Synaptic mechanisms underlying cholinergic control of thalamic reticular nucleus neurons

Journal of Physiology

Volumn 592, Issue 19, 2014, Pages 4137-4145

  Beierlein, Michael ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ATROPINE; CALCIUM CHANNEL; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; MUSCARINIC RECEPTOR; OTENZEPAD; CHOLINERGIC RECEPTOR;

ACETYLCHOLINE RELEASE; ARTICLE; CHOLINERGIC SYNAPSE; ENZYME ACTIVATION; GABAERGIC TRANSMISSION; IN VIVO STUDY; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NEUROTRANSMITTER RELEASE; NONHUMAN; SIGNAL TRANSDUCTION; SPATIOTEMPORAL ANALYSIS; SYNAPTIC TRANSMISSION; THALAMOCORTICAL TRACT; THALAMUS; THALAMUS RETICULAR NUCLEUS; ACTION POTENTIAL; ANIMAL; METABOLISM; NERVE CELL; PHYSIOLOGY; SYNAPSE; THALAMUS NUCLEUS;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; NEURONS; RECEPTORS, CHOLINERGIC; SYNAPSES; SYNAPTIC TRANSMISSION; THALAMIC NUCLEI;

EID: 84908599234     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.277376     Document Type: Article

References (48)

1. Arroyo S, Bennett C, Aziz D, Brown SP & Hestrin S (2012). Prolonged disynaptic inhibition in the cortex mediated by slow, non-α7 nicotinic excitation of a specific subset of cortical interneurons. J Neurosci 32, 3859-3864.
2. Arroyo S, Bennett C & Hestrin S (2014). Nicotinic modulation of cortical circuits. Front Neural Circuits 8, 30.
3. V3.3 calcium channel is the major sleep spindle pacemaker in thalamus. Proc Natl Acad Sci U S A 108, 13823-13828.
4. Bell KA, Shim H, Chen CK & McQuiston AR (2011). Nicotinic excitatory postsynaptic potentials in hippocampal CA1 interneurons are predominantly mediated by nicotinic receptors that contain α4 and β2 subunits. Neuropharmacology 61, 1379-1388.
5. Bennett C, Arroyo S, Berns D & Hestrin S (2012). Mechanisms generating dual-component nicotinic EPSCs in cortical interneurons. J Neurosci 32, 17287-17296.
6. Bista P, Meuth SG, Kanyshkova T, Cerina M, Pawlowski M, Ehling P, Landgraf P, Borsotto M, Heurteaux C, Pape HC, Baukrowitz T & Budde T (2012). Identification of the muscarinic pathway underlying cessation of sleep-related burst activity in rat thalamocortical relay neurons. Pflugers Arch 463, 89-102.
7. Blankenship JE, Wachtel H & Kandel ER (1971). Ionic mechanisms of excitatory, inhibitory, and dual synaptic actions mediated by an identified interneuron in abdominal ganglion of Aplysia. J Neurophysiol 34, 76-92.
8. Boucetta S, Cisse Y, Mainville L, Morales M & Jones BE (2014). Discharge profiles across the sleep-waking cycle of identified cholinergic, GABAergic, and glutamatergic neurons in the pontomesencephalic tegmentum of the rat. J Neurosci 34, 4708-4727.
9. Brombas A, Fletcher LN & Williams SR (2014). Activity-dependent modulation of layer 1 inhibitory neocortical circuits by acetylcholine. J Neurosci 34, 1932-1941.
10. + current amplifies distal dendritic signalling in thalamic reticular neurons. J Neurosci 30, 15419-15429.
11. Curro Dossi R, Pare D & Steriade M (1991). Short-lasting nicotinic and long-lasting muscarinic depolarizing responses of thalamocortical neurons to stimulation of mesopontine cholinergic nuclei. J Neurophysiol 65, 393-406.
12. Deleuze C, David F, Béhuret S, Sadoc G, Shin HS, Uebele VN, Renger JJ, Lambert RC, Leresche N & Bal T (2012). T-type calcium channels consolidate tonic action potential output of thalamic neurons to neocortex. J Neurosci 32, 12228-12236.
13. Descarries L, Gisiger V & Steriade M (1997). Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53, 603-625.
14. d'Incamps BL & Ascher P (2014). High affinity and low affinity heteromeric nicotinic acetylcholine receptors at central synapses. J Physiol (in press; DOI: 10.1113/jphysiol.2014.273128).
15. + channels: giving a boost to thalamic reticular neurons. J Neurosci 31, 5551-5553.
16. Glowatzki E & Fuchs PA (2000). Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea. Science 288, 2366-2368.
17. Gu Z & Yakel JL (2011). Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 71, 155-165.
18. Gulledge AT, Bucci DJ, Zhang SS, Matsui M & Yeh HH (2009). M1 receptors mediate cholinergic modulation of excitability in neocortical pyramidal neurons. J Neurosci 29, 9888-9902.
19. Gulledge AT & Stuart GJ (2005). Cholinergic inhibition of neocortical pyramidal neurons. J Neurosci 25, 10308-10320.
