Strychnine-sensitive glycine receptors on pyramidal neurons in layers II/III of the mouse prefrontal cortex are tonically activated

Journal of Neurophysiology

Volumn 112, Issue 5, 2014, Pages 1169-1178

  Salling, Michael C ^a   Harrison, Neil L ^a,b  

^a NewYork Presbyterian Hospital   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

GABA; Glycine; Prefrontal cortex; Tonic current

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; AMINO ACID RECEPTOR AFFECTING AGENT; GLYCINE RECEPTOR; STRYCHNINE;

ANIMAL; C57BL MOUSE; DRUG EFFECTS; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MOUSE; NERVE CELL INHIBITION; PHYSIOLOGY; PREFRONTAL CORTEX; PYRAMIDAL NERVE CELL;

ANIMALS; GABA AGONISTS; GLYCINE AGENTS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RECEPTORS, GABA-A; RECEPTORS, GLYCINE; STRYCHNINE;

EID: 84906897925     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00714.2013     Document Type: Article

References (62)

1. Abernathy K, Chandler LJ, Woodward JJ. Alcohol and the prefrontal cortex. Int Rev Neurobiol 91: 289-320, 2010.
2. Amatrudo JM, Weaver CM, Crimins JL, Hof PR, Rosene DL, Luebke JI. Influence of highly distinctive structural properties on the excitability of pyramidal neurons in monkey visual and prefrontal cortices. J Neurosci 32: 13644-13660, 2012.
3. Badanich KA, Mulholland PJ, Beckley JT, Trantham-Davidson H, Woodward JJ. Ethanol reduces neuronal excitability of lateral orbitofrontal cortex neurons via a glycine receptor dependent mechanism. Neuropsychopharma-cology 38: 1176-1188, 2013.
4. Bai D, Zhu G, Pennefather P, Jackson MF, MacDonald JF, Orser BA. Distinct functional and pharmacological properties of tonic and quantal inhibitory postsynaptic currents mediated by gamma-aminobutyric acidA receptors in hippocampal neurons. Mol Pharmacol 59: 814-824, 2001.
5. Belelli D, Harrison NL, Maguire J, Macdonald RL, Walker MC, Cope DW. Extrasynaptic GABAA receptors: form, pharmacology, and function. J Neurosci 29: 12757-12763, 2009.
6. Bosman LW, Rosahl TW, Brussaard AB. Neonatal development of the rat visual cortex: synaptic function of GABAA receptor alpha subunits. J Physiol 545: 169-181, 2002.
7. Brickley SG, Cull-Candy SG, Farrant M. Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J Physiol 497: 753-759, 1996.
8. Chattipakorn SC, McMahon LL. Pharmacological characterization of gly-cine-gated chloride currents recorded in rat hippocampal slices. J Neuro-physiol 87: 1515-1525, 2002.
9. Chattipakorn SC, McMahon LL. Strychnine-sensitive glycine receptors depress hyperexcitability in rat dentate gyrus. J Neurophysiol 89: 1339-1342, 2003.
10. Chudasama Y, Robbins TW. Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans. Biol Psychol 73: 19-38, 2006.
11. Cope DW, Hughes SW, Crunelli V. GABAA receptor-mediated tonic inhibition in thalamic neurons. J Neurosci 25: 11553-11563, 2005.
12. Dahchour A, Hoffman A, Deitrich R, de Witte P. Effects of ethanol on extracellular amino acid levels in high-and low-alcohol sensitive rats: a microdialysis study. Alcohol 35: 548-553, 2000.
13. Day M, Carr DB, Ulrich S, Ilijic E, Tkatch T, Surmeier DJ. Dendritic excitability of mouse frontal cortex pyramidal neurons is shaped by the interaction among HCN, Kir2, and Kleak channels. J Neurosci 25: 8776-8787, 2005.
14. DeFelipe J, Lopez-Cruz PL, Benavides-Piccione R, Bielza C, Larranaga P, Anderson S, Burkhalter A, Cauli B, Fairen A, Feldmeyer D, Fishell G, Fitzpatrick D, Freund TF, Gonzalez-Burgos G, Hestrin S, Hill S, Hof PR, Huang J, Jones EG, Kawaguchi Y, Kisvarday Z, Kubota Y, Lewis DA, Marin O, Markram H, McBain CJ, Meyer HS, Monyer H, Nelson SB, Rockland K, Rossier J, Rubenstein JL, Rudy B, Scanziani M, Shepherd GM, Sherwood CC, Staiger JF, Tamas G, Thomson A, Wang Y, Yuste R, Ascoli GA. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 14: 202-216, 2013.
