GABAB-Receptor-Mediated Inhibition in Developing Mouse Ventral Posterior Thalamic Nucleus

1997 ◽  
Vol 78 (1) ◽  
pp. 550-553 ◽  
Author(s):  
Richard A. Warren ◽  
Peyman Golshani ◽  
Edward G. Jones
Keyword(s):  
Postnatal Development ◽  
Thalamic Nucleus ◽  
Gabab Receptor ◽  
Reversal Potential ◽  
Internal Capsule ◽  
Postnatal Period ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Most Significant Change

Warren, Richard A., Peyman Golshani, and Edward G. Jones. GABAB-receptor-mediated inhibition in developing mouse ventral posterior thalamic nucleus. J. Neurophysiol. 78: 549–553, 1997. Inhibitory postsynaptic potentials (IPSPs) generated by activation of the thalamic reticular nucleus (RTN) were recorded in neurons of the ventral posterior nucleus (VP) in vitro in slices from mice aged postnatal day (P)1–P17. An early IPSP peaking 41 ± 2.5 (SE) ms after electrical stimulation of the internal capsule or RTN was found in 96% of VP neurons. This early IPSP was blocked by bicuculline, showing its dependence on γ-aminobutyric acid-A (GABAA) receptors. A late IPSP peaking 357 ± 27 ms after the stimulus was observed in 22% of VP neurons in control medium but was uncovered in 38% of neurons when bicuculline was added. The late IPSP was blocked by addition of a GABAB antagonist, 2-hydroxysaclofen, to the medium ( n = 7); it had a reversal potential of −98 ± 1.3 mV, 14 mV negative to the early component. In contrast to the early IPSP, whose reversal potential became more negative during postnatal development, the reversal potential of the late IPSP remained constant throughout the postnatal period studied. The most significant change in the late IPSP was shortening in duration, with reduction in latency-to-peak by >400 ms, between P1 and P10. No changes of comparable magnitude were observed in the duration of the earlier GABAA response. These results show that both GABAA and GABAB IPSPs are present very early in the postnatal thalamus and that their characteristics evolve along independent paths during postnatal development.

Oscillatory synaptic interactions between ventroposterior and reticular neurons in mouse thalamus in vitro

1994 ◽  
Vol 72 (4) ◽  
pp. 1993-2003 ◽  
Author(s):  
R. A. Warren ◽  
A. Agmon ◽  
E. G. Jones
Keyword(s):  
Receptor Antagonist ◽  
Gabab Receptor ◽  
Initial Response ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Excitatory Postsynaptic Potential ◽  
Postsynaptic Potential ◽  
Synaptic Interactions ◽  
Gabaa Receptor Antagonist

1. The thalamic reticular nucleus (RTN) has reciprocal connections with relay neurons in the dorsal thalamus. We used whole cell recording in a mouse in vitro slice preparation maintained at room temperature to study the synaptic interactions between the RTN and the ventroposterior thalamic nucleus (VP) during evoked low-frequency oscillations. 2. After a single electrical stimulus of the internal capsule, postsynaptic potentials (PSPs) were recorded in all VP and RTN neurons. In 76% of slices, there was an initial response followed by recurrent PSPs lasting for up to 8 s and with a frequency of approximately 2 Hz in both the VP and RTN. 3. In RTN neurons the initial response consisted of a fast excitatory postsynaptic potential (EPSP) that generated a burst of action potentials. Recurrent PSPs consisted of barrages of EPSPs that often reached burst threshold. The structure of subthreshold EPSP barrages in RTN neurons suggested that they were generated by bursting VP neurons. 4. In VP neurons the stimulus usually evoked a small EPSP followed by a large inhibitory postsynaptic potential (IPSP) that was often followed by a rebound burst. This initial response was often followed by a series of recurrent IPSPs presumably generated by RTN bursts, because intrinsic inhibitory neurons are absent in rodent VP. 5. IPSPs in VP neurons and recurrent EPSPs in RTN neurons were completely abolished by application of a gamma-aminobutyric acid-A (GABAA) receptor antagonist. A GABAB receptor antagonist produced no or little change in either the initial or recurrent response. 6. Recurrent IPSPs in VP neurons were abolished by glutamate receptor antagonists before the initial IPSP, which always remained stimulus dependent. 7. The dependency of recurring IPSPs in VP and recurring EPSPs in RTN upon GABA-mediated inhibition and excitatory amino acid-mediated excitation, plus the character of recurring EPSPs in the RTN strongly suggest that the recurring events were generated through reverse-reciprocal synaptic interactions between VP and RTN neurons. These synaptic interactions most likely play an important role in thalamic oscillations in behavior.

