Synaptic basis for developmental plasticity in somatosensory cortex

Current Opinion in Neurobiology

Volumn 14, Issue 1, 2004, Pages 89-95

  Foeller, Elisabeth ^a   Feldman, Daniel E ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

AMPA; GABA; L; Layer; Long term depression; Long term potentiation; LTD; LTP; N methyl D aspartate; NMDA; Primary somatosensory cortex; Primary visual cortex; S1; V1; amino 3 hydroxy 5 methyl 4 isoxazole propionic acid; aminobutyric acid

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

GABAERGIC TRANSMISSION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MEDIAL LEMNISCUS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; RECEPTIVE FIELD; REVIEW; SOMATOSENSORY CORTEX; SYNAPTIC MEMBRANE; SYNAPTOGENESIS; THALAMOCORTICAL TRACT; VIBRISSA;

EID: 1342328013     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2004.01.011     Document Type: Review

References (65)

1. Calford M.B. Dynamic representational plasticity in sensory cortex. Neuroscience. 111:2002;709-738.
2. Buonomano D.V., Merzenich M.M. Cortical plasticity: from synapses to maps. Annu Rev Neurosci. 21:1998;149-186.
3. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science. 274:1996;1133-1138.
4. Chen R., Cohen L.G., Hallett M. Nervous system reorganization following injury. Neuroscience. 111:2002;761-773.
5. Pantev C., Engelien A., Candia V., Elbert T. Representational cortex in musicians. Plastic alterations in response to musical practice. Ann N Y Acad Sci. 930:2001;300-314.
6. Dinse H.R., Ragert P., Pleger B., Schwenkreis P., Tegenthoff M. Pharmacological modulation of perceptual learning and associated cortical reorganization. Science. 301:2003;91-94 In this study, brief (3-h) tactile coactivation of the index finger in humans is shown to improve tactile discrimination performance and to induce S1 map plasticity, as measured by somatosensory evoked potentials. These effects are both blocked by an NMDA receptor antagonist and augmented by amphetamine, and the individual amount of map plasticity is highly correlated with discrimination performance. The authors conclude that discrimination learning and S1 map plasticity both involve NMDA receptor-mediated forms of synaptic plasticity.
7. Trachtenberg J.T., Chen B.E., Knott G.W., Feng G., Sanes J.R., Welker E., Svoboda K. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature. 420:2002;788-794 In vivo two-photon imaging and ultrastructure analysis are used to demonstrate that dendritic spines are motile in adult S1, that spine motility is associated with synapse formation, and that whisker experience regulates spine dynamics. Thus, experience is likely to regulate the rapid formation and elimination of synapses, even in adult S1.
8. Zito K., Svoboda K. Activity-dependent synaptogenesis in the adult Mammalian cortex. Neuron. 35:2002;1015-1017.
9. Woolsey T.A., Van der Loos H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. The description of a cortical field composed of discrete cytoarchitectonic units. Brain Res. 17:1970;205-242.
10. Simons D.J. Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol. 41:1978;798-820.
11. Armstrong-James M., Fox K. Spatiotemporal convergence and divergence in the rat S1 'barrel' cortex. J Comp Neurol. 263:1987;265-281.
12. Fox K. Anatomical pathways and molecular mechanisms for plasticity in the barrel cortex. Neuroscience. 111:2002;799-814.
13. Feldman D.E., Nicoll R.A., Malenka R.C. Synaptic plasticity at thalamocortical synapses in developing rat somatosensory cortex: LTP, LTD, and silent synapses. J Neurobiol. 41:1999;92-101.
14. Antonini A., Stryker M.P. Rapid remodeling of axonal arbors in the visual cortex. Science. 260:1993;1819-1821.
15. Stern E.A., Maravall M., Svoboda K. Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron. 31:2001;305-315.
16. Diamond M.E., Huang W., Ebner F.F. Laminar comparison of somatosensory cortical plasticity. Science. 265:1994;1885-1888.
17. Armstrong-James M., Diamond M.E., Ebner F.F. An innocuous bias in whisker use in adult rats modifies receptive fields of barrel cortex neurons. J Neurosci. 14:1994;6978-6991.
18. Trachtenberg J.T., Trepel C., Stryker M.P. Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science. 287:2000;2029-2032.
19. Trachtenberg J.T., Stryker M.P. Rapid anatomical plasticity of horizontal connections in the developing visual cortex. J Neurosci. 21:2001;3476-3482.
20. Heynen A.J., Yoon B.J., Liu C.H., Chung H.J., Huganir R.L., Bear M.F. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat Neurosci. 6:2003;854-862 This paper provides biochemical and physiological evidence that short periods of monocular deprivation during the critical period induce LTD in visual cortex, including at L4 to L2/3 synapses. Deprivation alters AMPA receptor phosphorylation and cell surface expression in the same manner as does experimentally induced LTD, and occludes subsequent LTD at L4 to L2/3 synapses in vitro. These findings suggest that LTD is a key mechanism in ocular dominance plasticity in visual cortex.
