vitro. Neurons were classified according to the shape and duration of the action potential into F (short-duration, fast spike) and S (long duration, slow spike with a “hump”) types. Most type F (33/34) neurons had axons with conduction velocities >1.5 m/s, while only 30% (6/23) of type S neurons reached these conduction speeds suggesting differences in myelination. Cooling reduced axonal conduction velocity and prolonged spike duration in both neuronal types. In F-type neurons with strong inward rectification. cooling also increased the excitability, augmenting the input resistance and reducing the current firing threshold. These effects were not observed in S-type neurons lacking inward rectification. In striking contrast to results obtained in cultured TG neurons, cooling or menthol did not induce firing in recordings from the acutely isolated ganglion. However, after application of submillimolar concentrations (100 μM) of the potassium channel blocker 4-aminopyridine (4-AP), 29% previously unresponsive neurons developed cold sensitivity. An additional 31% developed ongoing activity that was sensitive to temperature. Only neurons with strong inward rectification (mostly F-type) became thermosensitive. Cooling- and 4-AP–evoked firing were insensitive to intracellular application of 4-AP or somatic membrane hyperpolarization, suggesting that their action was most prominent at the level of the axon. The lack of excitatory actions of low temperature in the excised intact ganglion contrasts with the impulse discharges induced by cooling in trigeminal nerve terminals of the same species, suggesting a critical difference between cold-transduction mechanisms at the level of the nerve terminals and the soma.


2003 ◽  
Vol 90 (1) ◽  
pp. 405-414 ◽  
Author(s):  
Regula E. Egli ◽  
Danny G. Winder

The bed nucleus of the stria terminalis (BNST) is a structure uniquely positioned to integrate stress information and regulate both stress and reward systems. Consistent with this arrangement, evidence suggests that the BNST, and in particular the noradrenergic input to this structure, is a key component of affective responses to drugs of abuse. We have utilized an in vitro slice preparation from adult mice to determine synaptic and membrane properties of these cells, focusing on the dorsal and ventral subdivisions of the anterolateral BNST (dBNST and vBNST) because of the differential noradrenergic input to these two regions. We find that while resting membrane potential and input resistance are comparable between these subdivisions, excitable properties, including a low-threshold spike (LTS) likely mediated by T-type calcium channels and an Ih-dependent potential, are differentially distributed. Inhibitory and excitatory postsynaptic potentials (IPSPs and EPSPs, respectively) are readily evoked in both dBNST and vBNST. The fast IPSP is predominantly GABAA-receptor mediated and is partially blocked by the AMPA/kainate-receptor antagonist CNQX. In the presence of the GABAA-receptor antagonist picrotoxin, cells in dBNST but not vBNST are more depolarized and have a higher input resistance, suggesting tonic GABAergic inhibition of these cells. The EPSPs elicited in BNST are monosynaptic, exhibit paired pulse facilitation, and contain both an AMPA- and an N-methyl-d-aspartate (NMDA) receptor-mediated component. These data support the hypothesis that neurons of the dorsal and ventral BNST differentially integrate synaptic input, which is likely of behavioral significance. The data also suggest mechanisms by which information may flow through stress and reward circuits.


1989 ◽  
Vol 62 (1) ◽  
pp. 109-118 ◽  
Author(s):  
M. Yoshimura ◽  
T. M. Jessell