15. Drasbek KR, Jensen K. THIP, a hypnotic and antinociceptive drug, enhances an extrasynaptic GABAA receptor-mediated conductance in mouse neocor-tex. Cereb Cortex 16: 1134-1141, 2006.
16. Elliott R, Baker SC, Rogers RD, O'Leary DA, Paykel ES, Frith CD, Dolan RJ, Sahakian BJ. Prefrontal dysfunction in depressed patients performing a complex planning task: a study using positron emission tomography. Psychol Med 27: 931-942, 1997.
17. Farrant M, Nusser Z. Variations on an inhibitory theme: phasic and tonic activation of GABAA receptors. Nat Rev Neurosci 6: 215-229, 2005.
18. Fino E, Packer AM, Yuste R. The logic of inhibitory connectivity in the neocortex. Neuroscientist 19: 228-237, 2013.
19. Flint AC, Liu X, Kriegstein AR. Nonsynaptic glycine receptor activation during early neocortical development. Neuron 20: 43-53, 1998.
20. Franklin KB, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 1997.
21. Franklin KB, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 2008.
22. Fritschy JM, Mohler H. GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359: 154-194, 1995.
23. Goldstein RZ, Volkow ND. Dysfunction of the prefrontal cortex in addiction: neuroimaging findings and clinical implications. Nat Rev Neurosci 12: 652-669, 2011.
24. Harsing LG Jr, Matyus P. Mechanisms of glycine release, which build up synaptic and extrasynaptic glycine levels: the role of synaptic and non-synaptic glycine transporters. Brain Res Bull 93: 110-119, 2013.
25. Hedrick T, Waters J. Effect of temperature on spiking patterns of neocortical layer 2/3 and layer 6 pyramidal neurons. Front Neural Circuits 6: 28, 2012.
26. Hoestgaard-Jensen K, Dalby NO, Wolinsky TD, Murphey C, Jones KA, Rottlander M, Frederiksen K, Watson WP, Jensen K, Ebert B. Pharmacological characterization of a novel positive modulator at alpha4beta3delta-containing extrasynaptic GABAA receptors. Neuro-pharmacology 58: 702-711, 2010.
27. Horio M, Kohno M, Fujita Y, Ishima T, Inoue R, Mori H, Hashimoto K. Levels of D-serine in the brain and peripheral organs of serine racemase (Srr) knock-out mice. Neurochem Int 59: 853-859, 2011.
28. Jia F, Chandra D, Homanics GE, Harrison NL. Ethanol modulates synaptic and extrasynaptic GABAA receptors in the thalamus. J Pharmacol Exp Ther 326: 475-482, 2008.
29. Jia F, Goldstein PA, Harrison NL. The modulation of synaptic GABAA receptors in the thalamus by eszopiclone and zolpidem. J Pharmacol Exp Ther 328: 1000-1006, 2009.
30. Jia F, Pignataro L, Schofield CM, Yue M, Harrison NL, Goldstein PA. An extrasynaptic GABAA receptor mediates tonic inhibition in thalamic VB neurons. J Neurophysiol 94: 4491-4501, 2005.
31. Jonsson S, Kerekes N, Hyytia P, Ericson M, Soderpalm B. Glycine receptor expression in the forebrain of male AA/ANA rats. Brain Res 1305: S27-S36, 2009.
32. Kawaguchi Y. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J Neurophysiol 69: 416-431, 1993.
33. Kirsch J. Glycinergic transmission. Cell Tissue Res 326: 535-540, 2006.
34. Krettek JE, Price JL. The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171: 157-191, 1977.
35. Kunz PA, Burette AC, Weinberg RJ, Philpot BD. Glycine receptors support excitatory neurotransmitter release in developing mouse visual cortex. J Physiol 590: 5749-5764, 2012.
36. Lu Y, Ye JH. Glycine-activated chloride currents of neurons freshly isolated from the prefrontal cortex of young rats. Brain Res 1393: 17-22, 2011.
37. Malosio ML, Marqueze-Pouey B, Kuhse J, Betz H. Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J 10: 2401-2409, 1991.
38. Mori M, Gahwiler BH, Gerber U. Beta-alanine and taurine as endogenous agonists at glycine receptors in rat hippocampus in vitro. J Physiol 539: 191-200, 2002.
39. Murakami T, Furuse M. The impact of taurine- and beta-alanine-supple-mented diets on behavioral and neurochemical parameters in mice: antide-pressant versus anxiolytic-like effects. Amino Acids 39: 427-434, 2010.
40. Nusser Z, Mody I. Selective modulation of tonic and phasic inhibitions in dentate gyrus granule cells. J Neurophysiol 87: 2624-2628, 2002.
