Mapping of the Functional Interconnections Between Thalamic Reticular Neurons Using Photostimulation

2006 ◽  
Vol 96 (5) ◽  
pp. 2593-2600 ◽  
Author(s):  
Ying-Wan Lam ◽  
Christopher S. Nelson ◽  
S. Murray Sherman
Keyword(s):  
Laser Scanning ◽  
Spatial Extent ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Reticular Cell ◽  
Relay Cell ◽  
Dominant Form ◽  
Electrical Synapses ◽  
Reticular Neurons ◽  
Reticular Cells

The thalamic reticular nucleus is strategically located in the axonal pathways between thalamus and cortex, and reticular cells exert strong, topographic inhibition on thalamic relay cells. Although evidence exists that reticular neurons are interconnected through conventional and electrical synapses, the spatial extent and relative strength of these synapses are unclear. To address these issues, we used uncaging of glutamate by laser-scanning photostimulation to provide precisely localized and consistent activation of reticular cell bodies and dendrites in an in vitro slice preparation from the rat as a means to study reticulo-reticular connections. Among the 47 recorded reticular neurons, 29 (62%) received GABAergic axodendritic input from an area immediately surrounding each of the recorded cell bodies, and 8 (17%) responded with depolarizing spikelets, suggesting inputs through electrical synapses. We also found that TTX completely blocked all evoked IPSCs, implying that any dendrodendritic synapses between reticular cells either are relatively weak, have no nearby glutamatergic receptors, or are dependent on back-propagation of action potentials. Finally, we showed that the GABAergic connections between reticular cells are weaker than those from reticular cells to relay cells. Our results suggest that the GABAergic axodendritic synapse is the dominant form of reticulo-reticular connectivity, and because they are much weaker than the reticulo-relay cell synapses, their functional purpose may be to regulate the spatial extent of the reticular inhibition on relay cells.

Mapping by Laser Photostimulation of Connections Between the Thalamic Reticular and Ventral Posterior Lateral Nuclei in the Rat

2005 ◽  
Vol 94 (4) ◽  
pp. 2472-2483 ◽  
Author(s):  
Ying-Wan Lam ◽  
S. Murray Sherman
Keyword(s):  
Laser Scanning ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Relay Cell ◽  
Reticular Neurons ◽  
Caged Glutamate ◽  
Tracing Techniques ◽  
Laser Scanning Photostimulation ◽  
Lateral Nucleus

We used laser scanning photostimulation through a focused UV laser of caged glutamate in an in vitro slice preparation through the rat’s somatosensory thalamus to study topography and connectivity between the thalamic reticular nucleus and ventral posterior lateral nucleus. This enabled us to focally stimulate the soma or dendrites of reticular neurons. We were thus able to confirm and extend previous observations based mainly on neuroanatomical pathway tracing techniques: the projections from the thalamic reticular nucleus to the ventral posterior lateral nucleus have precise topography. The reticular zone, which we refer to as a “footprint,” within which photostimulation evoked inhibitory postsynaptic currents (IPSCs) in relay cells, was relatively small and oval, with the long axis being parallel to the border between the thalamic reticular nucleus and ventral posterior lateral nucleus. These evoked IPSCs were large, and by using appropriate GABA antagonists, we were able to show both GABAA and GABAB components. This suggests that photostimulation strongly activated reticular neurons. Finally, we were able to activate a disynaptic relay cell-to-reticular-to- relay cell pathway by evoking IPSCs in relay cells from photostimulation of the region surrounding a recorded relay cell. This, too, suggests strong responses of relay cells, responses strong enough to evoke spiking in their postsynaptic reticular targets. The regions of photostimulation for these disynaptic responses were much larger than the above-mentioned reticular footprints, and this suggests that reticulothalamic axon arbors are less widespread than thalamoreticular arbors, that there is more convergence in thalamoreticular connections than in reticulothalamic connections, or both.

scholarly journals Two classes of excitatory synaptic responses in rat thalamic reticular neurons

2016 ◽  
Vol 116 (3) ◽  
pp. 995-1011 ◽  
Author(s):  
Charlotte Deleuze ◽  
John R. Huguenard
Keyword(s):  
Nmda Receptors ◽  
Sensory Processing ◽  
Clustering Algorithm ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Reticular Cell ◽  
Reticular Neurons ◽  
Relay Neurons