1. The membrane properties of substantia gelatinosa (SG) neurons in an in vitro adult rat transverse spinal cord slice preparation with attached dorsal root have been examined. Intracellular recordings were obtained from identified SG neurons. 2. Seventy-six percent of SG neurons exhibited a time-dependent anomalous rectification (AR) when the membrane was hyperpolarized from the resting potential. The time-dependent AR was blocked by cesium (Cs+, 2 mM) but not by barium (Ba2+, 2 mM). Application of Cs+ itself caused membrane hyperpolarization in those SG neurons that expressed the time-dependent AR. The activation of the time-dependent AR was maximal at potentials 5-10 mV below the resting membrane potential. 3. In a few SG neurons, the current-voltage relationship revealed a marked inward rectification, even though there was no detectable time-dependent anomalous rectification during hyperpolarization. Analysis of the Ba2+- and Cs+-sensitivity of these neurons confirmed that SG neurons expressed two distinct ARs, one of which is fast and Ba2+-sensitive and the other of which is time-dependent and Ba2+-insensitive. 4. Fifty-one percent of SG neurons exhibited a transient outward rectification when hyperpolarizing current pulses were applied from potentials more positive than -60 mV or when depolarizing pulses were applied from potentials more negative than -65 mV. The transient outward rectification persisted for 0.3-2 s when hyperpolarizing pulses were applied at -55 mV. 5. The transient outward rectification was associated with a decrease in membrane resistance and was enhanced in low K+ solutions. 4-aminopyridine (4-AP, 2 mM) reversibly blocked the transient outward rectification. 6. The time-dependent anomalous and transient outward rectifying currents exerted opposite effects on the firing properties of SG neurons. Activation of the time-dependent AR increased neuronal excitability. In neurons that exhibited the time-dependent AR, membrane depolarization caused the appearance of a rebound depolarization that resulted in the generation of spikes with only a short delay after application of the depolarizing pulse. In contrast, the transient outward rectifying current markedly delayed spike firing in response to depolarizing pulses. This delay was blocked by application of 4-AP. 7. The diversity in response properties of subpopulations of SG neurons may result in part from this heterogeneity in membrane properties.


2013 ◽  
Vol 110 (8) ◽  
pp. 1751-1764 ◽  
Author(s):  
Wenying Wang ◽  
Hyo Jeong Kim ◽  
Ping Lv ◽  
Bruce Tempel ◽  
Ebenezer N. Yamoah

Developmental plasticity in spiral ganglion neurons (SGNs) ensues from profound alterations in the functional properties of the developing hair cell (HC). For example, prehearing HCs are spontaneously active. However, at the posthearing stage, HC membrane properties transition to graded receptor potentials. The dendrotoxin (DTX)-sensitive Kv1 channel subunits (Kv1.1, 1.2, and 1.6) shape the firing properties and membrane potential of SGNs, and the expression of the channel undergoes developmental changes. Because of the stochastic nature of Kv subunit heteromultimerization, it has been difficult to determine physiologically relevant subunit-specific interactions and their functions in the underlying mechanisms of Kv1 channel plasticity in SGNs. Using Kcna2 null mutant mice, we demonstrate a surprising paradox in changes in the membrane properties of SGNs. The resting membrane potential of Kcna2−/− SGNs was significantly hyperpolarized compared with that of age-matched wild-type (WT) SGNs. Analyses of outward currents in the mutant SGNs suggest an apparent approximately twofold increase in outward K+ currents. We show that in vivo and in vitro heteromultimerization of Kv1.2 and Kv1.4 α-subunits underlies the striking and unexpected alterations in the properties of SGNs. The results suggest that heteromeric interactions of Kv1.2 and Kv1.4 dominate the defining features of Kv1 channels in SGNs.


1996 ◽  
Vol 75 (1) ◽  
pp. 248-267 ◽  
Author(s):  
G. F. Tseng ◽  
D. A. Prince

1. The electrophysiological properties of rat corticospinal neurons (CSNs) were studied 3, 9, and 12 mo after axotomy in the cervical spinal cord, with the use of a combination of the in vitro neocortical slice technique, intracellular recordings, and a double-labeling method that allowed identification of CSNs studied in vitro. 2. CSNs retained the rhodamine-labeled microspheres employed as a retrograde marker and were functionally active in the longest survival group (1 yr). 3. The somatic area of axotomized CSNs became progressively smaller, a reduction that amounted to 37% for all cells at 1 yr. There were no obvious differences between normal and axotomized cells in terms of apical dendritic widths, numbers of apical dendritic branches, or basal dendritic arbors. Intracortical axonal arborizations of axotomized neurons were in general similar to those of normal CSNs in that most axons ended in layers V and VI with only occasional collaterals reaching supragranular layers. 4. Axotomized CSNs were grouped according to their spike firing patterns during depolarizing current pulses so that their electrophysiological behavior could be compared with that of regular spiking and adapting groups of normal CSNs. No significant differences were found in resting membrane potential, or spike parameters between axotomized neurons in any survival group and normal controls. Neurons surviving 1 yr after axotomy had a higher input resistance (RN) than normal CSNs. There was a reduction in the percentage of CSNs that generated prominent spike depolarizing afterpotentials in the axotomized group. 5. The steady-state relationship between spike frequency and applied current (f-I slope) became steeper over time and was significantly greater 9 mo after axotomy in regular spiking (RS) and adapting neurons than in normal CSNs in the same groups. The increase in steady-state f-I slope was in part related to increases in the RN of axotomized neurons. 6. There was a significant decrease in the generation of slow afterhyperpolarizations following trains of spikes in axotomized versus normal RS neurons, first detected at 3 mo and also present in 9 mo and 1 yr survival groups. 7. Biphasic inhibitory postsynaptic potentials (IPSPs) were evoked in only 1 of 11 axotomized neurons in the 3-mo group, 2 of 12 cells examined at 9 mo, and 3 of 15 neurons 1 yr after axotomy. The proportions of neurons generating IPSPs were significantly smaller than in comparable groups of control CSNs. As a consequence, longer duration evoked excitatory postsynaptic potentials were generated by axotomized CSNs. 8. Results show that axotomized CSNs undergo alterations in intrinsic membrane properties and inhibitory synaptic electrogenesis that would tend to make them more responsive to excitatory inputs.


