Activity-dependent modulation of layer 1 inhibitory neocortical circuits by acetylcholine

Journal of Neuroscience

Volumn 34, Issue 5, 2014, Pages 1932-1941

  Brombas, Arne ^a   Fletcher, Lee N ^a   Williams, Stephen R ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Axon; Dendrite; Ion channel; Neocortex; Synaptic integration

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; ACETYLCHOLINE; CALCIUM ACTIVATED POTASSIUM CHANNEL; MECAMYLAMINE; MUSCARINIC RECEPTOR; TELENZEPINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; INTERNEURON; IONTOPHORESIS; MALE; MEMBRANE STEADY POTENTIAL; NEOCORTEX; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SOMATOSENSORY CORTEX; SPIKE; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP;

AXON; DENDRITE; ION-CHANNEL; NEOCORTEX; SYNAPTIC INTEGRATION;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; CALCIUM; CHOLINERGIC AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; EGTAZIC ACID; INTERNEURONS; IONTOPHORESIS; MALE; NEOCORTEX; NERVE NET; NEURAL INHIBITION; NEURAL PATHWAYS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; TIME FACTORS;

EID: 84893098620     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4470-13.2014     Document Type: Article

References (57)

1. + channels: form and function. Annu Rev Physiol 74: 245-269. CrossRef Medline
2. Adler EM, Augustine GJ, Duffy SN, Charlton MP (1991) Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J Neurosci 11: 1496-1507. Medline
3. 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. CrossRef Medline
4. Bartus RT, Dean RL 3rd, Beer B, Lippa AS (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217: 408-414. CrossRef Medline
5. Bennett C, Arroyo S, Berns D, Hestrin S (2012) Mechanisms generating dual-component nicotinic EPSCs in cortical interneurons. J Neurosci 32: 17287-17296. CrossRef Medline
6. Berridge MJ (2002) The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32: 235-249. CrossRef Medline
7. Buchanan KA, Petrovic MM, Chamberlain SE, Marrion NV, Mellor JR (2010) Facilitation of long-term potentiation by muscarinic M (1) receptors is mediated by inhibition of SK channels. Neuron 68: 948-963. CrossRef Medline
8. Buzsaki G, Bickford RG, Ponomareff G, Thal LJ, Mandel R, Gage FH (1988) Nucleus basalis and thalamic control of neocortical activity in the freely moving rat. J Neurosci 8: 4007-4026. Medline
9. Caulfield MP, Birdsall NJ (1998) International union of pharmacology: XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50: 279-290. Medline
10. Cauller LJ, Clancy B, Connors BW (1998) Backward cortical projections to primary somatosensory cortex in rats extend long horizontal axons in layer I. J Comp Neurol 390: 297-310. CrossRef Medline
11. Christophe E, Roebuck A, Staiger JF, Lavery DJ, Charpak S, Audinat E (2002) Two types of nicotinic receptors mediate an excitation of neocortical layer I interneurons. J Neurophysiol 88: 1318-1327. Medline
12. Chu Z, Galarreta M, Hestrin S (2003) Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci 23: 96-102. Medline
13. Contestabile A (2011) The history of the cholinergic hypothesis. Behav Brain Res 221: 334-340. CrossRef Medline
14. Coyle JT, Price DL, DeLong MR (1983) Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219: 1184-1190. CrossRef Medline
15. Cruikshank SJ, Ahmed OJ, Stevens TR, Patrick SL, Gonzalez AN, Elmaleh M, Connors BW (2012) Thalamic control of layer 1 circuits in prefrontal cortex. J Neurosci 32: 17813-17823. CrossRef Medline
16. Détári L, Rasmusson DD, Semba K (1999) The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex. Prog Neurobiol 58: 249-277. CrossRef Medline
17. Fiorillo CD, Williams JT (2000) Cholinergic inhibition of ventral midbrain dopamine neurons. J Neurosci 20: 7855-7860. Medline
18. Giessel AJ, Sabatini BL (2010) M1 muscarinic receptors boost synaptic potentials and calcium influx in dendritic spines by inhibiting postsynaptic SK channels. Neuron 68: 936-947. CrossRef Medline
19. Giovannini MG, Rakovska A, Benton RS, Pazzagli M, Bianchi L, Pepeu G (2001) Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 106: 43-53. CrossRef Medline
20. Goard M, Dan Y (2009) Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12: 1444-1449. CrossRef Medline
21. Gulledge AT, Stuart GJ (2005) Cholinergic inhibition of neocortical pyramidal neurons. J Neurosci 25: 10308-10320. CrossRef Medline
22. 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. CrossRef Medline
23. Harnett MT, Xu NL, Magee JC, Williams SR (2013) Potassium channels control the interaction between active dendritic integration compartments in layer 5 cortical pyramidal neurons. Neuron 79: 516-529. CrossRef Medline
24. Jiang X, Wang G, Lee AJ, Stornetta RL, Zhu JJ (2013) The organization of two new cortical interneuronal circuits. Nat Neurosci 16: 210-218. CrossRef Medline