Inhibitory Interactions Between Ferret Thalamic Reticular Neurons

2002 ◽  
Vol 87 (5) ◽  
pp. 2571-2576 ◽  
Author(s):  
Yousheng Shu ◽  
David A. McCormick
Keyword(s):  
Reversal Potential ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Inhibitory Input ◽  
Inhibitory Interaction ◽  
Postsynaptic Potentials ◽  
Inhibitory Postsynaptic Potentials ◽  
Reticular Neurons ◽  
Inhibitory Interactions

The thalamic reticular nucleus (nRt) provides an important inhibitory input to thalamic relay nuclei and is central in the generation of both normal and abnormal thalamocortical activities. Although local inhibitory interactions between these neurons may play an important role in controlling thalamocortical activities, the physiological features of this interaction have not been fully investigated. Here we sought to establish the nature of inhibitory interaction between nRt neurons with intracellular and extracellular recordings in slices of ferret nRt maintained in vitro. In many nRt neurons, intracellular recordings revealed spontaneous inhibitory postsynaptic potentials (IPSPs). In addition, the local excitation of nRt cells with glutamate led to the generation of IPSPs in the intracellularly recorded nRt neuron. These evoked IPSPs exhibited an average reversal potential of −72 mV and could be blocked by picrotoxin, a GABAA-receptor antagonist. These results indicate that nRt neurons interact locally through the activation of GABAA receptor-mediated inhibitory postsynaptic potentials. This lateral inhibition may play an important role in controlling the responsiveness of these cells to cortical and thalamic excitatory inputs in both normal and abnormal thalamocortical function.

Cholecystokinin depolarizes rat thalamic reticular neurons by suppressing a K+ conductance

1995 ◽  
Vol 74 (3) ◽  
pp. 990-1000 ◽  
Author(s):  
C. L. Cox ◽  
J. R. Huguenard ◽  
D. A. Prince
Keyword(s):  
Reversal Potential ◽  
Membrane Conductance ◽  
Membrane Depolarization ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Equilibrium Potential ◽  
K Channel ◽  
Neuron Activity ◽  
Cck Receptors

1. The thalamic reticular nucleus (nRt) is innervated by cholecystokinin (CCK)-containing neurons and contains CCK binding sites. We used tight-seal, whole cell recording techniques with in vitro rat thalamic slices to investigate the action of CCK on neurons in nRt and ventrobasal thalamus (VB). 2. Brief applications of the CCK agonist cholecystokinin octapeptide (26-33) sulfated (CCK8S) evoked prolonged spike discharges in nRt neurons but had no direct effects on VB neuron activity. This selective excitatory action of CCK8S in nRt resulted from a long-lasting membrane depolarization (2-10 min) associated with an increased input resistance. Voltage-clamp recordings revealed that CCK8S reduced membrane conductance by 0.6-3.8 nS, which amounted to 5-54% of the resting conductance of these neurons. 3. The conductance blocked by CCK8S was linear over the range of -50 to -100 mV and reversed near the potassium equilibrium potential. Modifications of extracellular K+ concentration altered the reversal potential of the conductance as predicted by the Nernst equation. The K+ channel blocker Cs+, applied either intracellularly or combined intra- and extracellularly, blocked the response to CCK8S. 4. The CCK8S-induced depolarization persisted after suppression of synaptic transmission by either tetrodotoxin or a low-Ca2+, high-Mg2+ extracellular solution, indicating that the depolarization was primarily due to activation of postsynaptic CCK receptors and not mediated through the release of other neurotransmitters. 5. The selective CCKA antagonists L364,718 and Cam-1481 attenuated the CCK8S-induced depolarization, whereas the CCKB antagonist L365,260 had little or no effect on the depolarization. 6. Our findings indicate that CCK8S, acting via CCKA-type receptors, reduces a K+ leak current, resulting in a long-lasting membrane depolarization that can presumably modify the firing mode of nRt neurons. Through this effect, CCK actions in nRt may strongly influence thalamocortical function.