2006 ◽  
Vol 95 (6) ◽  
pp. 3543-3552 ◽  
Author(s):  
Katrina Rimmer ◽  
Alexander A. Harper

We charted postnatal changes in the intrinsic electrophysiological properties and synaptic responses of rat intrinsic cardiac ganglion (ICG) neurons. We developed a whole-mount ganglion preparation of the excised right atrial ganglion plexus. Using intracellular recordings and nerve stimulation we tested the hypothesis that substantial transformations in the intrinsic electrical characteristics and synaptic transmission accompany postnatal development. Membrane potential ( Em) did not change but time constant (τ) and cell capacitance increased with postnatal development. Accordingly, input resistance ( Rin) decreased but specific membrane resistance ( Rm) increased postnatally. Comparison of the somatic active membrane properties revealed significant changes in electrical phenotype. All neonatal neurons had somatic action potentials (APs) with small overshoots and small afterhyperpolarizations (AHPs). Adult neurons had somatic APs with large overshoots and large AHP amplitudes. The range of AHP duration was larger in adults than in neonates. The AP characteristics of juvenile neurons resembled those of adults, with the exception of AHP duration, which fell midway between neonate and adult values. Phasic, multiply adapting, and tonic evoked discharge activities were recorded from ICG neurons. Most neurons displayed phasic discharge at each developmental stage. All neurons received excitatory synaptic inputs from the vagus or interganglionic nerve trunk(s), the strength of which did not change significantly with postnatal age. The changes in the electrophysiological properties of the postganglionic neuron suggest that increased complexity of parasympathetic regulation of cardiac function accompanies postnatal development.


1990 ◽  
Vol 69 (4) ◽  
pp. 1509-1517 ◽  
Author(s):  
G. G. Haddad ◽  
D. F. Donnelly ◽  
P. A. Getting

A brain stem slice preparation from adult and neonatal (less than or equal to 12 days old) rats and intracellular recordings were used to examine the cellular properties of neurons within the hypoglossal (HYP) nucleus. Resting membrane potential (Vm) for adult hypoglossal neurons was -80 +/- 2 (SE) mV. Rheobase was 2.1 +/- 0.4 nA, and input resistance (RN) was 20.8 +/- 1.5 M omega and decreased during the hyperpolarizing period ("sag"). Compared with adult HYP cells, newborn HYP neurons had significantly lower resting potentials (Vm = -73 +/- 2 mV), lower rheobase (0.7 +/- 0.2 nA), and higher RN (27.6 +/- 3.9 M omega). Single action potentials, elicited by short depolarizing-current pulses, were followed by a slow afterhyperpolarization in adult [6.4 +/- 0.3 mV, time constant (tc) 31.0 +/- 1.2 ms] and newborn cells (7.4 +/- 0.2 mV, tc 37.2 +/- 8.2 ms). Prolonged outward current (2 s) produced little spike frequency adaptation in either adult or newborn neurons. Onset of spike activity was not delayed by hyperpolarizing pulses preceding depolarizations. In addition, pharmacological experiments showed that HYP neurons have a tetrodotoxin-sensitive Na+ current and a delayed and an inward rectifier current but no major Ca2+ current. We conclude the following. 1) Electrophysiological membrane properties mature postnatally in HYP neurons; some of these developmental changes can be ascribed to an increase in soma size and dendritic outgrowth but others cannot. 2) Adult HYP neurons, compared with other brain stem neurons (i.e., vagal cells or cells in the nucleus tractus solitarius), are not endowed with major Ca2+ currents or K+ currents such as the A current and the Ca2(+)-activated K+ current.