The thalamic reticular nucleus (nRt), composed of GABAergic cells providing inhibition of relay neurons in the dorsal thalamus, receives excitation from the neocortex and thalamus. The two excitatory pathways promoting feedback or feedforward inhibition of thalamocortical neurons contribute to sensory processing and rhythm generation. While synaptic inhibition within the nRt has been carefully characterized, little is known regarding the biophysics of synaptic excitation. To characterize the functional properties of thalamocortical and corticothalamic connections to the nRt, we recorded minimal electrically evoked excitatory postsynaptic currents from nRt cells in vitro. A hierarchical clustering algorithm distinguished two types of events. Type 1 events had larger amplitudes and faster kinetics, largely mediated by α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors, whereas type 2 responses had more prominent N-methyl-d-aspartate (NMDA) receptor contribution. Type 1 responses showed subnormal axonal propagation and paired pulse depression, consistent with thalamocortical inputs. Furthermore, responses kinetically similar to type 1 events were evoked by glutamate-mediated activation of thalamic neurons. Type 2 responses, in contrast, likely arise from corticothalamic inputs, with larger NMDA conductance and weak Mg2+-dependent block, suggesting that NMDA receptors are critical for the cortical excitation of reticular neurons. The long-lasting action of NMDA receptors would promote reticular cell burst firing and produce powerful inhibitory output to relay neurons proposed to be important in triggering epilepsy. This work provides the first complete voltage-clamp analysis of the kinetics and voltage dependence of AMPA and NMDA responses of thalamocortical and corticothalamic synapses in the nRt and will be critical in optimizing biologically realistic neural network models of thalamocortical circuits relevant to sensory processing and thalamocortical oscillations.

scholarly journals Electrical Synapses in the Thalamic Reticular Nucleus

2002 ◽  
Vol 22 (3) ◽  
pp. 1002-1009 ◽  
Author(s):  
Carole E. Landisman ◽  
Michael A. Long ◽  
Michael Beierlein ◽  
Michael R. Deans ◽  
David L. Paul ◽  
...  
Keyword(s):  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Electrical Synapses

scholarly journals Different Topography of the Reticulothalmic Inputs to First- and Higher-Order Somatosensory Thalamic Relays Revealed Using Photostimulation

2007 ◽  
Vol 98 (5) ◽  
pp. 2903-2909 ◽  
Author(s):  
Ying-Wan Lam ◽  
S. Murray Sherman
Keyword(s):  
Laser Scanning ◽  
Higher Order ◽  
Gabaergic Neurons ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Local Inhibition ◽  
Strategic Position ◽  
Almost All ◽  
Laser Scanning Photostimulation ◽  
Lateral Nucleus

The thalamic reticular nucleus is a layer of GABAergic neurons that occupy a strategic position between the thalamus and cortex. Here we used laser scanning photostimulation to compare in young mice (9–12 days old) the organization of the reticular inputs to first- and higher-order somatosensory relays, namely, the ventral posterior lateral nucleus and posterior nucleus, respectively. The reticulothalamic input footprints to the ventral posterior lateral nucleus neurons consisted of small, single, topographically organized elliptical regions in a tier away from the reticulothalamic border. In contrast, those to the posterior nucleus were complicated and varied considerably among neurons: although almost all contained a single elliptical region near the reticulothalamic border, in most cases, they consisted of additional discontinuous regions or relatively diffuse regions throughout the thickness of the thalamic reticular nucleus. Our results suggest two sources of reticular inputs to the posterior nucleus neurons: one that is relatively topographic from regions near the reticulothalamic border and one that is relatively diffuse and convergent from most or all of the thickness of the thalamic reticular nucleus. We propose that the more topographic reticular input is the basis of local inhibition seen in posterior nucleus neurons and that the more diffuse and convergent input may represent circuitry through which the ventral posterior lateral and posterior nuclei interact.

scholarly journals Activity-dependent long-term potentiation of electrical synapses in the mammalian thalamus

2019 ◽  
Author(s):  
Brandon Fricker ◽  
Emily Heckman ◽  
Patrick C. Cunningham ◽  
Julie S. Haas
Keyword(s):  
Brain Area ◽  
Long Term Potentiation ◽  
Electrical Synapse ◽  
Thalamic Reticular Nucleus ◽  
Calcium Flux ◽  
Reticular Nucleus ◽  
Electrical Synapses ◽  
Term Potentiation ◽  
Activity Dependent

AbstractActivity-dependent changes of synapse strength have been extensively characterized at chemical synapses, but the relationship between physiological forms of activity and strength at electrical synapses remains poorly understood. For mammalian electrical synapses composed of hexomers of connexin36, physiological forms of neuronal activity in coupled pairs has thus far have only been linked to long-term depression; activity that results in strengthening of electrical synapses has not yet been identified. The thalamic reticular nucleus (TRN), a central brain area primarily connected by gap junctional (electrical) synapses, regulates cortical attention to the sensory surround. Bidirectional plasticity of electrical synapses may be a key mechanism underlying these processes in both healthy and diseased states. Here we show in electrically coupled TRN pairs that tonic spiking in one neuron results in long-term potentiation of electrical synapses between coupled pairs of TRN neurons. Potentiation is expressed asymmetrically, indicating that regulation of connectivity depends on the direction of use. Further, potentiation depends on calcium flux, and we thus propose a calcium-based activity rule for bidirectional plasticity of electrical synapse strength. Because electrical synapses dominate intra-TRN connectivity, these synapses and their modifications are key regulators of thalamic attention circuitry. More broadly, bidirectional modifications of electrical synapses are likely to be a widespread and powerful principle for ongoing, dynamic reorganization of neuronal circuitry across the brain.SummaryLong-term potentiation results from spiking in one cell of an electrically coupled pair. Asymmetry of synapses increases following unidirectional activity. We suggest a calcium-based rule for electrical synapse plasticity.

