Development and modulation of intrinsic membrane properties control the temporal precision of auditory brain stem neurons

2015 ◽  
Vol 113 (2) ◽  
pp. 524-536 ◽  
Author(s):  
Delwen L. Franzen ◽  
Sarah A. Gleiss ◽  
Christina Berger ◽  
Franziska S. Kümpfbeck ◽  
Julian J. Ammer ◽  
...  
Keyword(s):  
Action Potential ◽  
Brain Stem ◽  
Firing Pattern ◽  
Input Resistance ◽  
Membrane Properties ◽  
Auditory Signal ◽  
Intrinsic Properties ◽  
Temporal Precision ◽  
Auditory Brain Stem ◽  
Intrinsic Membrane Properties

Passive and active membrane properties determine the voltage responses of neurons. Within the auditory brain stem, refinements in these intrinsic properties during late postnatal development usually generate short integration times and precise action-potential generation. This developmentally acquired temporal precision is crucial for auditory signal processing. How the interactions of these intrinsic properties develop in concert to enable auditory neurons to transfer information with high temporal precision has not yet been elucidated in detail. Here, we show how the developmental interaction of intrinsic membrane parameters generates high firing precision. We performed in vitro recordings from neurons of postnatal days 9–28 in the ventral nucleus of the lateral lemniscus of Mongolian gerbils, an auditory brain stem structure that converts excitatory to inhibitory information with high temporal precision. During this developmental period, the input resistance and capacitance decrease, and action potentials acquire faster kinetics and enhanced precision. Depending on the stimulation time course, the input resistance and capacitance contribute differentially to action-potential thresholds. The decrease in input resistance, however, is sufficient to explain the enhanced action-potential precision. Alterations in passive membrane properties also interact with a developmental change in potassium currents to generate the emergence of the mature firing pattern, characteristic of coincidence-detector neurons. Cholinergic receptor-mediated depolarizations further modulate this intrinsic excitability profile by eliciting changes in the threshold and firing pattern, irrespective of the developmental stage. Thus our findings reveal how intrinsic membrane properties interact developmentally to promote temporally precise information processing.

Effects of aging on the intrinsic membrane properties of medial NTS neurons of Fischer-344 rats

1993 ◽  
Vol 70 (5) ◽  
pp. 1975-1987 ◽  
Author(s):  
S. M. Johnson ◽  
R. B. Felder
Keyword(s):  
Action Potential ◽  
Nucleus Tractus Solitarius ◽  
Input Resistance ◽  
Membrane Properties ◽  
Repetitive Firing ◽  
Resting Membrane Potential ◽  
Fischer 344 Rats ◽  
Fischer 344 ◽  
Steady State Current ◽  
Intrinsic Membrane Properties

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)

Hyperpolarization-Activated Current (Ih) in the Inferior Colliculus: Distribution and Contribution to Temporal Processing

2003 ◽  
Vol 90 (6) ◽  
pp. 3679-3687 ◽  
Author(s):  
Ursula Koch ◽  
Benedikt Grothe
Keyword(s):  
Brain Stem ◽  
Inferior Colliculus ◽  
Temporal Processing ◽  
Auditory Processing ◽  
Input Resistance ◽  
Temporal Analysis ◽  
Membrane Properties ◽  
Resting Membrane Potential ◽  
Auditory Brain Stem ◽  
Hyperpolarization Activated Current

Neurons in the inferior colliculus (IC) process acoustic information converging from inputs from almost all nuclei of the auditory brain stem. Despite its importance in auditory processing, little is known about the distribution of ion currents in IC neurons, namely the hyperpolarization-activated current Ih. This current, as shown in neurons of the auditory brain stem, contributes to the precise analysis of temporal information. Distribution and properties of the Ih current and its contribution to membrane properties and synaptic integration were examined by current- and voltage-clamp recordings obtained from IC neurons in acute slices of rats (P17-P19). Based on firing patterns to positive current injection, three basic response types were distinguished: onset, adapting, and sustained firing neurons. Onset and adapting cells showed an Ih-dependent depolarizing sag and had a more depolarized resting membrane potential and lower input resistance than sustained neurons. Ih amplitudes were largest in onset, medium in adapting, and small in sustained neurons. Ih activation kinetics was voltage dependent in all neurons and faster in onset and adapting compared with sustained neurons. Injecting trains of simulated synaptic currents into the neurons or evoking inhibitory postsynaptic potentials (IPSPs) by stimulating the lemniscal tract showed that Ih reduced temporal summation of excitatory and inhibitory potentials in onset but not in sustained neurons. Blocking Ih also abolished afterhyperpolarization and rebound spiking. These results suggest that, in a large proportion of IC cells, namely the onset and adapting neurons, Ih improves precise temporal processing and contributes to the temporal analysis of input patterns.