scholarly journals Focal Stimulation of the Thalamic Reticular Nucleus Induces Focal Gamma Waves in Cortex

1998 ◽  
Vol 79 (1) ◽  
pp. 474-477 ◽  
Author(s):  
Kurt D. Macdonald ◽  
Eva Fifkova ◽  
Michael S. Jones ◽  
Daniel S. Barth
Keyword(s):  
Electrical Stimulation ◽  
Internal Capsule ◽  
Thalamic Reticular Nucleus ◽  
Gamma Activity ◽  
Reticular Nucleus ◽  
Cortical Arousal ◽  
Electrical Potentials ◽  
Gamma Frequency ◽  
Slow Potentials ◽  
Stimulation Of

MacDonald, Kurt D., Eva Fifkova, Michael S. Jones, and Daniel S. Barth. Focal stimulation of the thalamic reticular nucleus induces focal gamma waves in cortex. J. Neurophysiol. 79: 474–477, 1998. Electrical stimulation of the thalamic reticular nucleus (TRN; 0.5-s trains of 500-Hz 0.5-ms pulses at 5–10 μA) evokes focal oscillations of cortical electrical potentials in the gamma frequency band (∼35–55 Hz). These evoked oscillations are specific to either the somatosensory or auditory cortex and to subregions of the cortical receptotopic map, depending on what part of the TRN is stimulated. Focal stimulation of the internal capsule, however, evokes focal slow potentials, without gamma activity. Our results suggest that the TRN's role extends beyond that of general cortical arousal to include specific modality and submodality activation of the forebrain.

Synchronization properties of spindle oscillations in a thalamic reticular nucleus model

1994 ◽  
Vol 72 (3) ◽  
pp. 1109-1126 ◽  
Author(s):  
D. Golomb ◽  
X. J. Wang ◽  
J. Rinzel
Keyword(s):  
Time Course ◽  
Cluster State ◽  
Large Population ◽  
Reversal Potential ◽  
Ionic Currents ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Quiescent State ◽  
Gamma Aminobutyric Acid ◽  
Cluster States

1. We address the hypothesis of Steriade and colleagues that the thalamic reticular nucleus (RE) is a pacemaker for thalamocortical spindle oscillations by developing and analyzing a model of a large population of all-to-all coupled inhibitory RE neurons. 2. Each RE neuron has three ionic currents: a low-threshold T-type Ca2+ current (ICa-T), a calcium-activated potassium current (IAHP) and a leakage current (IL). ICa-T underlies a cell's postinhibitory rebound properties, whereas IAHP hyperpolarizes the neuron after a burst. Each neuron, which is a conditional oscillator, is coupled to all other RE neurons via fast gamma-aminobutyric acid-A (GABAA) and slow GABAB synapses. 3. For generating network oscillations IAHP may not be necessary. Synaptic inhibition can provide the hyperpolarization for deinactivating ICa-T that causes bursting if the reversal potentials for GABAA and GABAB synapses are sufficiently negative. 4. If model neurons display sufficiently powerful rebound excitability, an isolated RE network of such neurons oscillates with partial but typically not full synchrony. The neurons spontaneously segregate themselves into several macroscopic clusters. The neurons within a cluster follow the same time course, but the clusters oscillate differently from one another. In addition to activity patterns in which clusters burst sequentially (e.g., 2 or 3 clusters bursting alternately), a two-cluster state may occur with one cluster active and one quiescent. Because the neurons are all-to-all coupled, the cluster states do not have any spatial structure. 5. We have explored the sensitivity of such partially synchronized patterns to heterogeneity in cells' intrinsic properties and to simulated neuroelectric noise. Although either precludes precise clustering, modest levels of heterogeneity or noise lead to approximate clustering of active cells. The population-averaged voltage may oscillate almost regularly but individual cells burst at nearly every second cycle or less frequently. The active-quiescent state is not robust at all to heterogeneity or noise. Total asynchrony is observed when heterogeneity or noise is too large, e.g., even at 25% heterogeneity for our reference set of parameter values. 6. The fast GABAA inhibition (with a reversal potential more negative than, say, -65 mV) favors the cluster states and prevents full synchrony. Our simulation results suggest two mechanisms that can fully synchronize the isolated RE network model. With GABAA removed or almost totally blocked, GABAB inhibition (because it is slow) can lead to full synchrony, which is partially robust to heterogeneity and noise.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Corticothalamic Inhibition in the Thalamic Reticular Nucleus