Asymmetry and modulation of spike timing in electrically coupled neurons

2015 ◽  
Vol 113 (6) ◽  
pp. 1743-1751 ◽  
Author(s):  
Jessica Sevetson ◽  
Julie S. Haas
Keyword(s):  
Critical Role ◽  
Electrical Coupling ◽  
Brain Slices ◽  
Spike Timing ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Electrical Synapses ◽  
Thalamic Relay ◽  
Coupled Networks ◽  
The Brain

Electrical coupling mediates interactions between neurons of the thalamic reticular nucleus (TRN), which play a critical role in regulating thalamocortical and corticothalamic communication by inhibiting thalamic relay cells. Accumulating evidence has shown that asymmetry of electrical synapses is a fundamental and dynamic property, but the effect of asymmetry on coupled networks is unexplored. Recording from patched pairs in rat brain slices, we investigate asymmetry in the subthreshold regime and show that electrical synapses can exert powerful effects on the spike times of coupled neighbors. Electrical synaptic signaling modulates spike timing by 10–20 ms, in an effect that also exhibits asymmetry. Furthermore, we show through modeling that coupling asymmetry expands the set of outputs for pairs of coupled neurons through enhanced regions of synchrony and reversals of spike order. These results highlight the power and specificity of signaling exerted by electrical synapses, which contribute to information flow across the brain.

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.

scholarly journals Functional topographic organization of the motor reticulothalamic pathway

2015 ◽  
Vol 113 (9) ◽  
pp. 3090-3097 ◽  
Author(s):  
Ying-Wan Lam ◽  
S. Murray Sherman
Keyword(s):  
Laser Scanning ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Thalamic Nuclei ◽  
Dorsal Thalamus ◽  
Thalamic Relay ◽  
Thalamocortical Projections ◽  
Motor Information ◽  
Laser Scanning Photostimulation ◽  
Similar Organization

The thalamic reticular nucleus (TRN) is a thin layer of GABAergic cells lying rostral and lateral to the dorsal thalamus, and its projection to thalamic relay cells (i.e., the reticulothalamic pathway) strongly inhibits these cells. In an attempt to extend earlier studies of reticulothalamic connections to sensory thalamic nuclei, we used laser-scanning photostimulation to study the reticulothalamic projections to the main motor thalamic relays, the ventral anterior and lateral (VA and VL) nuclei, as well as to the nearby central lateral (CL) thalamic nucleus. VA/VL and the earlier studied somatosensory thalamic nuclei are considered “core” nuclei with topographic thalamocortical projections, whereas CL is thought to be a “matrix” nucleus with diffuse thalamocortical projections. We found that the TRN input footprints to VA/VL and CL are spatially localized and topographic and generally conform to the patterns established earlier for the TRN projections to sensory thalamic relays. These remarkable similarities suggest similar organization of reticulothalamic pathways and TRN regulation of thalamocortical communication for motor and sensory systems and perhaps also for core and matrix thalamus. Furthermore, we found that VA/VL and CL shared overlapping TRN input regions, suggesting that CL may also be involved in the relay of motor information.

scholarly journals GABABR Modulation of Electrical Synapses and Plasticity in the Thalamic Reticular Nucleus

2021 ◽  
Vol 22 (22) ◽  
pp. 12138
Author(s):  
Huaixing Wang ◽  
Julie S. Haas
Keyword(s):  
Signaling Pathways ◽  
Neuronal Activity ◽  
Gabab Receptor ◽  
Receptor Activation ◽  
Gabab Receptors ◽  
Electrical Synapse ◽  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Electrical Synapses ◽  
The Impact

Two distinct types of neuronal activity result in long-term depression (LTD) of electrical synapses, with overlapping biochemical intracellular signaling pathways that link activity to synaptic strength, in electrically coupled neurons of the thalamic reticular nucleus (TRN). Because components of both signaling pathways can also be modulated by GABAB receptor activity, here we examined the impact of GABAB receptor activation on the two established inductors of LTD in electrical synapses. Recording from patched pairs of coupled rat neurons in vitro, we show that GABAB receptor inactivation itself induces a modest depression of electrical synapses and occludes LTD induction by either paired bursting or metabotropic glutamate receptor (mGluR) activation. GABAB activation also occludes LTD from either paired bursting or mGluR activation. Together, these results indicate that afferent sources of GABA, such as those from the forebrain or substantia nigra to the reticular nucleus, gate the induction of LTD from either neuronal activity or afferent glutamatergic receptor activation. These results add to a growing body of evidence that the regulation of thalamocortical transmission and sensory attention by TRN is modulated and controlled by other brain regions. Significance: We show that electrical synapse plasticity is gated by GABAB receptors in the thalamic reticular nucleus. This effect is a novel way for afferent GABAergic input from the basal ganglia to modulate thalamocortical relay and is a possible mediator of intra-TRN inhibitory effects.

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