Experience-Dependent Rewiring of Specific Inhibitory Connections in Adult Neocortex

PLoS Biology

Volumn 12, Issue 2, 2014, Pages

  Kätzel, Dennis ^a   Miesenböck, Gero ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN MAPPING; BRAIN REGION; CELLULAR DISTRIBUTION; EXPERIMENTAL MOUSE; GABAERGIC TRANSMISSION; INTERNEURON; MOUSE; NEOCORTEX; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTOGENETICS; SENSORY DEPRIVATION (INTENTIONAL); SOMATOSENSORY CORTEX; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; VIBRISSA;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; GABAERGIC NEURONS; INTERNEURONS; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOCORTEX; NERVE NET; NEURONAL PLASTICITY; ORGAN SPECIFICITY; RHODOPSIN; SENSORY DEPRIVATION; SYNAPSES; TOUCH PERCEPTION; VIBRISSAE;

EID: 84895503357     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001798     Document Type: Article

References (57)

1. Hubel DH, Wiesel TN, (1974) Uniformity of monkey striate cortex: a parallel relationship between field size, scatter, and magnification factor. J Comp Neurol 158: 295-305.
2. Mountcastle VB (1978) An organizing principle for cerebral function: The unit module and the distributed system. In: Mountcastle VB, Edelman GM, editors. The mindful brain. Cambridge: MIT Press. pp. 7-50.
3. Sadato N, Pascual-Leone A, Grafman J, Ibanez V, Deiber MP, et al. (1996) Activation of the primary visual cortex by Braille reading in blind subjects. Nature 380: 526-528.
4. Douglas RJ, Martin KA, (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27: 419-451.
5. Kätzel D, Zemelman BV, Buetfering C, Wölfel M, Miesenböck G, (2011) The columnar and laminar organization of inhibitory connections to neocortical excitatory cells. Nat Neurosci 14: 100-107.
6. Chen JL, Lin WC, Cha JW, So PT, Kubota Y, et al. (2011) Structural basis for the role of inhibition in facilitating adult brain plasticity. Nat Neurosci 14: 587-594.
7. Keck T, Scheuss V, Jacobsen RI, Wierenga CJ, Eysel UT, et al. (2011) Loss of sensory input causes rapid structural changes of inhibitory neurons in adult mouse visual cortex. Neuron 71: 869-882.
8. Chen JL, Villa KL, Cha JW, So PT, Kubota Y, et al. (2012) Clustered dynamics of inhibitory synapses and dendritic spines in the adult neocortex. Neuron 74: 361-373.
9. van Versendaal D, Rajendran R, Saiepour MH, Klooster J, Smit-Rigter L, et al. (2012) Elimination of inhibitory synapses is a major component of adult ocular dominance plasticity. Neuron 74: 374-383.
10. Zemelman BV, Lee GA, Ng M, Miesenböck G, (2002) Selective photostimulation of genetically chARGed neurons. Neuron 33: 15-22.
11. Lima SQ, Miesenböck G, (2005) Remote control of behavior through genetically targeted photostimulation of neurons. Cell 121: 141-152.
12. Miesenböck G, (2009) The optogenetic catechism. Science 326: 395-399.
13. Hegemann P, Fuhrmann M, Kateriya S, (2001) Algal sensory photoreceptors. J Phycol 37: 668-676.
14. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, et al. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA 100: 13940-13945.
15. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K, (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268.
16. Petreanu L, Mao T, Sternson SM, Svoboda K, (2009) The subcellular organization of neocortical excitatory connections. Nature 457: 1142-1145.
17. Petreanu L, Huber D, Sobczyk A, Svoboda K, (2007) Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci 10: 663-668.
18. Wang H, Peca J, Matsuzaki M, Matsuzaki K, Noguchi J, et al. (2007) High-speed mapping of synaptic connectivity using photostimulation in Channelrhodopsin-2 transgenic mice. Proc Natl Acad Sci USA 104: 8143-8148.
19. Madisen L, Mao T, Koch H, Zhuo JM, Berenyi A, et al. (2012) A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci 15: 793-802.
20. Dantzker JL, Callaway EM, (2000) Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat Neurosci 3: 701-707.
21. Shepherd GM, Pologruto TA, Svoboda K, (2003) Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38: 277-289.
22. Shepherd GM, Svoboda K, (2005) Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J Neurosci 25: 5670-5679.
23. Aravanis AM, Wang LP, Zhang F, Meltzer LA, Mogri MZ, et al. (2007) An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. J Neural Eng 4: S143-S156.
24. Lefort S, Tomm C, Floyd Sarria J-C, Petersen CCH, (2009) The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 61: 301-316.
25. Xu X, Roby KD, Callaway EM, (2010) Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 518: 389-404.