41. Olah S, Fule M, Komlosi G, Varga C, Baldi R, Barzo P, Tamas G. Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461: 1278-1281, 2009. Ongur D, Price JL. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10: 206-219, 2000.
42. Peng Z, Hauer B, Mihalek RM, Homanics GE, Sieghart W, Olsen RW, Houser CR. GABAA receptor changes in delta subunit-deficient mice: altered expression of alpha4 and gamma2 subunits in the forebrain. J Comp Neurol 446: 179-197, 2002.
43. Petersen CC, Crochet S. Synaptic computation and sensory processing in neocortical layer 2/3. Neuron 78: 28-48, 2013.
44. Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G. GABAA receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101: 815-850, 2000.
45. Pribilla I, Takagi T, Langosch D, Bormann J, Betz H. The atypical M2 segment of the beta subunit confers picrotoxinin resistance to inhibitory glycine receptor channels. EMBO J 11: 4305-4311, 1992.
46. Rao SG, Williams GV, Goldman-Rakic PS. Destruction and creation of spatial tuning by disinhibition: GABAA blockade of prefrontal cortical neurons engaged by working memory. J Neurosci 20: 485-494, 2000.
47. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71: 45-61, 2011.
48. Salin P, Tseng GF, Hoffman S, Parada I, Prince DA. Axonal sprouting in layer V pyramidal neurons of chronically injured cerebral cortex. J Neurosci 15: 8234-8245, 1995.
49. Saxena NC, Macdonald RL. Assembly of GABAA receptor subunits: role of the delta subunit. J Neurosci 14: 7077-7086, 1994.
50. Seamans JK, Lapish CC, Durstewitz D. Comparing the prefrontal cortex of rats and primates: insights from electrophysiology. Neurotox Res 14: 249-262, 2008.
51. Semyanov A, Walker MC, Kullmann DM. GABA uptake regulates cortical excitability via cell type-specific tonic inhibition. Nat Neurosci 6: 484-490, 2003.
52. Thuault SJ, Malleret G, Constantinople CM, Nicholls R, Chen I, Zhu J, Panteleyev A, Vronskaya S, Nolan MF, Bruno R, Siegelbaum SA, Kandel ER. Prefrontal cortex HCN1 channels enable intrinsic persistent neural firing and executive memory function. J Neurosci 33: 13583-13599, 2013.
53. Uylings HB, Groenewegen HJ, Kolb B. Do rats have a prefrontal cortex? Behav Brain Res 146: 3-17, 2003.
54. Vandenberg RJ, Aubrey KR. Glycine transport inhibitors as potential anti-psychotic drugs. Expert Opin Ther Targets 5: 507-518, 2001.
55. Vardya I, Drasbek KR, Dosa Z, Jensen K. Cell type-specific GABAA receptor-mediated tonic inhibition in mouse neocortex. J Neurophysiol 100: 526-532, 2008.
56. Vicini S, Ferguson C, Prybylowski K, Kralic J, Morrow AL, Homanics GE. GABAA receptor alpha1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J Neurosci 21: 3009-3016, 2001.
57. Weinberger DR, Berman KF, Zec RF. Physiologic dysfunction of dorsolat-eral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. Arch Gen Psychiatry 43: 114-124, 1986.
58. Weitlauf C, Woodward JJ. Ethanol selectively attenuates NMDAR-mediated synaptic transmission in the prefrontal cortex. Alcohol Clin Exp Res 32: 690-698, 2008.
59. Yamada J, Furukawa T, Ueno S, Yamamoto S, Fukuda A. Molecular basis for the GABAA receptor-mediated tonic inhibition in rat somatosensory cortex. Cereb Cortex 17: 1782-1787, 2007.
60. Yoon JH, Minzenberg MJ, Ursu S, Ryan Walter BS, Wendelken C, Ragland JD, Carter CS. Association of dorsolateral prefrontal cortex dysfunction with disrupted coordinated brain activity in schizophrenia: relationship with impaired cognition, behavioral disorganization, and global function. Am J Psychiatry 165: 1006-1014, 2008.
61. Zhang LH, Gong N, Fei D, Xu L, Xu TL. Glycine uptake regulates hippocampal network activity via glycine receptor-mediated tonic inhibition. Neuropsychopharmacology 33: 701-711, 2008a.
62. Zhang XB, Sun GC, Liu LY, Yu F, Xu TL. Alpha2 subunit specificity of cyclothiazide inhibition on glycine receptors. Mol Pharmacol 73: 1195-1202, 2008b.