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.

Anatomic, Intrinsic, and Synaptic Properties of Dorsal and Ventral Division Neurons in Rat Medial Geniculate Body

1999 ◽  
Vol 81 (5) ◽  
pp. 1999-2016 ◽  
Author(s):  
Edward L. Bartlett ◽  
Philip H. Smith
Keyword(s):  
Membrane Potential ◽  
Nmda Receptors ◽  
Brain Slices ◽  
Medial Geniculate Body ◽  
Dendritic Tree ◽  
Dendritic Morphology ◽  
Thalamic Reticular Nucleus ◽  
Membrane Properties ◽  
Reticular Nucleus ◽  
Medial Geniculate

Anatomic, intrinsic, and synaptic properties of dorsal and ventral division neurons in rat medial geniculate body. Presently little is known about what basic synaptic and cellular mechanisms are employed by thalamocortical neurons in the two main divisions of the auditory thalamus to elicit their distinct responses to sound. Using intracellular recording and labeling methods, we characterized anatomic features, membrane properties, and synaptic inputs of thalamocortical neurons in the dorsal (MGD) and ventral (MGV) divisions in brain slices of rat medial geniculate body. Quantitative analysis of dendritic morphology demonstrated that tufted neurons in both divisions had shorter dendrites, smaller dendritic tree areas, more profuse branching, and a greater dendritic polarization compared with stellate neurons, which were only found in MGD. Tufted neuron dendritic polarization was not as strong or consistent as earlier Golgi studies suggested. MGV and MGD cells had similar intrinsic properties except for an increased prevalence of a depolarizing sag potential in MGV neurons. The sag was the only intrinsic property correlated with cell morphology, seen only in tufted neurons in either division. Many MGV and MGD neurons received excitatory and inhibitory inferior colliculus (IC) inputs (designated IN/EX or EX/IN depending on excitation/inhibition sequence). However, a significant number only received excitatory inputs (EX/O) and a few only inhibitory (IN/O). Both MGV and MGD cells displayed similar proportions of response combinations, but suprathreshold EX/O responses only were observed in tufted neurons. Excitatory and inhibitory postsynaptic potentials (EPSPs and IPSPs) had multiple distinguishable amplitude levels implying convergence. Excitatory inputs activated α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) and N-methyl-d-aspartate (NMDA) receptors the relative contributions of which were variable. For IN/EX cells with suprathreshold inputs, first-spike timing was independent of membrane potential unlike that of EX/O cells. Stimulation of corticothalamic (CT) and thalamic reticular nucleus (TRN) axons evoked a GABAA IPSP, EPSP, GABAB IPSP sequence in most neurons with both morphologies in both divisions. TRN IPSPs and CT EPSPs were graded in amplitude, again suggesting convergence. CT inputs activated AMPA and NMDA receptors. The NMDA component of both IC and CT inputs had an unusual voltage dependence with a detectable dl-2-amino-5-phosphonovaleric acid-sensitive component even below −70 mV. First-spike latencies of CT evoked action potentials were sensitive to membrane potential regardless of whether the TRN IPSP was present. Overall, our in vitro data indicate that reported regional differences in the in vivo responses of MGV and MGD cells to auditory stimuli are not well correlated with major differences in intrinsic membrane features or synaptic responses between cell types.

scholarly journals Analysis of excitatory and inhibitory neuron types in the inferior colliculus based on Ih properties

2019 ◽  
Vol 121 (6) ◽  
pp. 2126-2139
Author(s):  
Victor Naumov ◽  
Julia Heyd ◽  
Fauve de Arnal ◽  
Ursula Koch
Keyword(s):  
Inferior Colliculus ◽  
Firing Pattern ◽  
Yellow Fluorescent Protein ◽  
Brain Slices ◽  
Inhibitory Neuron ◽  
Gabaergic Neurons ◽  
Membrane Properties ◽  
Firing Patterns ◽  
Glutamatergic Neurons ◽  
Excitatory Neurons

