scholarly journals Cholinergic Responses and Intrinsic Membrane Properties of Developing Thalamic Parafascicular Neurons

2009 ◽  
Vol 102 (2) ◽  
pp. 774-785 ◽  
Author(s):  
Meijun Ye ◽  
Abdallah Hayar ◽  
Edgar Garcia-Rill

Parafascicular (Pf) neurons receive cholinergic input from the pedunculopontine nucleus (PPN), which is active during waking and REM sleep. There is a developmental decrease in REM sleep in humans between birth and puberty and 10–30 days in rat. Previous studies have established an increase in muscarinic and 5-HT1 serotonergic receptor–mediated inhibition and a transition from excitatory to inhibitory GABAA responses in the PPN during the developmental decrease in REM sleep. However, no studies have been conducted on the responses of Pf cells to the cholinergic input from the PPN during development, which is a major target of ascending cholinergic projections and may be an important mechanism for the generation of rhythmic oscillations in the cortex. Whole cell patch-clamp recordings were performed in 9- to 20-day-old rat Pf neurons in parasagittal slices, and responses to the cholinergic agonist carbachol (CAR) were determined. Three types of responses were identified: inhibitory (55.3%), excitatory (31.1%), and biphasic (fast inhibitory followed by slow excitatory, 6.8%), whereas 6.8% of cells showed no response. The proportion of CAR-inhibited Pf neurons increased with development. Experiments using cholinergic antagonists showed that M2 receptors mediated the inhibitory response, whereas excitatory modulation involved M1, nicotinic, and probably M3 or M5 receptors, and the biphasic response was caused by the activation of multiple types of muscarinic receptors. Compared with CAR-inhibited cells, CAR-excited Pf cells showed 1) a decreased membrane time constant, 2) higher density of hyperpolarization-activated channels ( Ih), 3) lower input resistance ( Rin), 4) lower action potential threshold, and 5) shorter half-width duration of action potentials. Some Pf cells exhibited spikelets, and all were excited by CAR. During development, we observed decreases in Ih density, Rin, time constant, and action potential half-width. These results suggest that cholinergic modulation of Pf differentially affects separate populations, perhaps including electrically coupled cells. Pf cells tend to show decreased excitability and cholinergic activation during the developmental decrease in REM sleep.

1990 ◽  
Vol 63 (2) ◽  
pp. 333-346 ◽  
Author(s):  
R. Nitzan ◽  
I. Segev ◽  
Y. Yarom

1. Intracellular recordings from neurons in the dorsal motor nucleus of the vagus (vagal motoneurons, VMs) obtained in the guinea pig brain stem slice preparation were used for both horseradish peroxidase (HRP) labeling of the neurons and for measurements of their input resistance (RN) and time constant (tau 0). Based on the physiological data and on the morphological reconstruction of the labeled cells, detailed steady-state and compartmental models of VM were built and utilized to estimate the range of membrane resistivity, membrane capacitance, and cytoplasm resistivity values (Rm, Cm, and Ri, respectively) and to explore the integrative properties of these cells. 2. VMs are relatively small cells with a simple dendritic structure. Each cell has an average of 5.3 smooth (nonspiny), short (251 microns) dendrites with a low order (2) of branching. The average soma-dendritic surface area of VMs is 9,876 microns 2. 3. Electrically, VMs show remarkably linear membrane properties in the hyperpolarizing direction; they have an average RN of 67 +/- 23 (SD) M omega and a tau 0 of 9.4 +/- 4.1 ms. Several unfavorable experimental conditions precluded the possibility of faithfully recovering ("peeling") the first equalizing time constant (tau 1) and, thereby, of estimating the electrotonic length (Lpeel) of VMs. 4. Reconciling VM morphology with the measured RN and tau 0 through the models, assuming an Ri of 70 omega.cm and a spatially uniform Rm, yielded an Rm estimate of 5,250 omega.cm2 and a Cm of 1.8 microF/cm2. Peeling theoretical transients produced by these models result in an Lpeel of 1.35. Because of marked differences in the length of dendrites within a single cell, this value is larger than the maximal cable length of the dendrites and is twice as long as their average cable length. 5. The morphological and physiological data could be matched indistinguishably well if a possible soma shunt (i.e., Rm, soma less than Rm, dend) was included in the model. Although there is no unique solution for the exact model Rm, a general conclusion regarding the integrative capabilities of VM could be drawn. As long as the model is consistent with the experimental data, the average input resistance at the dendritic terminals (RT) and the steady-state central (AFT----S) and peripheral (AFS----T) attenuation factors are essentially the same in the different models. With Ri = 70 omega.cm, we calculated RT, AFS----T, and AFT----S to be, on the average, 580 M omega, 1.1, and 13, respectively.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 70 (5) ◽  
pp. 1975-1987 ◽  
Author(s):  
S. M. Johnson ◽  
R. B. Felder