scholarly journals Two Populations of Layer V Pyramidal Cells of the Mouse Neocortex: Development and Sensitivity to Anesthetics

2005 ◽  
Vol 94 (5) ◽  
pp. 3357-3367 ◽  
Author(s):  
Elodie Christophe ◽  
Nathalie Doerflinger ◽  
Daniel J. Lavery ◽  
Zoltán Molnár ◽  
Serge Charpak ◽  
...  
Keyword(s):  
Action Potential ◽  
Calcium Binding ◽  
Pyramidal Neurons ◽  
Pyramidal Cells ◽  
Membrane Properties ◽  
Subcortical Structures ◽  
Contralateral Cortex ◽  
Layer V ◽  
Intrinsic Membrane Properties ◽  
Two Populations

Previous studies have shown that layer V pyramidal neurons projecting either to subcortical structures or the contralateral cortex undergo different morphological and electrophysiological patterns of development during the first three postnatal weeks. To isolate the determinants of this differential maturation, we analyzed the gene expression and intrinsic membrane properties of layer V pyramidal neurons projecting either to the superior colliculus (SC cells) or the contralateral cortex (CC cells) by combining whole cell recordings and single-cell RT-PCR in acute slices prepared from postnatal day (P) 5–7 or P21–30 old mice. Among the 24 genes tested, the calcium channel subunits α1B and α1C, the protease Nexin 1, and the calcium-binding protein calbindin were differentially expressed in adult SC and CC cells and the potassium channel subunit Kv4.3 was expressed preferentially in CC cells at both stages of development. Intrinsic membrane properties, including input resistance, amplitude of the hyperpolarization-activated current, and action potential threshold, differed quantitatively between the two populations as early as from the first postnatal week and persisted throughout adulthood. However, the two cell types had similar regular action potential firing behaviors at all developmental stages. Surprisingly, when we increased the duration of anesthesia with ketamine–xylazine or pentobarbital before decapitation, a proportion of mature SC cells, but not CC cells, fired bursts of action potentials. Together these results indicate that the two populations of layer V pyramidal neurons already start to differ during the first postnatal week and exhibit different firing capabilities after anesthesia.

scholarly journals Subthreshold K+ Channel Dynamics Interact With Stimulus Spectrum to Influence Temporal Coding in an Auditory Brain Stem Model

2008 ◽  
Vol 99 (2) ◽  
pp. 534-544 ◽  
Author(s):  
Mitchell L. Day ◽  
Brent Doiron ◽  
John Rinzel
Keyword(s):  
Brain Stem ◽  
Pattern Classification ◽  
Power Spectra ◽  
Temporal Coding ◽  
K Channel ◽  
Temporal Precision ◽  
Channel Dynamics ◽  
Auditory Brain Stem ◽  
Low Pass ◽  
Temporal Encoding

Neurons in the auditory brain stem encode signals with exceptional temporal precision. A low-threshold potassium current, IKLT, present in many auditory brain stem structures and thought to enhance temporal encoding, facilitates spike selection of rapid input current transients through an associated dynamic gate. Whether the dynamic nature of IKLT interacts with the timescales in spectrally rich input to influence spike encoding remains unclear. We examine the general influence of IKLT on spike encoding of stochastic stimuli using a pattern classification analysis between spike responses from a ventral cochlear nucleus (VCN) model containing IKLT, and the same model with the IKLT dynamics removed. The influence of IKLT on spike encoding depended on the spectral content of the current stimulus such that maximal IKLT influence occurred for stimuli with power concentrated at frequencies low enough (<500 Hz) to allow IKLT activation. Further, broadband stimuli significantly decreased the influence of IKLT on spike encoding, suggesting that broadband stimuli are not well suited for investigating the influence of some dynamic membrane nonlinearities. Finally, pattern classification on spike responses was performed for physiologically realistic conductance stimuli created from various sounds filtered through an auditory nerve (AN) model. Regardless of the sound, the synaptic input arriving at VCN had similar low-pass power spectra, which led to a large influence of IKLT on spike encoding, suggesting that the subthreshold dynamics of IKLT plays a significant role in shaping the response of real auditory brain stem neurons.