21. Calford M.B., Wright L.L., Metha A.B., Taglianetti V. Topographic plasticity in primary visual cortex is mediated by local corticocortical connections. J Neurosci. 23:2003;6434-6442.
22. Wallace H., Glazewski S., Liming K., Fox K. The role of cortical activity in experience-dependent potentiation and depression of sensory responses in rat barrel cortex. J Neurosci. 21:2001;3881-3894.
23. Glazewski S., McKenna M., Jacquin M., Fox K. Experience-dependent depression of vibrissae responses in adolescent rat barrel cortex. Eur J Neurosci. 10:1998;2107-2116.
24. Rema V., Armstrong-James M., Ebner F.F. Experience-dependent plasticity of adult rat S1 cortex requires local NMDA receptor activation. J Neurosci. 18:1998;10196-10206.
25. Shepherd G.M., Pologruto T.A., Svoboda K. Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron. 38:2003;277-289 Experience-dependent changes in L4 to L2/3 circuit organization are measured by mapping monosynaptic inputs to L2/3 neurons in S1 slices using laser scanning photostimulation. Whisker deprivation, during an early critical period when L4 to L2/3 circuits are first forming, impairs the development of inputs from L4 barrels and enhances the inputs from L4 septa, which are normally sparse. These findings indicate that barrel (lemniscal) and septal (non-lemniscal) circuits compete to innervate L2/3, and that early experience favors lemniscal inputs.
26. ••] constitute the first direct observations of experience-induced LTD in vivo.
27. Hickmott P.W., Merzenich M.M. Local circuit properties underlying cortical reorganization. J Neurophysiol. 88:2002;1288-1301.
28. Takahashi T., Svoboda K., Malinow R. Experience strengthening transmission by driving AMPA receptors into synapses. Science. 299:2003;1585-1588 This elegant paper uses electrophysiology and viral transfection to demonstrate that experience drives an LTP-like insertion of AMPA receptor subunits at immature L4 to L2/3 synapses in rat S1. Whisker experience causes measurable insertion of GluR1 subunits and an increase in AMPA currents; in addition, the details of subunit incorporation are identical to those observed during LTP in vitro. Blocking GluR1 delivery, a manipulation that prevents LTP, prevents experience-driven potentiation of AMPA currents, indicating that experience drives LTP at L4 to L2/3 synapses in vivo.
29. Bender K.J., Rangel J., Feldman D.E. Development of columnar topography in the excitatory layer 4 to layer 2/3 projection in rat barrel cortex. J Neurosci. 23:2003;8759-8770 The development of L4 to L2/3 axonal topography is studied using axonal reconstructions of single excitatory L4 cells from rat S1 slices. Whisker deprivation protocols that induce receptive field plasticity in L2/3 and/or drive LTD at L4 to L2/3 synapses fail to alter axonal morphology. These results indicate that experience-dependent plasticity in post-neonatal animals is unlikely to involve large-scale anatomical reorganization of L4 to L2/3 projections.
30. Finnerty G.T., Roberts L.S., Connors B.W. Sensory experience modifies the short-term dynamics of neocortical synapses. Nature. 400:1999;367-371.
31. Urban J., Kossut M., Hess G. Long-term depression and long-term potentiation in horizontal connections of the barrel cortex. Eur J Neurosci. 16:2002;1772-1776.
32. Hirsch J.A., Gilbert C.D. Long-term changes in synaptic strength along specific intrinsic pathways in the cat visual cortex. J Physiol. 461:1993;247-262.
33. Rioult-Pedotti M.S., Friedman D., Donoghue J.P. Learning-induced LTP in neocortex. Science. 290:2000;533-536.
34. Petersen CCH, Brecht M, Sakmann B: Activity-dependent synaptic wiring of layer 2/3 rat barrel cortex underlying map plasticity. Washington, DC: Society for Neuroscience Abstract 2002; Program No. 413.3 URL: http://sfn.scholarone. com/itin2002/.
35. Keller A., Carlson G.C. Neonatal whisker clipping alters intracortical, but not thalamocortical projections, in rat barrel cortex. J Comp Neurol. 412:1999;83-94.
36. Kossut M., Juliano S.L. Anatomical correlates of representational map reorganization induced by partial vibrissectomy in the barrel cortex of adult mice. Neuroscience. 92:1999;807-817.
37. Darian-Smith C., Gilbert C.D. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature. 368:1994;737-740.
38. Lowel S., Singer W. Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. Science. 255:1992;209-212.