1999 ◽  
Vol 82 (1) ◽  
pp. 209-215 ◽  
Author(s):  
David F. Donnelly

Carotid body chemoreceptors increase their responsiveness to hypoxia in the postnatal period, but the mechanism for this increase is unresolved. The purpose of the present study was to examine developmental changes in cellular characteristics of chemoreceptor afferent neurons in the petrosal ganglia with the underlying hypothesis that developmental changes occur and may account for the developmental increase in chemoreceptor responsiveness. Chemoreceptor complexes (carotid body, sinus nerve, glossopharyngeal nerve, and petrosal ganglia) were harvested from rats, aged 3–40 days, and intracellular recordings were obtained from petrosal ganglion neurons using sharp electrode impalement. All chemoreceptor neurons across ages were C fibers with conduction velocities <1 m/s and generated repetitive action potentials with depolarization. Resting membrane potential was −61.3 ± 0.9 (SE) mV ( n = 78) and input resistance was 108 ± 6 MΩ and did not significantly change with age. Cell capacitance was 32.4 ± 1.7 pF and did not change with age. Rheobase averaged 0.21 ± 0.02 nA and slightly increased with age. Action potentials were followed by an afterhyperpolarization of 12.4 ± 0.6 mV and time constant 6.9 ± 0.5 ms; only the time constant decreased with age. These results, obtained in rat, demonstrate electrophysiologic characteristics which differ substantially from that previously described in cat chemoreceptor neurons. In general developmental changes in cell characteristics are small and are unlikely to account for the developmental increase in chemoreceptor responsiveness with age.


1993 ◽  
Vol 70 (4) ◽  
pp. 1401-1411 ◽  
Author(s):  
P. A. Nunez-Abades ◽  
J. M. Spielmann ◽  
G. Barrionuevo ◽  
W. E. Cameron

1. Experiments were performed to determine the change in membrane properties of genioglossal (GG) motoneurons during development. Intracellular recordings were made in 127 GG motoneurons from rats postnatal ages 1-30 days. 2. The input resistance (R(in)) and the membrane time constant (t(aum)) decreased between 5-6 and 13-15 days from 84.8 +/- 25.4 (SD) to 47.0 +/- 18.9 M omega (P < 0.01) and from 10.0 +/- 4.2 to 7.3 +/- 3.3 ms (P < 0.05), respectively. During this period, the rheobase (Irh) increased (P < 0.01) from 0.13 +/- 0.07 to 0.27 +/- 0.14 nA, and the percentage of cells exhibiting inward rectification increased from 5 to 40%. Voltage threshold (Vthr) of the action potential remained unchanged postnatally. 3. There was also a postnatal change in the shape of the action potential. Specifically, between 1-2 and 5-6 days, there was a decrease (P < 0.05) in the spike half-width from 2.23 +/- 0.53 to 1.45 +/- 0.44 ms, resulting, in part, from a steepening (P < 0.05) of the slope of the falling phase of the action potential from 21.6 +/- 10.1 to 32.9 +/- 13.1 mV/ms. The slope of the rising phase also increased significantly (P < 0.01) between 1-2 and 13-15 days from 68.4 +/- 31.0 to 91.4 +/- 44.3 mV/ms. 4. The average duration of the medium afterhyperpolarization (mAHPdur) decreased (P < 0.05) between 1-2 (193 +/- 53 ms) and 5-6 days (159 +/- 43 ms). Whereas the mAHPdur was found to be independent of membrane potential, there was a linear relationship between the membrane potential and the amplitude of the medium AHP (mAHPamp). From this latter relationship, a reversal potential for the mAHPamp was extrapolated to be -87 mV. No evidence for the existence of a slow AHP was found in these developing motoneurons. 5. All cells analyzed (n = 74) displayed adaptation during the first three spikes. The subsequent firing pattern was classified into two groups, adapting and nonadapting. Cells at birth were all adapting, whereas all cells but two from animals 13 days and older were nonadapting. At the intermediate age (5-6 days), the minority (27%) was adapting and the majority (73%) was nonadapting. 6. The mean slope of primary range for the first interspike interval (1st ISI) was approximately 90 Hz/nA. This value was similar for both adapting and nonadapting cells and did not change postnatally.(ABSTRACT TRUNCATED AT 400 WORDS)


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