Inhibitory Neuron Transplantation into Adult Visual Cortex Creates a New Critical Period that Rescues Impaired Vision

Neuron

Volumn 86, Issue 4, 2015, Pages 1055-1066

  Davis, Melissa F ^a   Figueroa Velez, Dario X ^a   Guevarra, Roblen P ^a   Yang, Michael C ^a   Habeeb, Mariyam ^a   Carathedathu, Mathew C ^a   Gandhi, Sunil P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CELL TRANSPLANTATION; EMBRYO; EMBRYO CELL; EVOKED VISUAL RESPONSE; EYE DOMINANCE; GANGLION; INHIBITORY NEURON; JUVENILE ANIMAL; MEDIAL GANGLIONIC EMINENCE; MOUSE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SPATIAL ORIENTATION; TASK PERFORMANCE; VISUAL ACUITY; VISUAL CORTEX; VISUAL DEPRIVATION; VISUAL DISCRIMINATION; VISUAL IMPAIRMENT; VISUAL STIMULATION; AGING; ANIMAL; C57BL MOUSE; GROWTH, DEVELOPMENT AND AGING; LEARNING; NERVE CELL INHIBITION; PHYSIOLOGY; SENSORY DEPRIVATION; VISION;

AGING; ANIMALS; CRITICAL PERIOD (PSYCHOLOGY); DOMINANCE, OCULAR; EVOKED POTENTIALS, VISUAL; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS; SENSORY DEPRIVATION; VISION, OCULAR; VISUAL CORTEX;

EID: 84930263015     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.03.062     Document Type: Article

References (42)