1. Recent studies have demonstrated that the arterial baroreflex is imparied with aging and have implicated central components of the baroreflex arc in this autonomic dysfunction. Neurons in the medial portion of the nucleus tractus solitarius (mNTS) receive a major input from the arterial baroreceptors. The present study was undertaken to characterize the intrinsic membrane properties of mNTS neurons in young rats and to test the hypothesis that these properties are altered with aging. An in vitro brain stem slice preparation was used to record intracellularly from mNTS neurons; passive membrane properties, action potential characteristics, and repetitive firing properties were examined and compared. 2. Neurons in the mNTS of young (3-5 mo old) Fischer-344 rats (F-344; n = 35) had a resting membrane potential of -57 +/- 6.9 mV (mean +/- SD), a membrane time constant of 18 +/- 9.0 ms, and an input resistance of 110 +/- 60 m omega. Action potential amplitude was 81 +/- 7.5 mV with a duration at half-height of 0.83 +/- 0.15 ms. The spontaneous firing rate in 24 cells was 4.3 +/- 2.9 Hz. The amplitude and duration of the action potential afterhyperpolarization (AHP) were 6.6 +/- 3.0 mV and 64 +/- 34 ms, respectively. All neurons expressed spike frequency adaptation, action potential AHP, and posttetanic hyperpolarization. Delayed excitation and postinhibitory rebound were present in 34 and 14% of neurons tested, respectively. Neurons from adult (10-12 mo old) F-344 rats (n = 34) were similar to the young F-344 rats with respect to all of these variables. 3. Neurons from aged (21-24 mo old) F-344 (n = 32) were similar to those from young and adult rats, but there were two potentially important differences: the mean input resistance of the aged neurons was higher (170 +/- 150 M omega), with a larger proportion (46% of aged neurons vs. 20% of young neurons and 21% of adult neurons) having input resistances > 150 M omega; and there was a tendency for a smaller percentage of aged neurons (16% of aged neurons vs. 34% of young neurons and 29% of adult neurons) to express delayed excitation. 4. The potential significance of a high input resistance was tested by comparing the steady-state current-voltage (I-V) relationships and the frequency-current (f-I) relationships among low-resistance (1-100 M omega), medium-resistance (101-200 M omega).(ABSTRACT TRUNCATED AT 400 WORDS)


1991 ◽  
Vol 157 (1) ◽  
pp. 101-122
Author(s):  
WERNER A. WUTTKE ◽  
MICHAEL S. BERRY

1. The giant salivary cells of Haementeria ghilianii are known to produce Ca2+-dependent action potentials and to release their secretory products in response to stimulation of the stomatogastric nerve. In this study, the electrophysiological effects of some putative transmitters were examined by perfusion of the gland and two promising candidates were selected for detailed analysis. 2. Acetylcholine (ACh) was the only substance tested which excited the gland cells. It produced a large, Na+-dependent depolarization that elicited 1–3 action potentials and desensitized to about 24% of its maximal value within 2 min. 3. Carbachol, tetramethylammonium and nicotine elicited similar responses to ACh, whereas choline and pilocarpine had negligible effects. 4. The ACh response was completely blocked by d-tubocurarine and strychnine, and was reduced by tetraethylammonium, hexamethonium and atropine. The receptors, therefore, cannot be clearly distinguished as nicotinic or muscarinic. 5. ACh did not elicit secretion, but this does not necessarily preclude it from acting as a neuroglandular transmitter. 6. 5-Hydroxytryptamine (5-HT) was the only transmitter candidate that elicited secretion, though it did not excite the gland cells. 7. 5-HT produced a subthreshold depolarization and an increase in input resistance. Action potentials, elicited by depolarizing pulses, were increased in amplitude and duration, and showed greatly reduced adaptation. 8. 5-HT potentiated the net inward current, evoked by subthreshold depolarizing pulses, by reducing outward K+ current. The inward current, carried by Ca2+, was not directly affected. In addition, 5-HT increased an inwardly rectifying current, carried by Na+ and K+. All the effects of 5-HT tended to increase cell excitability. 9. Salivary cell responses to 5-HT were reversibly antagonised by methysergide. 10. Responses to ACh or 5-HT were not mimicked by 3′, 5′-cyclic guanosine monophosphate, which greatly reduced spike amplitude and excitability. The effects were specific to the 3′, 5′ form; 2′, 3′-cyclic GMP had no effect. Cyclic GMP dramatically reduced the duration of action potentials that had been artificially prolonged by TEA+ or removal of external Ca2+. 11. Cyclic 3′, 5′-adenosine monophosphate and its dibutyryl derivative had little effect on membrane properties. 8-Bromo-cyclic AMP, however, mimicked all the effects of 5-HT. It is thought that 5-HT may exert its actions via cyclic AMP. 12. The possible role of 5-HT in salivary secretion is discussed.