39. Lu H.C., She W.C., Plas D.T., Neumann P.E., Janz R., Crair M.C. Adenylyl cyclase I regulates AMPA receptor trafficking during mouse cortical 'barrel' map development. Nat Neurosci. 6:2003;939-947 In this paper, barrelless mutant mice that lack adenylyl cyclase I and fail to form discrete S1 barrels are shown to have severe deficits in thalamocortical LTP and LTD, in AMPA receptor trafficking, and in functional maturation of thalamocortical synapses. These and other findings suggest that cAMP/protein kinase A signaling is required for thalamocortical synapse maturation and for barrel map formation.
40. Armstrong-James M., Fox K., Das-Gupta A. Flow of excitation within rat barrel cortex on striking a single vibrissa. J Neurophysiol. 68:1992;1345-1358.
41. Glazewski S., Giese K.P., Silva A., Fox K. The role of α-CaMKII autophosphorylation in neocortical experience-dependent plasticity. Nat Neurosci. 3:2000;911-918.
42. Hardingham N., Glazewski S., Pakhotin P., Mizuno K., Chapman P.F., Giese K.P., Fox K. Neocortical long-term potentiation and experience-dependent synaptic plasticity require α-calcium/calmodulin-dependent protein kinase II autophosphorylation. J Neurosci. 23:2003;4428-4436.
43. Jones E.G. GABAergic neurons and their role in cortical plasticity in primates. Cereb Cortex. 3:1993;361-372.
44. A receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr Opin Neurobiol. 13:2003;341-347.
45. Gaiarsa J.L., Caillard O., Ben-Ari Y. Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci. 25:2002;564-570.
46. Knott G.W., Quairiaux C., Genoud C., Welker E. Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron. 34:2002;265-273 Continuous 24-h stimulation of a single whisker is shown by electron microscopy to increase substantially and stably the density of inhibitory synapses on L4 spines, but to produce only modest and transient changes in excitatory synapse density. The changes in inhibitory synapses last at least 4 days and are paralleled by changes in the long-latency components of whisker-evoked responses in the stimulated barrel.
47. A α1 receptor subunit mRNA in somatosensory cortex of mice following learning-dependent plasticity of cortical representations. Brain Res Mol Brain Res. 96:2001;82-86.
48. Gierdalski M., Jablonska B., Siucinska E., Lech M., Skibinska A., Kossut M. Rapid regulation of GAD67 mRNA and protein level in cortical neurons after sensory learning. Cereb Cortex. 11:2001;806-815.
49. A receptor binding in layer IV of adult primate somatosensory cortex after peripheral nerve injury. Brain Res. 954:2002;68-72.
50. Micheva K.D., Beaulieu C. Development and plasticity of the inhibitory neocortical circuitry with an emphasis on the rodent barrel field cortex: a review. Can J Physiol Pharmacol. 75:1997;470-478.
51. 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. 282:1998;1504-1508.
52. Rozas C., Frank H., Heynen A.J., Morales B., Bear M.F., Kirkwood A. Developmental inhibitory gate controls the relay of activity to the superficial layers of the visual cortex. J Neurosci. 21:2001;6791-6801.
53. B receptor blockade on receptive fields of raccoon somatosensory cortical neurons during reorganization. Exp Brain Res. 145:2002;150-157.
54. Rasmusson D.D. Reorganization of raccoon somatosensory cortex following removal of the fifth digit. J Comp Neurol. 205:1982;313-326.
55. Rasmusson D.D., Turnbull B.G. Immediate effects of digit amputation on SI cortex in the raccoon: unmasking of inhibitory fields. Brain Res. 288:1983;368-370.
56. A receptors. J Neurophysiol. 86:2001;94-103.
57. Li C.X., Callaway J.C., Waters R.S. Removal of GABAergic inhibition alters subthreshold input in neurons in forepaw barrel subfield (FBS) in rat first somatosensory cortex (SI) after digit stimulation. Exp Brain Res. 145:2002;411-428.
58. Jung S.C., Shin H.C. Suppression of temporary deafferentation-induced plasticity in the primary somatosensory cortex of rats by GABA antagonist. Neurosci Lett. 334:2002;87-90.
59. Bienenstock E.L., Cooper L.N., Munro P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci. 2:1982;32-48.
60. Bear M.F., Cooper L.N., Ebner F.F. A physiological basis for a theory of synapse modification. Science. 237:1987;42-48.
61. Kyriazi H.T., Carvell G.E., Brumberg J.C., Simons D.J. Quantitative effects of GABA and bicuculline methiodide on receptive field properties of neurons in real and simulated whisker barrels. J Neurophysiol. 75:1996;547-560.
62. Zheng W., Knudsen E.I. Gabaergic inhibition antagonizes adaptive adjustment of the owl's auditory space map during the initial phase of plasticity. J Neurosci. 21:2001;4356-4365.
63. Foeller E, Celikel T, Feldman DE: Change in the balance between inhibition and excitation during whisker map plasticity in vivo. 2003 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Program No. 58.11, Online.
64. Fox K. A critical period for experience-dependent synaptic plasticity in rat barrel cortex. J Neurosci. 12:1992;1826-1838.
65. A receptor antagonism: implications for cortical reorganization. Exp Brain Res. 136:2001;447-455.