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.

Biophysical properties of hypoglossal neurons in vitro: intracellular studies in adult and neonatal rats

1990 ◽  
Vol 69 (4) ◽  
pp. 1509-1517 ◽  
Author(s):  
G. G. Haddad ◽  
D. F. Donnelly ◽  
P. A. Getting
Keyword(s):  
Brain Stem ◽  
Nucleus Tractus Solitarius ◽  
Outward Current ◽  
Input Resistance ◽  
Membrane Properties ◽  
Resting Membrane Potential ◽  
Single Action ◽  
Soma Size ◽  
Newborn Neurons

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.

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.

Dorsal and Ventral Distribution of Excitable and Synaptic Properties of Neurons of the Bed Nucleus of the Stria Terminalis

2003 ◽  
Vol 90 (1) ◽  
pp. 405-414 ◽  
Author(s):  
Regula E. Egli ◽  
Danny G. Winder
Keyword(s):  
Receptor Antagonist ◽  
Drugs Of Abuse ◽  
Input Resistance ◽  
Membrane Properties ◽  
Resting Membrane Potential ◽  
Stria Terminalis ◽  
Bed Nucleus ◽  
Adult Mice ◽  
Dependent Potential

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.

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
Keyword(s):  
Postnatal Development ◽  
Trigeminal Ganglion ◽  
Input Resistance ◽  
Membrane Capacitance ◽  
Membrane Properties ◽  
Inward Rectification ◽  
Resting Membrane Potential ◽  
Depolarization Rate ◽  
Ganglion Neurons

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.

scholarly journals Postnatal development of synaptic properties of the GABAergic projection from the inferior colliculus to the auditory thalamus

2013 ◽  
Vol 109 (12) ◽  
pp. 2866-2882 ◽  
Author(s):  
Yamini Venkataraman ◽  
Edward L Bartlett
Keyword(s):  
Inferior Colliculus ◽  
Temporal Processing ◽  
Brain Slices ◽  
Critical Time ◽  
Membrane Properties ◽  
Auditory Temporal Processing ◽  
Postsynaptic Potentials ◽  
Auditory Thalamus ◽  
Inhibitory Postsynaptic Potentials ◽  
Medial Geniculate

The development of auditory temporal processing is important for processing complex sounds as well as for acquiring reading and language skills. Neuronal properties and sound processing change dramatically in auditory cortex neurons after the onset of hearing. However, the development of the auditory thalamus or medial geniculate body (MGB) has not been well studied over this critical time window. Since synaptic inhibition has been shown to be crucial for auditory temporal processing, this study examined the development of a feedforward, GABAergic connection to the MGB from the inferior colliculus (IC), which is also the source of sensory glutamatergic inputs to the MGB. IC-MGB inhibition was studied using whole cell patch-clamp recordings from rat brain slices in current-clamp and voltage-clamp modes at three age groups: a prehearing group [ postnatal day (P)7–P9], an immediate posthearing group (P15–P17), and a juvenile group (P22–P32) whose neuronal properties are largely mature. Membrane properties matured substantially across the ages studied. GABAA and GABAB inhibitory postsynaptic potentials were present at all ages and were similar in amplitude. Inhibitory postsynaptic potentials became faster to single shocks, showed less depression to train stimuli at 5 and 10 Hz, and were overall more efficacious in controlling excitability with age. Overall, IC-MGB inhibition becomes faster and more precise during a time period of rapid changes across the auditory system due to the codevelopment of membrane properties and synaptic properties.

Roles of Inhibition in Creating Complex Auditory Responses in the Inferior Colliculus: Facilitated Combination-Sensitive Neurons

2005 ◽  
Vol 93 (6) ◽  
pp. 3294-3312 ◽  
Author(s):  
Kiran Nataraj ◽  
Jeffrey J. Wenstrup
Keyword(s):  
Brain Stem ◽  
Inferior Colliculus ◽  
Low Frequency ◽  
Auditory Responses ◽  
Auditory Brain Stem ◽  
Neural Interactions ◽  
Lower Brain Stem ◽  
Excitatory Responses ◽  
Sonar Echoes ◽  
Inhibitory Interactions