25. Kalmbach A, Hedrick T, Waters J (2012) Selective optogenetic stimulation of cholinergic axons in neocortex. J Neurophysiol 107: 2008-2019. CrossRef Medline
26. Kawaguchi Y (1997) Selective cholinergic modulation of cortical GABAergic cell subtypes. J Neurophysiol 78: 1743-1747. Medline
27. Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279: 1714-1718. CrossRef Medline
28. Kim HG, Connors BW (1993) Apical dendrites of the neocortex: correlation between sodium-and calcium-dependent spiking and pyramidal cell morphology. J Neurosci 13: 5301-5311. Medline
29. Köhler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J, Adelman JP (1996) Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273: 1709-1714. CrossRef Medline
30. Larkum M (2013) A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex. Trends Neurosci 36: 141-151. CrossRef Medline
31. Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398: 338-341. CrossRef Medline
32. Larkum ME, Waters J, Sakmann B, Helmchen F (2007) Dendritic spikes in apical dendrites of neocortical layer 2/3 pyramidal neurons. J Neurosci 27: 8999-9008. CrossRef Medline
33. Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B (2013) A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat Neurosci 16: 1662-1670. CrossRef Medline
34. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J, Herry C, Lüthi A (2011) A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 480: 331-335. CrossRef Medline
35. Mao T, Kusefoglu D, Hooks BM, Huber D, Petreanu L, Svoboda K (2011) Long-range neuronal circuits underlying the interaction between sensory and motor cortex. Neuron 72: 111-123. CrossRef Medline
36. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807. CrossRef Medline
37. McCormick DA, Prince DA (1986) Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol 375: 169-194. Medline
38. Mechawar N, Cozzari C, Descarries L (2000) Cholinergic innervation in adult rat cerebral cortex: a quantitative immunocytochemical description. J Comp Neurol 428: 305-318. CrossRef Medline
39. Metherate R, Cox CL, Ashe JH (1992) Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci 12: 4701-4711. Medline
40. Murayama M, Larkum ME (2009) Enhanced dendritic activity in awake rats. Proc Natl Acad Sci U S A 106: 20482-20486. CrossRef Medline
41. Murayama M, Pérez-Garci E, Nevian T, Bock T, Senn W, Larkum ME (2009) Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457: 1137-1141. CrossRef Medline
42. Oláh S, Füle M, Komlósi G, Varga C, Báldi R, Barzó P, Tamás G (2009) Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461: 1278-1281. CrossRef Medline
43. Palmer LM, Schulz JM, Murphy SC, Ledergerber D, Murayama M, Larkum ME (2012) The cellular basis of GABA (B)-mediated interhemispheric inhibition. Science 335: 989-993. CrossRef Medline
44. 2+ spikes in layer 5 somatosensory pyramidal neurons. Neuron 50: 603-616. CrossRef Medline
45. B receptors in cortical pyramidal neurons is mediated by a direct Gi/o-β-subunit interaction with Cav1 channels. J Physiol 591: 1599-1612. CrossRef Medline
46. Pi HJ, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A (2013) Cortical interneurons that specialize in disinhibitory control. Nature 503: 521-524. CrossRef Medline
47. Porter JT, Cauli B, Tsuzuki K, Lambolez B, Rossier J, Audinat E (1999) Selective excitation of subtypes of neocortical interneurons by nicotinic receptors. J Neurosci 19: 5228-5235. Medline
48. Prieto JJ, Peterson BA, Winer JA (1994) Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI). J Comp Neurol 344: 349-382. CrossRef Medline
49. Silberberg G, Markram H (2007) Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53: 735-746. CrossRef Medline
50. 2+ signaling in mouse cortical neurons studied by two-photon imaging and photoreleased inositol triphosphate. J Neurosci 23: 758-765. Medline
51. Tamás G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299: 1902-1905. CrossRef Medline
52. (2+)-ATPases. Trends Pharmacol Sci 19: 131-135. CrossRef Medline
53. Williams SR, Stuart GJ (2002) Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295: 1907-1910. CrossRef Medline
54. Winer JA, Larue DT (1989) Populations of GABAergic neurons and axons in layer I of rat auditory cortex. Neuroscience 33: 499-515. CrossRef Medline
55. Wozny C, Williams SR (2011) Specificity of synaptic connectivity between layer 1 inhibitory interneurons and layer 2/3 pyramidal neurons in the rat neocortex. Cereb Cortex 21: 1818-1826. CrossRef Medline
56. Xiang Z, Huguenard JR, Prince DA (1998) Cholinergic switching within neocortical inhibitory networks. Science 281: 985-988. CrossRef Medline
57. Xu NL, Harnett MT, Williams SR, Huber D, O'Connor DH, Svoboda K, Magee JC (2012) Nonlinear dendritic integration of sensory and motor pathways produces an object localization signal. Nature 492: 247-251. CrossRef Medline