Adrenergic gating of hebbian spike-timing-dependent plasticity in cortical interneurons

Journal of Neuroscience

Volumn 33, Issue 32, 2013, Pages 13171-13178

  Huang, Shiyong ^a   Huganir, Richard L ^b   Kirkwood, Alfredo ^a,b  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; BETA ADRENERGIC RECEPTOR; ISOPRENALINE; METABOTROPIC RECEPTOR; METHOXAMINE; N METHYL DEXTRO ASPARTIC ACID;

ADRENERGIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DEPRESSION; ELECTRODE; INTERNEURON; MOUSE; NERVE CELL PLASTICITY; NERVE POTENTIAL; NEUROMODULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SOMATOSENSORY CORTEX; VISUAL CORTEX;

ACTION POTENTIALS; ADRENERGIC AGENTS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ELECTRIC STIMULATION; FEMALE; GREEN FLUORESCENT PROTEINS; INTERNEURONS; ISOPROTERENOL; MALE; METHOXAMINE; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; PARVALBUMINS; RECEPTORS, ADRENERGIC; RECEPTORS, METABOTROPIC GLUTAMATE; TIME FACTORS; VISUAL CORTEX;

EID: 84881153569     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5741-12.2013     Document Type: Article

References (54)

1. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsáki G, Cauli B, Defelipe J, Fairén A, Feldmeyer 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 Rev Neurosci 9:557-568. CrossRef Medline
2. Atallah BV, Bruns W, Carandini M, Scanziani M (2012) Parvalbuminexpressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73:159-170. CrossRef Medline
3. Bezanilla F (2008) How membrane proteins sense voltage. Nat Rev Mol Cell Biol 9:323-332. CrossRef Medline
4. Castillo PE, Chiu CQ, Carroll RC (2011) Long-term plasticity at inhibitory synapses. Curr Opin Neurobiol 21:328-338. CrossRef Medline
5. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611. CrossRef Medline
6. Chen HX, Jiang M, Akakin D, Roper SN (2009) Long-term potentiation of excitatory synapses on neocortical somatostatin-expressing interneurons. J Neurophysiol 102:3251-3259. CrossRef Medline
7. Choi SY, Chang J, Jiang B, Seol GH, Min SS, Han JS, Shin HS, Gallagher M, Kirkwood A (2005) Multiple receptors coupled to PLC gate LTD in visual cortex. J Neurosci 25:11433-11443. CrossRef Medline
8. Dan Y, Poo MM (2004) Spike timing-dependent plasticity of neural circuits. Neuron 44:23-30. CrossRef Medline
9. Edelmann E, Lessmann V (2011) Dopamine modulates spike timingdependent plasticity and action potential properties in CA1 pyramidal neurons of acute rat hippocampal slices. Front Synaptic Neurosci 3:6. CrossRef Medline
10. Feldman DE (2012) The spike-timing dependence of plasticity. Neuron 75: 556-571. CrossRef Medline
11. Feldman DE, Nicoll RA, Malenka RC (1999) Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. J Neurobiol 41:92-101. CrossRef Medline
12. Ferster D, Miller KD (2000) Neural mechanisms of orientation selectivity in the visual cortex. Annu Rev Neurosci 23:441-471. CrossRef Medline
13. Fino E, Venance L (2010) Spike-timing dependent plasticity in the striatum. Front Synaptic Neurosci 2:6. CrossRef Medline
14. Fino E, Venance L (2011) Spike-timing dependent plasticity in striatal interneurons. Neuropharmacology 60:780-788. CrossRef Medline
15. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56:33-42. CrossRef Medline
16. Froemke RC, Debanne D, Bi GQ (2010) Temporal modulation of spiketiming- dependent plasticity. Front Synaptic Neurosci 2:19. CrossRef Medline
17. Gu Z, Yakel JL (2011) Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 71:155-165. CrossRef Medline
18. Gu Z, Lamb PW, Yakel JL (2011) Cholinergic coordination of presynaptic and postsynaptic activity induces timing-dependent hippocampal synaptic plasticity. J Neurosci 32:12337-12348. CrossRef Medline
19. Guo Y, Huang S, de Pasquale R, McGehrin K, Lee HK, Zhao K, Kirkwood A (2012) Dark exposure extends the integration window for spike-timingdependent plasticity. J Neurosci 32:15027-15035. CrossRef Medline
20. 2+ dependency for triggering retrograde endocannabinoid signal. Neuron 45:257-268. CrossRef Medline
21. Ho OH, Delgado JY, O'Dell TJ (2004) Phosphorylation of proteins involved in activity-dependent forms of synaptic plasticity is altered in hippocampal slices maintained in vitro. J Neurochem 91:1344-1357. CrossRef Medline
22. 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. CrossRef Medline
23. Huang S, Trevino M, He K, Ardiles A, de Pasquale R, Guo Y, Palacios A, Huganir R, Kirkwood A (2012) Pull-push neuromodulation of LTP and LTD enables bidirectional experience-induced synaptic scaling in visual cortex. Neuron 73:497-510. CrossRef Medline
24. Huang ZJ, Di Cristo G, Ango F (2007) Development of GABA innervation in the cerebral and cerebellar cortices. Nat Rev Neurosci 8:673-686. CrossRef Medline
25. Jiang B, Huang ZJ, Morales B, Kirkwood A (2005) Maturation of GABAergic transmission and the timing of plasticity in visual cortex. Brain Res Brain Res Rev 50:126-133. CrossRef Medline