We studied roles of inhibition on temporally sensitive facilitation in combination-sensitive neurons from the mustached bat's inferior colliculus (IC). In these integrative neurons, excitatory responses to best frequency (BF) tones are enhanced by much lower frequency signals presented in a specific temporal relationship. Most facilitated neurons (76%) showed inhibition at delays earlier than or later than the delays causing facilitation. The timing of inhibition at earlier delays was closely related to the best delay of facilitation, but the inhibition had little influence on the duration or strength of the facilitatory interaction. Local iontophoretic application of antagonists to receptors for glycine (strychnine, STRY) and γ-aminobutyric acid (GABA) (bicuculline, BIC) showed that STRY abolished facilitation in 96% of tested units, but BIC eliminated facilitation in only 28%. This suggests that facilitatory interactions are created in IC and reveals a differential role for these neurotransmitters. The facilitation may be created by coincidence of a postinhibitory rebound excitation activated by the low-frequency signal with the BF-evoked excitation. Unlike facilitation, inhibition at earlier delays was not eliminated by application of antagonists, suggesting an origin in lower brain stem nuclei. However, inhibition at delays later than facilitation, like facilitation itself, appears to originate within IC and to be more dependent on glycinergic than GABAergic mechanisms. Facilitatory and inhibitory interactions displayed by these combination-sensitive neurons encode information within sonar echoes and social vocalizations. The results indicate that these complex response properties arise through a series of neural interactions in the auditory brain stem and midbrain.

scholarly journals Transmitter Regulation of Plateau Properties in Turtle Motoneurons

1998 ◽  
Vol 79 (1) ◽  
pp. 45-50 ◽  
Author(s):  
Gytis Svirskis ◽  
Jørn Hounsgaard
Keyword(s):  
Membrane Potential ◽  
Metabotropic Glutamate Receptors ◽  
Input Resistance ◽  
Pattern Generation ◽  
Synaptic Activity ◽  
Membrane Properties ◽  
Resting Membrane Potential ◽  
Type I ◽  
Plateau Potentials ◽  
Inward Current

Svirskis, Gytis and Jørn Hounsgaard. Transmitter regulation of plateau properties in turtle motoneurons. J. Neurophysiol. 79: 45–50, 1998. In motoneurons, generation of plateau potentials is promoted by modulators that block potassium channels. In voltage-clamp experiments with triangular voltage ramp commands, we show that cis-(±)-1-aminocyclopentane-1,3-dicarboxylic acid ( cis-ACPD) and muscarine promote the generation of plateau potentials by increasing the dihydropyridine sensitive inward current, by increasing the input resistance, and by depolarizing the resting membrane potential. Type I metabotropic glutamate receptors (mGluR I) mediate the effects of cis-ACPD. Baclofen suppresses generation of plateau potentials by decreasing the dihydropyridine sensitive inward current, by decreasing the input resistance, and by hyperpolarizing the resting membrane potential. These results suggest that membrane properties of motoneurons are continuously modulated by synaptic activity in ways that may have profound effects on synaptic integration and pattern generation.

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)

Effects of intracochlear factors on spiral ganglion cells and auditory brain stem response after long-term electrical stimulation in deafened kittens

2000 ◽  
Vol 122 (3) ◽  
pp. 425-433
Author(s):  
Eugene N. Myers ◽  
Susumu Araki ◽  
Atsushi Kawano ◽  
H. Lee Seldon ◽  
Robert K. Shepherd ◽  
...  
Keyword(s):  
Brain Stem ◽  
Inferior Colliculus ◽  
Negative Correlation ◽  
Volume Fraction ◽  
Spiral Ganglion ◽  
Organ Of Corti ◽  
Scala Tympani ◽  
Auditory Brain Stem Response ◽  
Spiral Ganglion Cell ◽  
Auditory Brain Stem

Using an animal model, we have studied the response of the auditory brain stem to cochlear implantation and the effect of intracochlear factors on this response. Neonatally, pharmacologically deafened cats (100 to more than 180 days old) were implanted with a 4-electrode array in both cochleas. Then, the left cochlea of each cat was electrically stimulated for total periods of up to 1000 hours. After a terminal 14C-2-deoxyglucose (2DG) experiment, the fraction of the right inferior colliculus with a significant accumulation of 2DG label was calculated. Using 3-dimensional computer-aided reconstruction, we examined the cochleas of these animals for spiral ganglion cell (SGC) survival and intracochlear factors such as electrode positions, degeneration of the organ of Corti, and the degree of fibrosis of the scala tympani. The distribution of each parameter was calculated along the organ of Corti from the basal end. There was a positive correlation between SGC survival and the level of fibrosis in the scala tympani, and a negative correlation between SGC survival and the degree of organ of Corti degeneration. Finally, there was a negative correlation between the 2DG-labeled inferior colliculus volume fraction and the degree of fibrosis, particularly in the 1-mm region nearest the pair of electrodes, and presumably in the basal turn.

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