26. Fino E, Yuste R, (2011) Dense inhibitory connectivity in neocortex. Neuron 69: 1188-1203.
27. Xu X, Callaway EM, (2009) Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J Neurosci 29: 70-85.
28. Glazewski S, Fox K, (1996) Time course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. J Neurophysiol 75: 1714-1729.
29. Fox K, Wong RO, (2005) A comparison of experience-dependent plasticity in the visual and somatosensory systems. Neuron 48: 465-477.
30. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, et al. (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807.
31. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M, (2007) Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 10: 743-753.
32. Somogyi P, Tamas G, Lujan R, Buhl EH, (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26: 113-135.
33. Gupta A, Wang Y, Markram H, (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287: 273-278.
34. Murthy VN, Schikorski T, Stevens CF, Zhu Y, (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32: 673-682.
35. House DR, Elstrott J, Koh E, Chung J, Feldman DE, (2011) Parallel regulation of feedforward inhibition and excitation during whisker map plasticity. Neuron 72: 819-831.
36. Antonini A, Stryker MP, (1993) Rapid remodeling of axonal arbors in the visual cortex. Science 260: 1819-1821.
37. Maravall M, Koh IY, Lindquist WB, Svoboda K, (2004) Experience-dependent changes in basal dendritic branching of layer 2/3 pyramidal neurons during a critical period for developmental plasticity in rat barrel cortex. Cereb Cortex 14: 655-664.
38. Trachtenberg JT, Chen BE, Knott GW, Feng G, Sanes JR, et al. (2002) Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 420: 788-794.
39. Marik SA, Yamahachi H, McManus JN, Szabo G, Gilbert CD, (2010) Axonal dynamics of excitatory and inhibitory neurons in somatosensory cortex. PLoS Biol 8: e1000395.
40. Hofer SB, Mrsic-Flogel TD, Bonhoeffer T, Hubener M, (2009) Experience leaves a lasting structural trace in cortical circuits. Nature 457: 313-317.
41. Jacob V, Petreanu L, Wright N, Svoboda K, Fox K, (2012) Regular spiking and intrinsic bursting pyramidal cells show orthogonal forms of experience-dependent plasticity in layer V of barrel cortex. Neuron 73: 391-404.
42. Cruikshank SJ, Urabe H, Nurmikko AV, Connors BW, (2010) Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65: 230-245.
43. Kampa BM, Letzkus JJ, Stuart GJ, (2006) Cortical feed-forward networks for binding different streams of sensory information. Nat Neurosci 9: 1472-1473.
44. Berger TK, Silberberg G, Perin R, Markram H, (2010) Brief bursts self-inhibit and correlate the pyramidal network. PLoS Biol 8: e1000473.
45. Koralek KA, Jensen KF, Killackey HP, (1988) Evidence for two complementary patterns of thalamic input to the rat somatosensory cortex. Brain Res 463: 346-351.
46. Diamond ME, Armstrong-James M, Budway MJ, Ebner FF, (1992) Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J Comp Neurol 319: 66-84.
47. Lu SM, Lin RC, (1993) Thalamic afferents of the rat barrel cortex: a light- and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosens Mot Res 10: 1-16.
48. 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.
49. Gonchar Y, Burkhalter A, (2003) Distinct GABAergic targets of feedforward and feedback connections between lower and higher areas of rat visual cortex. J Neurosci 23: 10904-10912.
50. Anderson JC, Martin KA, (2006) Synaptic connection from cortical area V4 to V2 in macaque monkey. J Comp Neurol 495: 709-721.
51. Matyas F, Sreenivasan V, Marbach F, Wacongne C, Barsy B, et al. (2010) Motor control by sensory cortex. Science 330: 1240-1243.
52. Milo R, Shen-Orr S, Itzkovitz S, Kashtan N, Chklovskii D, et al. (2002) Network motifs: simple building blocks of complex networks. Science 298: 824-827.
53. Sporns O, Kötter R, (2004) Motifs in brain networks. PLoS Biol 2: e369.
54. Song S, Sjöström PJ, Reigl M, Nelson S, Chklovskii DB, (2005) Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 3: e68.
55. Finnerty GT, Roberts LS, Connors BW, (1999) Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400: 367-371.
56. Myatt DR, Hadlington T, Ascoli GA, Nasuto SJ, (2012) Neuromantic-from semi-manual to semi-automatic reconstruction of neuron morphology. Front Neuroinform 6: 4.
57. Shepherd GMG, Raastad M, Andersen P, (2002) General and variable features of varicosity spacing along unmyelinated axons in the hippocampus and cerebellum. Proc Natl Acad Sci USA 99: 6340-6345.