2004 ◽  
Vol 91 (2) ◽  
pp. 759-766 ◽  
Author(s):  
Liming Zhang ◽  
Edward G. Jones
Keyword(s):  
Barrel Cortex ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Receptor Antagonists ◽  
Experimental Conditions ◽  
Inhibitory Network ◽  
Corticothalamic Projection ◽  
Substantial Network ◽  
Layer Vi

Mutual inhibition between the GABAergic cells of the thalamic reticular nucleus (RTN) is important in regulating oscillations in the thalamocortical network, promoting those in the spindle range of frequencies over those at lower frequencies. Excitatory inputs to the RTN from the cerebral cortex are numerically large and particularly powerful in inducing spindles. However, the extent to which corticothalamic influences can engage the inhibitory network of the RTN has not been fully explored. Focal electrical stimulation of layer VI in the barrel cortex of the mouse thalamocortical slice in vitro resulted in prominent di- or polysynaptic inhibitory postsynaptic currents (IPSCs) in RTN cells under the experimental conditions used. The majority of cortically induced responses consisted of mixed PSCs in which the inhibitory component predominated or of large IPSCs alone, implying inhibition of neighboring cells by other, cortically excited RTN cells. Within the mixed PSCs, fixed and variable latency components could commonly be identified. IPSCs could be blocked by application of ionotropic glutamate receptor antagonists or of GABAA receptor antagonists, also indicating their dependence on corticothalamic excitation triggering disynaptic or polysynaptic inhibition. Spontaneous GABAA receptor-dependent IPSCs were routinely observed in the RTN and, taken together with the results of cortical stimulation, indicate the existence of a substantial network of intrareticular inhibitory connections that can be effectively recruited by the corticothalamic system. These results suggest activation of cortical excitatory inputs triggers the propagation of inhibitory currents within the RTN and support the view that activation of the RTN from the somatosensory cortex, although focused by the topography of the corticothalamic projection, is capable of disynaptically engaging the whole inhibitory network of the RTN, by local and probably by reentrant GABAA receptor–based synapses, thus spreading the corticothalamic influence throughout the RTN.

scholarly journals A thalamic reticular circuit for head direction cell tuning and spatial navigation

2019 ◽  
Author(s):  
Gil Vantomme ◽  
Zita Rovó ◽  
Romain Cardis ◽  
Elidie Béard ◽  
Georgia Katsioudi ◽  
...  
Keyword(s):  
Spatial Navigation ◽  
Sensory Information ◽  
Search Strategies ◽  
Retrosplenial Cortex ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Head Direction ◽  
Thalamic Nuclei

SummaryTo navigate in space, an animal must refer to sensory cues to orient and move. Circuit and synaptic mechanisms that integrate cues with internal head-direction (HD) signals remain, however, unclear. We identify an excitatory synaptic projection from the presubiculum (PreS) and the multisensory-associative retrosplenial cortex (RSC) to the anterodorsal thalamic reticular nucleus (TRN), so far classically implied in gating sensory information flow. In vitro, projections to TRN involved AMPA/NMDA-type glutamate receptors that initiated TRN cell burst discharge and feedforward inhibition of anterior thalamic nuclei. In vivo, chemogenetic anterodorsal TRN inhibition modulated PreS/RSC-induced anterior thalamic firing dynamics, broadened the tuning of thalamic HD cells, and led to preferential use of allo-over egocentric search strategies in the Morris water maze. TRN-dependent thalamic inhibition is thus an integral part of limbic navigational circuits wherein it coordinates external sensory and internal HD signals to regulate the choice of search strategies during spatial navigation.