1995 ◽  
Vol 74 (5) ◽  
pp. 1972-1981 ◽  
Author(s):  
R. H. Liu ◽  
J. Yamuy ◽  
M. C. Xi ◽  
F. R. Morales ◽  
M. H. Chase

1. This study was undertaken to investigate the effects of adriamycin (ADM, Doxorubicin) on the basic electrophysiological properties of spinal cord motoneurons in the adult cat. ADM was injected into the biceps, gastrocnemius, semitendinosus, and semimembranosus muscles of the left hindlimb (1.2 mg per muscle). Intracellular recordings from motoneurons innervating these muscles were carried out 12, 20, or 40 days after ADM administration and from corresponding motoneurons in untreated control cats. 2. Twelve days after ADM injection, motoneurons innervating ADM-treated muscles (ADM MNs) exhibited statistically significant increases in input resistance, membrane time constant, and amplitude of the action potential's afterhyperpolarization (AHP). In addition, there was a statistically significant decrease in rheobase and in the delay between the action potential of the initial segment (IS) and that of the somadendritic (SD) portion of the motoneuron (IS-SD delay). There were no significant changes in the resting membrane potential, threshold depolarization, action potential amplitude, or axonal conduction velocity. 3. The changes in electrical properties of motoneurons at 20 and 40 days after ADM injection were qualitatively similar to those observed at 12 days. However, at 40 days after ADM injection there was a statistically significant decrease in the axonal conduction velocity of the ADM MNs. 4. The normal correlations that are present between the AHP duration and electrical properties of the control motoneurons were observed in the ADM MNs, e.g., AHP duration was positively correlated with the input resistance and time constant and negatively correlated with the axonal conduction velocity. The correlation coefficients, however, were reduced in comparison with the control data. 5. This study demonstrates that ADM exerts significant effects on the electrical properties of motoneurons when injected into their target muscles. The majority of the changes in motoneuron electrical properties caused by ADM resemble those observed in motoneurons of aged cats. Additional research is required to determine whether the specific changes induced in motoneurons by ADM and those that occur in motoneurons in old age are due to similar degradative mechanisms.


2010 ◽  
Vol 103 (1) ◽  
pp. 490-498 ◽  
Author(s):  
Amanda Zimmerman ◽  
Shawn Hochman

Spinal cord sympathetic preganglionic neurons (SPNs) integrate activity from descending and sensory systems to determine the final central output of the sympathetic nervous system. The intermediolateral column (IML) has the highest number and density of SPNs and, within this region, SPN somas are found in distinct clusters within thoracic and upper lumbar spinal segments. Whereas SPNs exhibit a rostrocaudal gradient of end-target projections, individual clusters contain SPNs with diverse functional roles. Here we explored diversity in the electrophysiological properties observed in Hb9-eGFP–identified SPNs in the IML of neonatal mice. Overall, mouse SPN intrinsic membrane properties were comparable with those seen in other species. A wide range of values was obtained for all measured properties (up to a 10-fold difference), suggesting that IML neurons are highly differentiated. Using linear regression we found strong correlations between many cellular properties, including input resistance, rheobase, time constant, action potential shape, and degree of spike accommodation. The best predictor of cell function was rheobase, which correlated well with firing frequency–injected current ( f– I) slopes as well as other passive and active membrane properties. The range in rheobase suggests that IML neurons have a recruitment order with stronger synaptic drives required for maximal recruitment. Using cluster analysis, we identified at least four subpopulations of SPNs, including one with a long time constant, low rheobase, and high f– I gain. We thus propose that the IML contains populations of neurons that are differentiable by their membrane properties and hypothesize they represent diverse functional classes.