26. Jiang B, Trevino M, Kirkwood A (2007) Sequential development of longterm potentiation and depression in different layers of the mouse visual cortex. J Neurosci 27:9648-9652. CrossRef Medline
27. Jiang B, Sohya K, Sarihi A, Yanagawa Y, Tsumoto T (2010a) Laminarspecific maturation of GABAergic transmission and susceptibility to visual deprivation are related to endocannabinoid sensitivity in mouse visual cortex. J Neurosci 30:14261-14272. CrossRef Medline
28. Jiang B, Huang S, de Pasquale R, Millman D, Song L, Lee HK, Tsumoto T, Kirkwood A (2010b) The maturation of GABAergic transmission in visual cortex requires endocannabinoid-mediated LTD of inhibitory inputs during a critical period. Neuron 66:248-259. CrossRef Medline
29. Kameyama K, Sohya K, Ebina T, Fukuda A, Yanagawa Y, Tsumoto T (2010) Difference in binocularity and ocular dominance plasticity between GABAergic and excitatory cortical neurons. J Neurosci 30:1551-1559. CrossRef Medline
30. Kuhlman SJ, Lu J, Lazarus MS, Huang ZJ (2010) Maturation of GABAergic inhibition promotes strengthening of temporally coherent inputs among convergent pathways. PLoS Comput Biol 6:e1000797. CrossRef Medline
31. Kuhlman SJ, Tring E, Trachtenberg JT (2011) Fast-spiking interneurons have an initial orientation bias that is lost with vision. Nat Neurosci 14: 1121-1123. CrossRef Medline
32. Kullmann DM, Moreau AW, Bakiri Y, Nicholson E (2012) Plasticity of inhibition. Neuron 75:951-962. CrossRef Medline
33. Lamsa KP, Heeroma JH, Somogyi P, Rusakov DA, Kullmann DM (2007) Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit. Science 315:1262-1266. CrossRef Medline
34. Lamsa KP, Kullmann DM, Woodin MA (2010) Spike-timing dependent plasticity in inhibitory circuits. Front Synaptic Neurosci 2:8. CrossRef Medline
35. Lee HK, Kirkwood A (2011) AMPA receptor regulation during synaptic plasticity in hippocampus and neocortex. Semin Cell Dev Biol 22:514-520. CrossRef Medline
36. 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. CrossRef Medline
37. Li YT, Ma WP, Li LY, Ibrahim LA, Wang SZ, Tao HW (2012) Broadening of inhibitory tuning underlies contrast-dependent sharpening of orientation selectivity in mouse visual cortex. J Neurosci 32:16466-16477. CrossRef Medline
38. Lu JT, Li CY, Zhao JP, Poo MM, Zhang XH (2007) Spike-timing-dependent plasticity of neocortical excitatory synapses on inhibitory interneurons depends on target cell type. J Neurosci 27:9711-9720. CrossRef Medline
39. Markram H, Gerstner W, Sjostrom PJ (2011) A history of spike-timingdependent plasticity. Front Synaptic Neurosci 3:4. CrossRef Medline
40. Martin KA (2002) Microcircuits in visual cortex. Curr Opin Neurobiol 12: 418-425. CrossRef Medline
41. McMahon LL, Kauer JA (1997) Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18:295-305. CrossRef Medline
42. Morales B, Choi SY, Kirkwood A (2002) Dark rearing alters the development of GABAergic transmission in visual cortex. J Neurosci 22:8084-8090. Medline
43. Nissen W, Szabo A, Somogyi J, Somogyi P, Lamsa KP (2010) Cell typespecific long-term plasticity at glutamatergic synapses onto hippocampal interneurons expressing either parvalbumin or CB1 cannabinoid receptor. J Neurosci 30:1337-1347. CrossRef Medline
44. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20: 3354-3368. Medline
45. Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159-1163. CrossRef Medline
46. Richards BA, Aizenman CD, Akerman CJ (2010) In vivo spike-timingdependent plasticity in the optic tectum of Xenopus laevis. Front Synaptic Neurosci 2:7. CrossRef Medline
47. Sarihi A, Jiang B, Komaki A, Sohya K, Yanagawa Y, Tsumoto T (2008) Metabotropic glutamate receptor type 5-dependent long-term potentiation of excitatory synapses on fast-spiking GABAergic neurons in mouse visual cortex. J Neurosci 28:1224-1235. CrossRef Medline
48. Seol GH, Ziburkus J, Huang S, Song L, Kim IT, Takamiya K, Huganir RL, Lee HK, Kirkwood A (2007) Neuromodulators control the polarity of spiketiming- dependent synaptic plasticity. Neuron 55:919-929. CrossRef Medline
49. Shouval HZ, Wang SS, Wittenberg GM (2010) Spike timing dependent plasticity: a consequence of more fundamental learning rules. Front Comput Neurosci 4.
50. Song S, Abbott LF (2001) Cortical development and remapping through spike timing-dependent plasticity. Neuron 32:339-350. CrossRef Medline
51. Song S, Miller KD, Abbott LF (2000) Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3:919-926. CrossRef Medline
52. Szabo A, Somogyi J, Cauli B, Lambolez B, Somogyi P, Lamsa KP (2012) Calcium-permeable AMPA receptors provide a common mechanism for LTP in glutamatergic synapses of distinct hippocampal interneuron types. J Neurosci 32:6511-6516. CrossRef Medline
53. 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. CrossRef Medline
54. Zhang JC, Lau PM, Bi GQ (2009) Gain in sensitivity and loss in temporal contrast of STDP by dopaminergic modulation at hippocampal synapses. Proc Natl Acad Sci U S A 106:13028-13033. CrossRef Medline