Functional Mapping of GABAB-Receptor Subtypes in the Thalamus

2007 ◽  
Vol 98 (6) ◽  
pp. 3791-3795 ◽  
Author(s):  
Daniel Ulrich ◽  
Valérie Besseyrias ◽  
Bernhard Bettler
Keyword(s):  
Cognitive Deficits ◽  
Gabab Receptor ◽  
Cell Activity ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Receptor Subtypes ◽  
Type B ◽  
Acid Type ◽  
Output Neurons ◽  
Electrophysiological Methods

The thalamus plays an important role in attention mechanisms and the generation of brain rhythms. γ-Aminobutyric acid type B (GABAB) receptors are known to regulate the main output neurons of the thalamus, the thalamocortical relay (TCR) cells. However, the contributions of the two predominant GABAB-receptor subtypes, GABAB(1a,2) and GABAB(1b,2), to the control of TCR cell activity are unknown. Here, we used genetic and electrophysiological methods to investigate subtype-specific GABAB effects at the inputs to TCR cells. We found that mainly GABAB(1a,2) receptors inhibit the release of glutamate from corticothalamic fibers impinging onto TCR cells. In contrast, both GABAB(1a,2) and GABAB(1b,2) receptors efficiently inhibit the release of GABA from thalamic reticular nucleus (TRN) neurons onto TCR neurons. Likewise, both GABAB(1a,2) and GABAB(1b,2) receptors efficiently activate somatodendritic K+ currents in TCR cells. In summary, our data show that GABAB(1b,2) receptors cannot compensate for the absence of GABAB(1a,2) receptors at glutamatergic inputs to TCR cells. This shows that the predominant association of GABAB(1a,2) receptors with glutamatergic terminals is a feature that is preserved at several brain synapses. Furthermore, our data indicate that the cognitive deficits observed with mice lacking GABAB(1a,2) receptors could to some extent relate to attention deficits caused by disinhibited release of glutamate onto TCR neurons.

Giant Spontaneous Depolarizing Potentials in the Developing Thalamic Reticular Nucleus

2007 ◽  
Vol 97 (3) ◽  
pp. 2364-2372 ◽  
Author(s):  
Susanne Pangratz-Fuehrer ◽  
Uwe Rudolph ◽  
John R. Huguenard
Keyword(s):  
Developmental Stage ◽  
Postnatal Development ◽  
Gaba Receptors ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Glutamate Antagonists ◽  
Early Postnatal Development ◽  
Functional Development ◽  
Α3 Subunit ◽  
Cortical Circuit

The thalamic reticular nucleus (nRt) provides a major source of inhibition in the thalamo-cortical circuit and is critically involved in the generation of spindle oscillations. Here we describe the properties of thalamic giant depolarizing potentials (tGDPs) that were observed in nRt during early development. tGDPs persisted in presence of ionotropic glutamate antagonists but were completely abolished by GABAAR antagonist SR 35591. tGDPs occurred primarily between p3 and p8 (in 30–50% of cells) and occasionally up until p15. tGDPs lasted 0.4–3 s with peak conductances of 2–13 nS and occurred at frequencies between 0.02 and 0.06 Hz. We used mice with a benzodiazepine-insensitive α3 subunit [α3(H126R)] to probe for the identity of the GABA receptors responsible for tGDP generation. Benzodiazepine enhancement of tGDP amplitude and duration persisted in nRt neurons in α3(H126R) mice, indicating that the GABAARs containing α3 are not critical for tGDP generation and suggesting that tGDPs are mediated by GABAARs containing the α5 subunit, which is transiently expressed in nRt neurons in early postnatal development. Furthermore we found that exogenous GABA application depolarized nRt neurons younger than p8, indicating elevated [Cl−]i at this developmental stage. Taken together, these data suggest that in immature nRt, long-lasting depolarizing responses mediated by GABA receptors could trigger Ca2+ entry and play a role in functional development of the spindle-generating circuitry.

scholarly journals Postnatal development of cholinergic input to the thalamic reticular nucleus of the mouse

2018 ◽  
Vol 49 (8) ◽  
pp. 978-989 ◽  
Author(s):  
Guela Sokhadze ◽  
Peter W. Campbell ◽  
William Guido
Keyword(s):  
Postnatal Development ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus
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