Electrical properties of oxytocin neurons in organotypic cultures from postnatal rat hypothalamus

1996 ◽  
Vol 76 (4) ◽  
pp. 2772-2785 ◽  
Author(s):  
P. Jourdain ◽  
D. A. Poulain ◽  
D. T. Theodosis ◽  
J. M. Israel
Keyword(s):  
Electrical Properties ◽  
Action Potential ◽  
Glutamate Receptors ◽  
Action Potentials ◽  
Firing Pattern ◽  
Membrane Conductance ◽  
Input Resistance ◽  
Resting Potential ◽  
Organotypic Cultures ◽  
Current Pulses

1. Intracellular recordings were performed on immunocytochemically identified oxytocin (OT) neurons (n = 101) maintained for 2-7 wk in hypothalamic organotypic cultures derived from 4-to 6-day-old rat neonates. The neurons displayed a resting potential of -58.9 +/- 6.8 mV (mean +/- SD, n = 74), an input resistance of 114 +/- 26.8 M omega (n = 66), and a time constant of 9.6 +/- 1.4 ms (n = 57). Voltage-current (V-I) relations, linear at resting potential, showed a pronounced outward rectification when depolarized from hyperpolarized membrane potentials. At these hyperpolarized potentials, depolarizing current pulses induced a delayed action potential. 2. Action potentials had an amplitude of 73.4 +/- 9.7 mV and a duration of 1.9 +/- 0.2 ms. Each action potential was followed by an afterhyperpolarization of 7.9 +/- 2.0 mV in amplitude lasting 61.7 +/- 11.3 ms. The depolarizing phase of action potentials was both Na+ and Ca2+ dependent, whereas repolarization was due to a K+ conductance increase. 3. When Ba2+ was substituted for Ca2+ in the medium, OT neurons displayed prolonged sustained depolarizations. In the presence of tetrodotoxin (TTX), these depolarizations were triggered by depolarizing current pulses and arrested by hyperpolarizing current pulses or by local application of Ca2+, Co2+, Cd2+, No sustained depolarization was obtained when nifedipine was added to the medium. These data suggest that OT cells in organotypic culture possess L-type Ca2+ channels. 4. All OT neurons generated spontaneous action potentials at resting potential. Of 59 neurons, 29 showed a slow, irregular firing pattern (< or = 2.5 spikes/s), 24 generated a fast continuous firing pattern (> or = 2.5 spikes/s), and 6 cells displayed a bursting pattern of activity consisting of alternating periods of spike discharge and quiescence. None of the bursting cells exhibited regenerative endogenous potentials (plateau potentials). On the contrary, in four of these cells, the bursting activity was clearly due to patterned synaptic activity. 5. The cultured OT cells responded to exogenous gamma-aminobutyric acid (GABA) and muscimol with a hyperpolarization and an increase in membrane conductance. These effects still were observed in the presence of TTX, indicating that they were due to direct activation of GABA receptors in the cells. The GABA-induced response was mediated by GABAA receptors because it was blocked by bicuculline, but not by GABAB receptors, because baclofen and hydroxysaclofen had no effect on membrane potential and input resistance. 6. OT neurons responded to exogenous glutamate, quisqualate, and kainate with a depolarization concomitant with an increase in membrane conductance. N-methyl-D-aspartate depolarized the cells in Mg(2+)-free medium. These effects were observed in the presence of TTX, suggesting that OT cells expressed ionotropic glutamate receptors. Trans-(1S,3R)-1-amino-1,3-cyclopentane-dicarboxylic acid and (+/-)-alpha-amino-4-carboxymethylphenylglycine had no effect on OT cells, thus excluding the presence of metabotropic glutamate receptors. 7. Taken together, our observations demonstrate that hypothalamic slice cultures from 4- to 6-day-old rat neonates contain well-differentiated OT neurons that display electrical properties similar to those shown by adult neurons in vitro. Such cultures provide a reliable model to investigate membrane properties of adult OT neurons and a useful means to study the long-term modulation of their electrical behaviour by various agents known to affect OT cells in vivo.

scholarly journals A1 adenosine receptor-mediated GIRK channels contribute to the resting conductance of CA1 neurons in the dorsal hippocampus

