GABA-A receptor inhibition of local calcium signaling in spines and dendrites

Journal of Neuroscience

Volumn 34, Issue 48, 2014, Pages 15898-15911

  Marlin, Joseph J ^a   Carter, Adam G ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

Calcium signaling; Dendrite; Inhibition; Interneuron; Prefrontal cortex; Spine

Indexed keywords

3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL) PYRIDAZINIUM BROMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOPYRIDINE; PARVALBUMIN; RHODOPSIN; SEROTONIN 3A RECEPTOR; SOMATOSTATIN; TETRODOTOXIN; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CURRENT CLAMP TECHNIQUE; DENDRITE; FEMALE; FLUORESCENCE MICROSCOPY; HISTOLOGY; INTERNEURON; MALE; MEMBRANE STEADY POTENTIAL; MOUSE; NERVE CELL INHIBITION; NONHUMAN; OPTOGENETICS; PYRAMIDAL NERVE CELL; SPINE; WHOLE CELL PATCH CLAMP; ANIMAL; C57BL MOUSE; DENDRITIC SPINE; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CALCIUM SIGNALING; DENDRITES; DENDRITIC SPINES; FEMALE; MALE; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; RECEPTORS, GABA-A;

EID: 84911885407     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0869-13.2014     Document Type: Article

References (68)

