scholarly journals A calcium-dependent pathway underlies activity-dependent plasticity of electrical synapses in the thalamic reticular nucleus

2017 ◽  
Vol 595 (13) ◽  
pp. 4417-4430 ◽  
Author(s):  
Jessica Sevetson ◽  
Sarah Fittro ◽  
Emily Heckman ◽  
Julie S. Haas
Keyword(s):  
Thalamic Reticular Nucleus ◽  
Reticular Nucleus ◽  
Electrical Synapses ◽  
Dependent Plasticity ◽  
Calcium Dependent ◽  
Activity Dependent ◽  
Dependent Pathway

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.

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

2020 ◽  
Author(s):  
Brandon Alexander Fricker ◽  
Emily Lauren Heckman ◽  
Patrick C Cunningham ◽  
Huaixing Wang ◽  
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

Activity-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 characterized and understood. For mammalian electrical synapses comprising hexamers of connexin36, physiological forms of neuronal activity in coupled pairs have thus far 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 interconnected by electrical synapses, regulates cortical input from and attention to the sensory surround. Here, we show in electrically coupled TRN pairs that tonic spiking in one neuron results in long-term potentiation of electrical synapses with a magnitude of plasticity that alters the functionality of the synapse. 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 activity-dependent modifications are key dynamic regulators of thalamic attention circuitry. More broadly, we speculate that bidirectional modifications of electrical synapses may be a widespread and powerful principle for ongoing, dynamic reorganization of neuronal circuitry across the brain.

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.

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

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.

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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