1. Beurdeley M., Spatazza J., Lee H.H.C., Sugiyama S., Bernard C., Di Nardo A.A., Hensch T.K., Prochiantz A. Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J.Neurosci. 2012, 32:9429-9437.
2. Brainard D.H. The psychophysics toolbox. Spat. Vis. 1997, 10:433-436.
3. Chen T.-W., Wardill T.J., Sun Y., Pulver S.R., Renninger S.L., Baohan A., Schreiter E.R., Kerr R.A., Orger M.B., Jayaraman V., et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 2013, 499:295-300.
4. Fagiolini M., Hensch T.K. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 2000, 404:183-186.
5. Fagiolini M., Fritschy J.-M., Löw K., Möhler H., Rudolph U., Hensch T.K. Specific GABAA circuits for visual cortical plasticity. Science 2004, 303:1681-1683.
6. Fu Y., Kaneko M., Tang Y., Alvarez-Buylla A., Stryker M.P. A cortical disinhibitory circuit for enhancing adult plasticity. Elife 2015, 4.
7. Heimel J.A., Hartman R.J., Hermans J.M., Levelt C.N. Screening mouse vision with intrinsic signal optical imaging. Eur. J. Neurosci. 2007, 25:795-804.
8. Hensch T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 2005, 6:877-888.
9. Hensch T.K., Fagiolini M., Mataga N., Stryker M.P., Baekkeskov S., Kash S.F. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 1998, 282:1504-1508.
10. Hippenmeyer S., Vrieseling E., Sigrist M., Portmann T., Laengle C., Ladle D.R., Arber S. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 2005, 3:e159.
11. Huang Z.J., Kirkwood A., Pizzorusso T., Porciatti V., Morales B., Bear M.F., Maffei L., Tonegawa S. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 1999, 98:739-755.
12. Jacobs G.H., Williams G.A., Fenwick J.A. Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse. Vision Res. 2004, 44:1615-1622.
13. Kalatsky V.A., Stryker M.P. New paradigm for optical imaging: temporally encoded maps of intrinsic signal. Neuron 2003, 38:529-545.
14. Kaneko M., Stryker M.P. Sensory experience during locomotion promotes recovery of function in adult visual cortex. Elife 2014, 3:e02798.
15. Kaneko M., Hanover J.L., England P.M., Stryker M.P. TrkB kinase is required for recovery, but not loss, of cortical responses following monocular deprivation. Nat. Neurosci. 2008, 11:497-504.
16. Kerlin A.M., Andermann M.L., Berezovskii V.K., Reid R.C. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 2010, 67:858-871.
17. Kuhlman S.J., Tring E., Trachtenberg J.T. Fast-spiking interneurons have an initial orientation bias that is lost with vision. Nat. Neurosci. 2011, 14:1121-1123.
18. Kuhlman S.J., Olivas N.D., Tring E., Ikrar T., Xu X., Trachtenberg J.T. A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 2013, 501:543-546.
19. Lehmann K., Löwel S. Age-dependent ocular dominance plasticity in adult mice. PLoS ONE 2008, 3:e3120.
20. Li Y.-T., Ma W.-P., Pan C.-J., Zhang L.I., Tao H.W. Broadening of cortical inhibition mediates developmental sharpening of orientation selectivity. J.Neurosci. 2012, 32:3981-3991.
21. Madisen L., Zwingman T.A., Sunkin S.M., Oh S.W., Zariwala H.A., Gu H., Ng L.L., Palmiter R.D., Hawrylycz M.J., Jones A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 2010, 13:133-140.
22. Maya Vetencourt J.F., Sale A., Viegi A., Baroncelli L., De Pasquale R., O'Leary O.F., Castrén E., Maffei L. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 2008, 320:385-388.
23. Miyoshi G., Hjerling-Leffler J., Karayannis T., Sousa V.H., Butt S.J.B., Battiste J., Johnson J.E., Machold R.P., Fishell G. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J.Neurosci. 2010, 30:1582-1594.
24. Montey K.L., Eaton N.C., Quinlan E.M. Repetitive visual stimulation enhances recovery from severe amblyopia. Learn. Mem. 2013, 20:311-317.
25. Niell C.M., Stryker M.P. Highly selective receptive fields in mouse visual cortex. J.Neurosci. 2008, 28:7520-7536.
26. Pla R., Borrell V., Flames N., Marín O. Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J.Neurosci. 2006, 26:6924-6934.
27. Pologruto T.A., Sabatini B.L., Svoboda K. ScanImage: flexible software for operating laser scanning microscopes. Biomed. Eng. Online 2003, 2:13.
28. Prusky G.T., Douglas R.M. Developmental plasticity of mouse visual acuity. Eur. J. Neurosci. 2003, 17:167-173.
29. Prusky G.T., West P.W., Douglas R.M. Behavioral assessment of visual acuity in mice and rats. Vision Res. 2000, 40:2201-2209.
30. Runyan C.A., Sur M. Response selectivity is correlated to dendritic structure in parvalbumin-expressing inhibitory neurons in visual cortex. J.Neurosci. 2013, 33:11724-11733.
31. Runyan C.A., Schummers J., Van Wart A., Kuhlman S.J., Wilson N.R., Huang Z.J., Sur M. Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron 2010, 67:847-857.
32. Sato M., Stryker M.P. Distinctive features of adult ocular dominance plasticity. J.Neurosci. 2008, 28:10278-10286.
33. Sawtell N.B., Frenkel M.Y., Philpot B.D., Nakazawa K., Tonegawa S., Bear M.F. NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 2003, 38:977-985.
34. Southwell D.G., Froemke R.C., Alvarez-Buylla A., Stryker M.P., Gandhi S.P. Cortical plasticity induced by inhibitory neuron transplantation. Science 2010, 327:1145-1148.
35. Southwell D.G., Nicholas C.R., Basbaum A.I., Stryker M.P., Kriegstein A.R., Rubenstein J.L., Alvarez-Buylla A. Interneurons from embryonic development to cell-based therapy. Science 2014, 344:1240622.
36. Stephany C.-É., Chan L.L.H., Parivash S.N., Dorton H.M., Piechowicz M., Qiu S., McGee A.W. Plasticity of binocularity and visual acuity are differentially limited by nogo receptor. J.Neurosci. 2014, 34:11631-11640.
37. Sugiyama S., Di Nardo A.A., Aizawa S., Matsuo I., Volovitch M., Prochiantz A., Hensch T.K. Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 2008, 134:508-520.
38. Tang Y., Stryker M.P., Alvarez-Buylla A., Espinosa J.S. Cortical plasticity induced by transplantation of embryonic somatostatin or parvalbumin interneurons. Proc. Natl. Acad. Sci. USA 2014, 111:18339-18344.
39. Tognini P., Manno I., Bonaccorsi J., Cenni M.C., Sale A., Maffei L. Environmental enrichment promotes plasticity and visual acuity recovery in adult monocular amblyopic rats. PLoS ONE 2012, 7:e34815.
40. Vong L., Ye C., Yang Z., Choi B., Chua S., Lowell B.B. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 2011, 71:142-154.
41. Wichterle H., Garcia-Verdugo J.M., Herrera D.G., Alvarez-Buylla A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat. Neurosci. 1999, 2:461-466.
42. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.