1992 ◽  
Vol 68 (5) ◽  
pp. 1746-1759 ◽  
Author(s):  
S. P. Schneider

1. The functional organization of interneurons in spinal laminae III-V was studied in an isolated preparation of hamster dorsal horn with sensory innervation from an excised skin patch. Morphological details of 40 neurons were visualized by intracellular injection of horseradish peroxidase. Active and passive membrane properties, synaptic responses to cutaneous nerve volleys, and responses to innocuous mechanical stimuli were determined for 25 cells with identified axons. 2. Neurons were classified into two types: 1) cells with local axons, branching in proximity to the cell soma and dendrites, that produced numerous synaptic boutons (740 +/- 504/axon; mean +/- SD), often arranged in clusters and 2) neurons with deep axons that usually bifurcated into rostral and caudal daughter branches up to 2.5 mm long, giving off collaterals ventral to the cell body and dendrites and forming significantly fewer boutons (155 +/- 140/axon) than local axon cells. A majority of boutons of local axon and deep axon cells, 89 and 83%, respectively, were of the en passant type. 3. Dendritic trees of local axon cells were relatively compact dorsoventrally (119 +/- 42 microns) and mediolaterally (128 +/- 45 microns), but were elongated rostrocaudally (404 +/- 121 microns). In comparison, dendritic trees of deep axon cells radiated significantly farther dorsoventrally (218 +/- 88 microns) and mediolaterally (180 +/- 34 microns), but exhibited comparable rostrocaudal spread (413 +/- 128 microns). There was no correlation between dorsoventral and mediolateral dendritic spread and mediolateral soma location for either cell type. However, for medially situated deep axon cells the rostrocaudal dendritic spread was up to 180% greater than for those located laterally. For nearly one-half of all cells (49%; 17/35) dendritic processes extended dorsally into lamina II. 4. Local axon cells had resting membrane potentials that were more negative than deep axon cells (-59.5 +/- 6.1 and -53.6 +/- 4.7 mV, respectively), but the amplitude and duration of action potentials generated by the two types were similar. Neuronal input resistance (RN) and membrane time constant (tau m) varied widely from cell to cell, but were not significantly different for local axon (77.4 +/- 46.8 M omega, 13.4 +/- 9.5 ms) and deep axon cells (46.5 +/- 19.2 M omega, 6.6 +/- 3.0 ms). 5. Volleys in myelinated afferent fibers activated fast rising excitatory postsynaptic potentials (EPSPs) that exhibited later, more slowly rising potentials with multiple components in a majority of deep axon (89%) and local axon (72%) neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 69 (4) ◽  
pp. 1350-1362 ◽  
Author(s):  
D. G. Rainnie ◽  
E. K. Asprodini ◽  
P. Shinnick-Gallagher

1. Intracellular current-clamp recordings were made from neurons of the basolateral nucleus of the amygdala (BLA) of the rat in the in vitro slice preparation. Neurons were identified morphologically after intracellular injection of biocytin, and the electrophysiological properties and morphological characteristics were correlated. 2. Three distinct morphological subtypes were identified: Class I pyramidal neurons, Class I stellate neurons, and Class II neurons. Each morphological subtype could also be distinguished according to its characteristic electrophysiological properties. 3. Class I pyramidal neurons typically had pyramidal perikarya (cross-sectional area = 245 microns2) with spine-laden apical and basal dendrites. The axon originated from the largest basal dendrite and produced several collaterals that ramified throughout the dendritic arborization of the parent cell. These neurons were characterized electrophysiologically by their higher input resistance (65.6 M omega), long time constant of membrane charging tau 0 (27.8 ms), long duration action potential (half-width = 0.85 ms), and regular firing pattern [1st interspike interval ISI) = 91 ms]. 4. Class I stellate neurons differed morphologically from Class I pyramidal neurons only in the size (cross sectional area = 330 microns 2) and stellate appearance of their perikarya. These neurons had characteristic lower input resistance (40.1 M omega), shorter time constant of membrane charging tau 0 (14.5 ms), shorter duration action potential (half-width = 0.7 ms), and a burst firing pattern (1st ISI = 6.0 ms), all of which were statistically different from Class I pyramidal neurons. 5. Class II neurons were multipolar (cross sectional area = 235 microns 2) and were distinguishable from Class I neurons by the almost complete absence of dendritic spines. Class II neurons were characterized electrophysiologically by a midrange input resistance (58 M omega), intermediate time constant of membrane charging tau 0 (19 ms), intermediate action-potential duration (half-width = 0.77 ms), and a burst firing pattern (1st ISI = 6.0 ms). In contrast to Class I neurons, action-potential firing of Class II neurons did not accommodate in response to prolonged depolarizing current injection. 6. In conclusion, BLA neurons may be characterized by their specific electrophysiological properties as well as by their morphological traits. Therefore, permitting assessment of signal transduction in identified populations of neurons within this nucleus.


