GABAergic circuits control stimulus-instructed receptive field development in the optic tectum

Nature Neuroscience

Volumn 13, Issue 9, 2010, Pages 1098-1106

  Richards, Blake A ^a   Voss, Oliver P ^a   Akerman, Colin J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; GABAERGIC SYSTEM; GABAERGIC TRANSMISSION; LEARNING; NERVE CELL PLASTICITY; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL; RECEPTIVE FIELD; SIGNAL TRANSDUCTION; SPIKE WAVE; VISUAL STIMULATION; XENOPUS LAEVIS; ACTION POTENTIAL; ANIMAL; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; MOTION; MOVEMENT PERCEPTION; NERVE CELL; NERVE TRACT; PATCH CLAMP TECHNIQUE; PHOTOSTIMULATION; PHYSIOLOGY; SIGNAL PROCESSING; SUPERIOR COLLICULUS; SYNAPTIC TRANSMISSION; TIME;

ACTION POTENTIALS; ANIMALS; GAMMA-AMINOBUTYRIC ACID; LARVA; MOTION; MOTION PERCEPTION; NEURAL PATHWAYS; NEURONS; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; RECEPTORS, GABA-A; SIGNAL PROCESSING, COMPUTER-ASSISTED; SUPERIOR COLLICULI; SYNAPTIC TRANSMISSION; TIME FACTORS; XENOPUS LAEVIS; GABA-A RECEPTOR ANTAGONISTS;

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT;

EID: 77956189503     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2612     Document Type: Article

References (50)