2015 ◽  
Vol 113 (7) ◽  
pp. 2511-2523 ◽  
Author(s):  
Chung Sub Kim ◽  
Daniel Johnston
Keyword(s):  
Dorsal Hippocampus ◽  
Input Resistance ◽  
Membrane Properties ◽  
Resting Membrane Potential ◽  
Girk Channels ◽  
Ca1 Neurons ◽  
Cation Conductance ◽  
Cornu Ammonis ◽  
Intrinsic Membrane Properties ◽  
G Protein Coupled

The dorsal and ventral hippocampi are functionally and anatomically distinct. Recently, we reported that dorsal Cornu Ammonis area 1 (CA1) neurons have a more hyperpolarized resting membrane potential and a lower input resistance and fire fewer action potentials for a given current injection than ventral CA1 neurons. Differences in the hyperpolarization-activated cyclic nucleotide-gated cation conductance between dorsal and ventral neurons have been reported, but these differences cannot fully account for the different resting properties of these neurons. Here, we show that coupling of A1 adenosine receptors (A1ARs) to G-protein-coupled inwardly rectifying potassium (GIRK) conductance contributes to the intrinsic membrane properties of dorsal CA1 neurons but not ventral CA1 neurons. The block of GIRKs with either barium or the more specific blocker Tertiapin-Q revealed that there is more resting GIRK conductance in dorsal CA1 neurons compared with ventral CA1 neurons. We found that the higher resting GIRK conductance in dorsal CA1 neurons was mediated by tonic A1AR activation. These results demonstrate that the different resting membrane properties between dorsal and ventral CA1 neurons are due, in part, to higher A1AR-mediated GIRK activity in dorsal CA1 neurons.

Intracellular recordings from morphologically identified neurons of the basolateral amygdala

1993 ◽  
Vol 69 (4) ◽  
pp. 1350-1362 ◽  
Author(s):  
D. G. Rainnie ◽  
E. K. Asprodini ◽  
P. Shinnick-Gallagher
Keyword(s):  
Action Potential ◽  
Time Constant ◽  
Firing Pattern ◽  
Pyramidal Neurons ◽  
Input Resistance ◽  
Class Ii ◽  
Class I ◽  
Sectional Area ◽  
Cross Sectional ◽  
Electrophysiological Properties

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.

scholarly journals Changes in Membrane Properties of Chick Embryonic Hearts during Development

1972 ◽  
Vol 60 (4) ◽  
pp. 430-453 ◽  
Author(s):  
Nick Sperelakis ◽  
K. Shigenobu
Keyword(s):  
Action Potential ◽  
Input Resistance ◽  
Membrane Properties ◽  
Resting Potential ◽  
Lower Sensitivity ◽  
Na Channels ◽  
Electrophysiological Properties ◽  
Ventricular Cells ◽  
High K ◽  
Pacemaker Potentials

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 (&gt; 8 days) are fast and TTX-sensitive, but they revert back to slow channels when placed in culture.

scholarly journals Intrinsic membrane properties determine hippocampal differential firing pattern in vivo in anesthetized rats

Hippocampus ◽  
2015 ◽  
Vol 26 (5) ◽  
pp. 668-682 ◽  
Author(s):  
Janina Kowalski ◽  
Jian Gan ◽  
Peter Jonas ◽  
Alejandro J. Pernía‐Andrade
Keyword(s):  
Firing Pattern ◽  
Membrane Properties ◽  
Anesthetized Rats ◽  
Intrinsic Membrane Properties

How Is the Respiratory Rhythm Generated? A Model

Physiology ◽  
1986 ◽  
Vol 1 (3) ◽  
pp. 109-112 ◽  
Author(s):  
DW Richter ◽  
D Ballantyne ◽  
JE Remmers
Keyword(s):  
Brain Stem ◽  
Neuronal Network ◽  
Respiratory Rhythm ◽  
Synaptic Activity ◽  
Membrane Properties ◽  
Respiratory Neurons ◽  
Control Sequence ◽  
Intrinsic Membrane Properties ◽  
The Brain ◽  
Respiratory Movements

This article presents a model of the neuronal network that generates the rhythm for respiratory movements. It incorporates new data on the synaptic activity and discharge properties of respiratory neurons in the brain stem and on the modulation of their excitability by nonsynaptic intrinsic membrane properties. The model allows a description of the control sequence that generates the rhythm.

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