The inferior colliculus (IC) is a large midbrain nucleus that integrates inputs from many auditory brainstem and cortical structures. Despite its prominent role in auditory processing, the various cell types and their connections within the IC are not well characterized. To further separate GABAergic and non-GABAergic neuron types according to their physiological properties, we used a mouse model that expresses channelrhodopsin and enhanced yellow fluorescent protein in all GABAergic neurons and allows identification of GABAergic cells by light stimulation. Neuron types were classified upon electrophysiological measurements of the hyperpolarizing-activated current ( Ih) in acute brain slices of young adult mice. All GABAergic neurons from our sample displayed slow-activating Ih with moderate amplitudes, whereas a subset of excitatory neurons showed fast-activating Ih with large amplitudes. This is in agreement with our finding that immunoreactivity against the fast-gating hyperpolarization-activated and cyclic-nucleotide-gated 1 (HCN1) channel was present around excitatory neurons, whereas the slow-gating HCN4 channel was found perisomatically around most inhibitory neurons. Ih properties and neurotransmitter types were correlated with firing patterns to depolarizing current pulses. All GABAergic neurons displayed adapting firing patterns very similar to the majority of glutamatergic neurons. About 15% of the glutamatergic neurons showed an onset spiking pattern, always in combination with large and fast Ih. We conclude that HCN channel subtypes are differentially distributed in IC neuron types and correlate with neurotransmitter type and firing pattern. In contrast to many other brain regions, membrane properties and firing patterns were similar in GABAergic neurons and about one-third of the excitatory neurons. NEW & NOTEWORTHY Neuron types in the central nucleus of the auditory midbrain are not well characterized regarding their transmitter type, ion channel composition, and firing pattern. The present study shows that GABAergic neurons have slowly activating hyperpolarizing-activated current ( Ih) and an adaptive firing pattern whereas at least four types of glutamatergic neurons exist regarding their Ih properties and firing patterns. Many of the glutamatergic neurons were almost indistinguishable from the GABAergic neurons regarding Ih properties and firing pattern.

scholarly journals Is GABA neurotransmission enhanced in auditory thalamus relative to inferior colliculus?

2014 ◽  
Vol 111 (2) ◽  
pp. 229-238 ◽  
Author(s):  
Rui Cai ◽  
Bopanna I. Kalappa ◽  
Thomas J. Brozoski ◽  
Lynne L. Ling ◽  
Donald M. Caspary
Keyword(s):  
Inferior Colliculus ◽  
Chloride Channel ◽  
Single Unit ◽  
Ex Vivo ◽  
Medial Geniculate Body ◽  
Gamma Aminobutyric Acid ◽  
Auditory Thalamus ◽  
Medial Geniculate

Gamma-aminobutyric acid (GABA) is the major inhibitory neurotransmitter in the central auditory system. Sensory thalamic structures show high levels of non-desensitizing extrasynaptic GABAA receptors (GABAARs) and a reduction in the redundancy of coded information. The present study compared the inhibitory potency of GABA acting at GABAARs between the inferior colliculus (IC) and the medial geniculate body (MGB) using quantitative in vivo, in vitro, and ex vivo experimental approaches. In vivo single unit studies compared the ability of half maximal inhibitory concentrations of GABA to inhibit sound-evoked temporal responses, and found that GABA was two to three times ( P < 0.01) more potent at suppressing MGB single unit responses than IC unit responses. In vitro whole cell patch-clamp slice recordings were used to demonstrate that gaboxadol, a δ-subunit selective GABAAR agonist, was significantly more potent at evoking tonic inhibitory currents from MGB neurons than IC neurons ( P < 0.01). These electrophysiological findings were supported by an in vitro receptor binding assay which used the picrotoxin analog [3H]TBOB to assess binding in the GABAAR chloride channel. MGB GABAARs had significantly greater total open chloride channel capacity relative to GABAARs in IC ( P < 0.05) as shown by increased total [3H]TBOB binding. Finally, a comparative ex vivo measurement compared endogenous GABA levels and suggested a trend towards higher GABA concentrations in MGB than in IC. Collectively, these studies suggest that, per unit GABA, high affinity extrasynaptic and synaptic GABAARs confer a significant inhibitory GABAAR advantage to MGB neurons relative to IC neurons. This increased GABA sensitivity likely underpins the vital filtering role of auditory thalamus.

The Roles of Endogenous Membrane Properties and Synaptic Interaction in Generating the Heartbeat Rhythm of the Leech, Hirudo Medicinalis

1979 ◽  
Vol 82 (1) ◽  
pp. 163-176
Author(s):  
RONALD L. CALABRESE
Keyword(s):  
Electrical Coupling ◽  
Physiological Saline ◽  
Endogenous Rhythm ◽  
Membrane Properties ◽  
Inhibitory Synapses ◽  
Postsynaptic Potentials ◽  
Inhibitory Postsynaptic Potentials ◽  
Current Pulses ◽  
Motor Neurones ◽  
Inhibitory Interactions