1. Goodman, C.S. & Shatz, C.J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72, 77-98 (1993).
2. Katz, L.C. & Shatz, C.J. Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138 (1996).
3. Wiesel, T.N. & Hubel, D.H. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003-1017 (1963).
4. Stryker, M.P. Evidence for a possible role for spontaneous electrical activity in the development of the mammalian visual cortex. in Problems and Concepts in Developmental Neurophysiology (eds. Kellaway, P. & Noebels, J.L.) 110-130 (John Hopkins University Press, Baltimore, 1989).
5. Weliky, M. & Katz, L.C. Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386, 680-685 (1997).
6. Engert, F., Tao, H.W., Zhang, L.I. & Poo, M. Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons. Nature 419, 470-475 (2002).
7. Li, Y., Van Hooser, S.D., Mazurek, M., White, L.E. & Fitzpatrick, D. Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456, 952-956 (2008).
8. Meliza, C.D. & Dan, Y. Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking. Neuron 49, 183-189 (2006).
9. Sengpiel, F., Stawinski, P. & Bonhoeffer, T. Influence of experience on rientation maps in cat visual cortex. Nat. Neurosci. 2, 727-732 (1999).
10. Vislay-Meltzer, R.L., Kampff, A.R. & Engert, F. Spatiotemporal specificity of neuronal activity directs the modification of receptive fields in the developing retinotectal system. Neuron 50, 101-114 (2006).
11. Mu, Y. & Poo, M. Spike timing-dependent LTP/LTD mediates visual experience-dependent plasticity in a developing retinotectal system. Neuron 50, 115-125 (2006).
12. Schuett, S., Bonhoeffer, T. & H'bener, M. Pairing-induced changes of orientation maps in cat visual cortex. Neuron 32, 325-337 (2001).
13. Shon, A.P., Rao, R.P.N. & Sejnowski, T.J. Motion detection and prediction through spike-timing dependent plasticity. Network 15, 179-198 (2004).
14. Wenisch, O.G., Noll, J. & Hemmen, J. Spontaneously emerging direction selectivity maps in visual cortex through STDP. Biol. Cybern. 93, 239-247 (2005).
15. Weliky, M. Correlated neuronal activity and visual cortical development. Neuron 27, 427-430 (2000).
16. Ramoa, A.S., Paradiso, M.A. & Freeman, R.D. Blockade of intracortical inhibition in kitten striate cortex: effects on receptive field properties and associated loss of ocular dominance plasticity. Exp. Brain Res. 73, 285-296 (1988).
17. Gabernet, L., Jadhav, S.P., Feldman, D.E., Carandini, M. & Scanziani, M. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48, 315-327 (2005).
18. Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feedforward inhibition. Science 293, 1159-1163 (2001).
19. Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442-446 (2003).
20. Cobb, S.R., Buhl, E.H., Halasy, K., Paulsen, O. & Somogyi, P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75-78 (1995).
21. Akerman, C.J. & Cline, H.T. Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. J. Neurosci. 26, 5117-5130 (2006).
22. Dunning, D.D., Hoover, C.L., Soltesz, I., Smith, M.A. & O'Dowd, D.K. GABAA receptor-mediated miniature postsynaptic currents and alpha-subunit expression in developing cortical neurons. J. Neurophysiol. 82, 3286-3297 (1999).
23. Hollrigel, G.S. & Soltesz, I. Slow kinetics of miniature IPSCs during early postnatal development in granule cells of the dentate gyrus. J. Neurosci. 17, 5119-5128 (1997).
24. Liu, Y., Zhang, L.I. & Tao, H.W. Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage. J. Neurosci. 27, 5301-5312 (2007).
25. Tao, H.W. & Poo, M. Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45, 829-836 (2005).
26. Tyzio, R. et al. The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J. Neurosci. 19, 10372-10382 (1999).
27. Luhmann, H.J. & Prince, D.A. Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol. 65, 247-263 (1991).
28. Mueller, A.L., Taube, J.S. & Schwartzkroin, P.A. Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to gamma-aminobutyric acid in rabbit hippocampus studied in vitro. J. Neurosci. 4, 860-867 (1984).
29. Zhang, L.I., Tao, H.W. & Poo, M. Visual input induces long-term potentiation of developing retinotectal synapses. Nat. Neurosci. 3, 708-715 (2000).
30. Zhang, L.I., Tao, H.W., Holt, C.E., Harris, W.A. & Poo, M. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395, 37-44 (1998).
31. Gao, X.B. & Van Den Pol, A.N. GABA, not glutamate, a primary transmitter driving action potentials in developing hypothalamic neurons. J. Neurophysiol. 85, 425-434 (2001).
32. Staley, K.J. & Mody, I. Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor-mediated postsynaptic conductance. J. Neurophysiol. 68, 197-212 (1992).
33. Ulrich, D. Differential arithmetic of shunting inhibition for voltage and spike rate in neocortical pyramidal cells. Eur. J. Neurosci. 18, 2159-2165 (2003).
34. Gulledge, A.T. & Stuart, G.J. Excitatory actions of GABA in the cortex. Neuron 37, 299-309 (2003).
35. Chen, G., Trombley, P.Q. & van den Pol, A.N. Excitatory actions of GABA in developing rat hypothalamic neurones. J. Physiol. (Lond.) 494, 451-464 (1996).
36. Pratt, K.G., Dong, W. & Aizenman, C.D. Development and spike timing-dependent plasticity of recurrent excitation in the Xenopus optic tectum. Nat. Neurosci. 11, 467-475 (2008).
37. Holt, C.E. & Harris, W.A. Order in the initial retinotectal map in Xenopus: a new technique for labeling growing nerve fibres. Nature 301, 150-152 (1983).
38. Froemke, R.C. & Dan, Y. Spike timing-dependent synaptic modification induced by natural spike trains. Nature 416, 433-438 (2002).
39. Sjöström, P.J., Turrigiano, G.G. & Nelson, S.B. Rate, timing and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149-1164 (2001).
40. Wulff, P. et al. Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat. Neurosci. 12, 1042-1049 (2009).
41. Akerman, C.J. & Cline, H.T. Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci. 30, 382-389 (2007).
42. Pavlov, I., Riekki, R. & Taira, T. Synergistic action of GABAA and NMDA receptors in the induction of long-term depression in glutamatergic synapses in the newborn rat hippocampus. Eur. J. Neurosci. 20, 3019-3026 (2004).
43. Wang, D.D. & Kriegstein, A.R. GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J. Neurosci. 28, 5547-5558 (2008).
44. Hensch, T.K. et al. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504-1508 (1998).
45. Nieuwkoop, P.D. & Faber, J. Normal Table of Xenopus laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg till the End of Metamorphosis (North-Holland Pub., Amsterdam, 1967).
46. Khawaled, R., Bruening-Wright, A., Adelman, J.P. & Maylie, J. Bicuculline block of small-conductance calcium-activated potassium channels. Pflugers Arch. 438, 314-321 (1999).
47. Niell, C.M. & Smith, S.J. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron 45, 941-951 (2005).
48. Dayan, P. & Abbott, L.F. Neural encoding I: firing rates and spike statistics. in Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems (eds. Sejnowski, T.J. & Poggio, T.) 3-44 (MIT Press, Cambridge, Massachusetts, 2003).
49. Song, S., Miller, K.D. & Abbott, L.F. Competitive Hebbian learning through spike timing-dependent synaptic plasticity. Nat. Neurosci. 3, 919-926 (2000).
50. Tao, H.W., Zhang, L.I., Engert, F. & Poo, M. Emergence of input specificity of LTP during development of retinotectal connections in vivo. Neuron 31, 569-580 (2001).