1. Adesnik H, Bruns W, Taniguchi H, Huang ZJ, Scanziani M (2012) A neural circuit for spatial summation in visual cortex. Nature 490:226–231.
2. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsáki G, Cauli B, Defelipe J, Fairé n A, Feld-meyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, et al. (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat RevNeurosci 9:557–568.
3. Bloodgood BL, Sabatini BL (2007) Ca(2 +) signaling in dendritic spines. Curr Opin Neurobiol 17:345–351.
4. Brombas A, Fletcher LN, Williams SR (2014) Activity-dependent modulation of layer 1 inhibitory neocortical circuits by acetylcholine. J Neurosci 34:1932–1941.
5. Chalifoux JR, Carter AG (2010) GABAB receptors modulate NMDA receptor calcium signals in dendritic spines. Neuron 66:101–113.
6. Chalifoux JR, Carter AG (2011a) GABAB receptor modulation of voltage-sensitive calcium channels in spines and dendrites. J Neurosci 31:4221-4232.
7. Chalifoux JR, Carter AG (2011b) Glutamate spillover promotes the generation of NMDA spikes. J Neurosci 31:16435–16446.
8. Chiu CQ, Lur G, Morse TM, Carnevale NT, Ellis-Davies GC, Higley MJ (2013) Compartmentalization of GABAergic inhibition by dendritic spines. Science 340:759–762.
9. Couey JJ, Meredith RM, Spijker S, Poorthuis RB, Smit AB, Brussaard AB, Mansvelder HD (2007) Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54:73–87.
10. Courtin J, Chaudun F, Rozeske RR, Karalis N, Gonzalez-Campo C, Wurtz H, Abdi A, Baufreton J, Bienvenu TC, Herry C (2014) Prefrontal parvalbu-min interneurons shape neuronal activity to drive fear expression. Nature 505:92–96.
11. DeFelipe J, Lopez-Cruz PL, Benavides-Piccione R, Bielza C, Larrañaga 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, et al. (2013) New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat RevNeurosci 14:202–216.
12. Di Cristo G, Wu C, Chattopadhyaya B, Ango F, Knott G, Welker E, Svoboda K, Huang ZJ (2004) Subcellular domain-restricted GABAergic innervation in primary visual cortex in the absence of sensory and thalamic inputs. Nat Neurosci 7:1184–1186.
13. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56:33–42.
14. Fritschy JM, Mohler H (1995) GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154–194.
15. Gentet LJ, Kremer Y, Taniguchi H, Huang ZJ, Staiger JF, Petersen CC (2012) Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci 15:607–612.
16. Gidon A, Segev I (2012) Principles governing the operation of synaptic inhibition in dendrites. Neuron 75:330–341.
17. Gong S, Doughty M, Harbaugh CR, Cummins A, Hatten ME, Heintz N, Gerfen CR (2007) Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci 27: 9817–9823.
18. Hao J, Wang XD, Dan Y, Poo MM, Zhang XH (2009) An arithmetic rule for spatial summation of excitatory and inhibitory inputs in pyramidal neurons. Proc Natl Acad Sci USA 106:21906–21911.
19. Hayama T, Noguchi J, Watanabe S, Takahashi N, Hayashi-Takagi A, Ellis-Davies GC, Matsuzaki M, Kasai H (2013) GABA promotes the competitive selection of dendritic spines by controlling local Ca2 + signaling. Nat Neurosci 16:1409–1416.
20. Hippenmeyer S, Vrieseling E, Sigrist M, Portmann T, Laengle C, Ladle DR, Arber S (2005) A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol 3:e159.
21. Isaacson JS, Scanziani M (2011) How inhibition shapes cortical activity. Neuron 72:231–243.
22. Jadi M, Polsky A, Schiller J, Mel BW (2012) Location-dependent effects of inhibition on local spiking in pyramidal neuron dendrites. PLoS Comput Biol 8, e1002550.
23. Kanemoto Y, Matsuzaki M, Morita S, Hayama T, Noguchi J, Senda N, Mo-motake A, Arai T, Kasai H (2011) Spatial distributions of GABA receptors and local inhibition of Ca2 + transients studied with GABA uncaging in the dendrites of CA1 pyramidal neurons. PLoS One 6:e22652.
24. Kawaguchi Y (1993) Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristicsin rat frontal cortex. J Neurophysiol 69:416–431.
25. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476–486.
26. Kerlin AM, Andermann ML, Berezovskii VK, Reid RC (2010) Broadly tuned response propertiesofdiverse inhibitory neuron subtypesinmouse visual cortex. Neuron 67:858–871.
27. Kim HG, Beierlein M, Connors BW (1995) Inhibitory control of excitable dendrites in neocortex. J Neurophysiol 74:1810–1814.
28. Koch C, Poggio T, Torre V (1983) Nonlinear interactions inadendritic tree: localization, timing, and role in information processing. Proc Natl Acad Sci U S A 80:2799–2802.
29. Kubota Y, Hatada S, Kondo S, Karube F, Kawaguchi Y (2007) Neocortical inhibitory terminals innervate dendritic spines targeted by thalamocorti-cal afferents. J Neurosci 27:1139–1150.
30. Kuhlman SJ, Olivas ND, Tring E, Ikrar T, Xu X, Trachtenberg JT (2013) A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 501:543–546.
31. Kvitsiani D, Ranade S, Hangya B, Taniguchi H, Huang JZ, Kepecs A (2013) Distinct behavioural and network correlates of two interneuron types in prefrontal cortex. Nature 498:363–366.
32. Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338–341.
33. Lee SH, Kwan AC, Zhang S, Phoumthipphavong V, Flannery JG, Masmanidis SC, Taniguchi H, Huang ZJ, Zhang F, Boyden ES, Deisseroth K, Dan Y (2012) Activation of specific interneurons improves V1 feature selectivity and visual perception. Nature 488:379–383.
34. Lee S, Kruglikov I, Huang ZJ, Fishell G, Rudy B (2013) A disinhibitory circuit mediates motor integration in the somatosensory cortex. Nat Neu-rosci 16:1662–1670.
35. 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.
36. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312–324.
37. Little JP, Carter AG (2012) Subcellular synaptic connectivity of layer 2 pyramidal neurons in the medial prefrontal cortex. J Neurosci 32:12808–12819.
38. Liu G (2004) Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat Neurosci 7:373–379.
39. Llinás R, Nicholson C, Freeman JA, Hillman DE (1968) Dendritic spikes and their inhibition in alligator Purkinje cells. Science 160:1132–1135.
40. Lovett-Barron M, Turi GF, Kaifosh P, Lee PH, Bolze F, Sun XH, Nicoud JF, Zemelman BV, Sternson SM, Losonczy A (2012) Regulationofneuronal input transformations by tunable dendritic inhibition. Nat Neurosci 15: 423–430, S1–3.
41. MacAskill AF, Little JP, Cassel JM, Carter AG (2012) Subcellular connectivity underlies pathway-specific signaling in the nucleus accumbens. Nat Neurosci 15:1624–1626.
42. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neu-rosci 5:793–807.
43. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815–823.
44. Müller C, Beck H, Coulter D, Remy S (2012) Inhibitory controloflinear and supralinear dendritic excitation in CA1 pyramidal neurons. Neuron 75: 851–864.
45. Murayama M, Pérez-Garci E, Nevian T, Bock T, Senn W, Larkum ME (2009) Dendritic encoding of sensory stimuli controlled by deep cortical in-terneurons. Nature 457:1137–1141.
46. 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.
47. Palmer L, Murayama M, Larkum M (2012a) Inhibitory regulation of dendritic activity in vivo. Front Neural Circuits 6:26.
48. Palmer LM, Schulz JM, Murphy SC, Ledergerber D, Murayama M, Larkum ME (2012b) The cellular basis of GABA(B)-mediated interhemispheric inhibition. Science 335:989–993.
49. Perez-Garci E, Gassmann M, Bettler B, Larkum ME (2006) TheGABAB1bisoform mediates long-lasting inhibition of dendritic Ca2+ spikes in layer 5 somatosensory pyramidal neurons. Neuron 50:603–616.
50. Petreanu L, Mao T, Sternson SM, Svoboda K (2009) The subcellular organization of neocortical excitatory connections. Nature 457:1142–1145.
51. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M (2013) Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 16:1068–1076.
52. Pi HJ, Hangya B, Kvitsiani D, Sanders JI, Huang ZJ, Kepecs A (2013) Cortical interneurons that specialize in disinhibitory control. Nature 503: 521–524.
53. Pouille F, Marin-Burgin A, Adesnik H, Atallah BV, Scanziani M (2009) Input normalization by global feedforward inhibition expands cortical dynamic range. Nat Neurosci 12:1577–1585.
54. Rial Verde EM, Zayat L, Etchenique R, Yuste R (2008) Photorelease of GABA with visible light using an inorganic caging group. Front Neural Circuits 2:2.
55. Rubenstein JL, Merzenich MM (2003) Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes Brain Behav 2:255-267.
56. Rudy B, Fishell G, Lee S, Hjerling-Leffler J (2011) Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71:45–61.
57. Silberberg G, Markram H (2007) Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53:735–746.
58. Sohal VS, Zhang F, Yizhar O, Deisseroth K (2009) Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459: 698–702.
59. Somogyi P, Tamas G, Lujan R, Buhl EH (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev 26:113–135.
60. Spruston N (2008) Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 9:206–221.
61. Tamas G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902–1905.
62. Tamas G, Buhl EH, Somogyi P (1997) Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurone in the cat visual cortex. J Physiol 500:715–738.
63. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Fu Y, Lu J, Lin Y, Miyoshi G, Shima Y, Fishell G, Nelson SB, Huang ZJ (2011) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:995–1013.
64. Tsubokawa H, Ross WN (1996) IPSPs modulate spike backpropagation and associated [Ca2 +]i changes in the dendrites of hippocampal CA1 pyramidal neurons. J Neurophysiol 76:2896–2906.
65. Vicini S (1999) New perspectives in the functional role of GABA(A) channel heterogeneity. Mol Neurobiol 19:97–110.
66. Wilson NR, Runyan CA, Wang FL, Sur M (2012) Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488:343–348.
67. Yasuda R, Nimchinsky EA, Scheuss V, Pologruto TA, Oertner TG, Sabatini BL, Svoboda K (2004) Imaging calcium concentration dynamics in small neuronal compartments. Science STKE 2004:pl5.
68. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O’Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477:171-178.