1. Inhibitory synapses among the central neurones involved in the generation of the heartbeat rhythm of the leech were blocked by either low Cl− physiological saline or presynaptic hyperpolarizing current. 2. Low Cl− saline reversibly blocked inhibitory postsynaptic potentials (IPSPs) from the HN cells onto both other HN cells and HE cells but did not block electrical coupling among HN cells. 3. The rhythmic bursts of impulses in HE cells were abolished when IPSPs were blocked by either low Cl− saline or hyperpolarization of HN cells. 4. The rhythmic bursts of impulses in HN cells were not abolished (except in cell HN(5)) when IPSPs were blocked by low Cl− saline, but phase relations became unfixed (unless the cells were electrically coupled). 5. Both brief depolarizing and hyperpolarizing current pulses reset the rhythm of HN cells whose IPSPs were blocked by low Cl− saline. 6. The results indicate that the motor neurones to the heart (HE cells) produce rhythmic impulse bursts because their steady discharge is periodically inhibited by the HN interneurones. The pattern generated by the HN cells originates from an endogenous rhythm co-ordinated by the inhibitory interactions and electrical coupling between these cells.

Membrane Properties and Firing Patterns of Inferior Colliculus Neurons: An In Vivo Patch-Clamp Study in Rodents

2007 ◽  
Vol 98 (1) ◽  
pp. 443-453 ◽  
Author(s):  
M. L. Tan ◽  
H. P. Theeuwes ◽  
L. Feenstra ◽  
J.G.G. Borst
Keyword(s):  
Patch Clamp ◽  
Inferior Colliculus ◽  
Membrane Properties ◽  
Resting Membrane Potential ◽  
Firing Patterns ◽  
Postsynaptic Potentials ◽  
Whole Cell Patch Clamp ◽  
Auditory Nucleus ◽  
Clamp Study

The inferior colliculus (IC) is a large auditory nucleus in the midbrain, which is a nearly obligatory relay center for ascending auditory projections. We made in vivo whole cell patch-clamp recordings of IC cells in young-adult anesthetized C57/Bl6 mice and Wistar rats to characterize their membrane properties and spontaneous inputs. We observed spikelets in both rat (18%) and mouse (13%) IC neurons, suggesting that IC neurons may be connected by electrical synapses. In many cells, spontaneous postsynaptic potentials were sufficiently large to contribute to spike irregularity. Cells differed considerably in the number of simultaneous spontaneous postsynaptic potentials that would be needed to trigger an action potential. Depolarizing and hyperpolarizing current injections showed six different types of firing patterns: buildup, accelerating, burst-onset, burst-sustained, sustained, and accommodating. Their relative frequencies were similar in both species. In mice, about half of the cells showed a clear depolarizing sag, suggesting that they have the hyperpolarization-activated current Ih. This sag was observed more often in burst and in accommodating cells than in buildup, accelerating, or sustained neurons. Cells with Ih had a significantly more depolarized resting membrane potential. They were more likely to fire rebound spikes and generally showed long-lasting afterhyperpolarizations following long depolarizations. We therefore suggest a separate functional role for Ih.

Phase-Locked Responses to Pure Tones in the Auditory Thalamus

2007 ◽  
Vol 98 (4) ◽  
pp. 1941-1952 ◽  
Author(s):  
Mark N. Wallace ◽  
Lucy A. Anderson ◽  
Alan R. Palmer
Keyword(s):  
Guinea Pig ◽  
Inferior Colliculus ◽  
Phase Locking ◽  
Medial Geniculate Body ◽  
Low Frequency ◽  
Sine Wave ◽  
Temporal Coding ◽  
Auditory Thalamus ◽  
Medial Geniculate ◽  
The Brain

Accurate temporal coding of low-frequency tones by spikes that are locked to a particular phase of the sine wave (phase-locking), occurs among certain groups of neurons at various processing levels in the brain. Phase-locked responses have previously been studied in the inferior colliculus and neocortex of the guinea pig and we now describe the responses in the auditory thalamus. Recordings were made from 241 single units, 32 (13%) of which showed phase-locked responses. Units with phase-locked responses were mainly (82%) located in the ventral division of the medial geniculate body (MGB), and also the medial division (18%), but were not found in the dorsal or shell divisions. The upper limiting frequency of phase-locking varied greatly between units (60–1,100 Hz) and between anatomical divisions. The upper limit in the ventral division was 520 Hz and in the medial was 1,100 Hz. The range of steady-state delays calculated from phase plots also varied: ventral division, 8.6–14 ms (mean 11.1 ms; SD 1.56); medial division, 7.5–11 ms (mean 9.3 ms; SD 1.5). Taken together, these measurements are consistent with the medial division receiving a phase-locked input directly from the brain stem, without an obligatory relay in the inferior colliculus. Cells in both the ventral and medial divisions of the MGB showed a response that phase-locked to the fundamental frequency of a guinea pig purr and may be involved in analyzing communication calls.

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.

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