20. Hallanger AE, Levey AI, Lee HJ, Rye DB & Wainer BH (1987). The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262, 105-124.
21. Hallanger AE & Wainer BH (1988). Ultrastructure of ChAT-immunoreactive synaptic terminals in the thalamic reticular nucleus of the rat. J Comp Neurol 278, 486-497.
22. Han Y, Shi YF, Xi W, Zhou R, Tan ZB, Wang H, Li XM, Chen Z, Feng G, Luo M, Huang ZL, Duan S & Yu YQ (2014). Selective activation of cholinergic basal forebrain neurons induces immediate sleep-wake transitions. Curr Biol 24, 693-698.
23. Harris KD & Thiele A (2011). Cortical state and attention. Nat Rev Neurosci 12, 509-523.
24. Hassani OK, Lee MG, Henny P & Jones BE (2009). Discharge profiles of identified GABAergic in comparison to cholinergic and putative glutamatergic basal forebrain neurons across the sleep-wake cycle. J Neurosci 29, 11828-11840.
25. Hirata A, Aguilar J & Castro-Alamancos MA (2006). Noradrenergic activation amplifies bottom-up and top-down signal-to-noise ratios in sensory thalamus. J Neurosci 26, 4426-4436.
26. Hu B, Steriade M & Deschenes M (1989a). The effects of brainstem peribrachial stimulation on neurons of the lateral geniculate nucleus. Neuroscience 31, 13-24.
27. Hu B, Steriade M & Deschenes M (1989b). The effects of brainstem peribrachial stimulation on perigeniculate neurons: the blockage of spindle waves. Neuroscience 31, 1-12.
28. Jones EG (2007). The Thalamus. Cambridge University Press, Cambridge, New York.
29. Kawai H, Lazar R & Metherate R (2007). Nicotinic control of axon excitability regulates thalamocortical transmission. Nat Neurosci 10, 1168-1175.
30. Lee KH & McCormick DA (1995). Acetylcholine excites GABAergic neurons of the ferret perigeniculate nucleus through nicotinic receptors. J Neurophysiol 73, 2123-2128.
31. Lee MG, Hassani OK, Alonso A & Jones BE (2005). Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J Neurosci 25, 4365-4369.
32. Lee SH & Dan Y (2012). Neuromodulation of brain states. Neuron 76, 209-222.
33. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J, Herry C & Luthi A (2011). A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480, 331-335.
34. Lüthi A (2013). Sleep spindles: where they come from, what they do. Neuroscientist 20, 243-256.
35. Ma M & Luo M (2012). Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb. J Neurosci 32, 10105-10116.
36. McCormick DA & Bal T (1997). Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci 20, 185-215.
37. Muñoz W & Rudy B (2014). Spatiotemporal specificity in cholinergic control of neocortical function. Curr Opin Neurobiol 26C, 149-160.
38. Parent M & Descarries L (2008). Acetylcholine innervation of the adult rat thalamus: distribution and ultrastructural features in dorsolateral geniculate, parafascicular, and reticular thalamic nuclei. J Comp Neurol 511, 678-691.
39. Parikh V, Kozak R, Martinez V & Sarter M (2007). Prefrontal acetylcholine release controls cue detection on multiple timescales. Neuron 56, 141-154.
40. Pinault D (2004). The thalamic reticular nucleus: structure, function and concept. Brain Res Brain Res Rev 46, 1-31.
41. Pinault D & Deschênes M (1992). Muscarinic inhibition of reticular thalamic cells by basal forebrain neurones. Neuroreport 3, 1101-1104.
42. Pinto L, Goard MJ, Estandian D, Xu M, Kwan AC, Lee SH, Harrison TC, Feng G & Dan Y (2013). Fast modulation of visual perception by basal forebrain cholinergic neurons. Nat Neurosci 16, 1857-1863.
43. Steriade M (2004). Acetylcholine systems and rhythmic activities during the waking-sleep cycle. Prog Brain Res 145, 179-196.
44. Sun YG, Pita-Almenar JD, Wu CS, Renger JJ, Uebele VN, Lu HC & Beierlein M (2013). Biphasic cholinergic synaptic transmission controls action potential activity in thalamic reticular nucleus neurons. J Neurosci 33, 2048-2059.
45. Sun YG, Wu CS, Lu HC & Beierlein M (2011). Target-dependent control of synaptic inhibition by endocannabinoids in the thalamus. J Neurosci 31, 9222-9230.
46. Vogt KE & Regehr WG (2001). Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci 21, 75-83.
47. Yarosh CA, Acosta CG & Ashe JH (1988). Modification of nicotinic ganglionic transmission by muscarinic slow postsynaptic potentials in the in vitro rabbit superior cervical ganglion. Synapse 2, 174-182.
48. Zhu JJ & Uhlrich DJ (1997). Nicotinic receptor-mediated responses in relay cells and interneurons in the rat lateral geniculate nucleus. Neuroscience 80, 191-202.