1972 ◽  
Vol 60 (4) ◽  
pp. 430-453 ◽  
Author(s):  
Nick Sperelakis ◽  
K. Shigenobu

The electrophysiological properties of embryonic chick hearts (ventricles) change during development; the largest changes occur between days 2 and 8. Resting potential (Em) and peak overshoot potential (+Emax) increase, respectively, from -35 mv and +11 mv at day 2 to -70 mv and +28 mv at days 12–21. Action potential duration does not change significantly. Maximum rate of rise of the action potential (+Vmax) increases from about 20 v/sec at days 2–3 to 150 v/sec at days 18–21; + Vmax of young cells is not greatly increased by applied hyperpolarizing current pulses. In resting Em vs. log [K+]o curves, the slope at high K+ is lower in young hearts (e.g. 30 mv/decade) than the 50–60 mv/decade obtained in old hearts, but the extrapolated [K+]i values (125–140 mM) are almost as high. Input resistance is much higher in young hearts (13 MΩ at day 2 vs. 4.5 MΩ at days 8–21), suggesting that the membrane resistivity (Rm) is higher. The ratio of permeabilities, PNa/PK, is high (about 0.2) in young hearts, due to a low PK, and decreases during ontogeny (to about 0.05). The low K+ conductance (gK) in young hearts accounts for the greater incidence of hyperpolarizing afterpotentials and pacemaker potentials, the lower sensitivity (with respect to loss of excitability) to elevation of [K+]o, and the higher chronaxie. Acetylcholine does not increase gK of young or old ventricular cells. The increase in (Na+, K+)-adenosine triphosphatase (ATPase) activity during development tends to compensate for the increase in gK. +Emax and + Vmax are dependent on [Na+]o in both young and old hearts. However, the Na+ channels in young hearts (2–4 days) are slow, tetrodotoxin (TTX)-insensitive, and activated-inactivated at lower Em. In contrast, the Na+ channels of cells in older hearts (> 8 days) are fast and TTX-sensitive, but they revert back to slow channels when placed in culture.


2002 ◽  
Vol 282 (6) ◽  
pp. G1045-G1051 ◽  
Author(s):  
Beverley A. Moore ◽  
Timothy M. R. Stewart ◽  
Ceredwyn Hill ◽  
Stephen J. Vanner

This study examines whether intestinal inflammation leads to changes in the properties of ion channels in dorsal root ganglia (DRG) neurons. Ileitis was induced by injection of trinitrobenzene sulfonic acid (TNBS), and DRG neurons innervating the ileum were labeled using fast blue. Intracellular recording techniques were used to measure electrophysiological properties of acutely dissociated neurons 12–24 h after dissection. Nociceptive neurons were identified by sensitivity to capsaicin, tetrodotoxin resistance, and size (<30 μm). The action potential threshold in neurons from TNBS-treated animals was reduced by >70% compared with controls ( P < 0.001), but the resting membrane potential was unchanged. Cell diameter, input resistance (67%), and action potential upstroke velocity (22%) increased in the TNBS group ( P < 0.05). The number of action potentials discharged increased in the TNBS group ( P < 0.001), whereas application of 4-aminopyridine to control cells mimicked this effect. This study demonstrates that ileitis induces hyperexcitability in nociceptive DRG neurons and changes in the properties of Na+ and K+channels at the soma, which persist after removal from the inflamed environment.


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.


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