Functional elimination of excitatory feedforward inputs underlies developmental refinement of visual receptive fields in zebrafish

Journal of Neuroscience

Volumn 31, Issue 14, 2011, Pages 5460-5469

  Zhang, Min ^a   Liu, Yan ^a   Wang, Sheng zhi ^a   Zhong, Wen ^c   Liu, Bao hua ^a   Tao, Huizhong Whit ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c GUANGDONG PROVINCIAL HOSPITAL OF CHINESE MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPUTER SIMULATION; CONTROLLED STUDY; EMBRYO; EXCITATORY POSTSYNAPTIC POTENTIAL; EYE DEVELOPMENT; FEMALE; MALE; NERVE CELL DIFFERENTIATION; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL; RETINA GANGLION CELL; RETINA RECEPTIVE FIELD; RETINOTECTAL PROJECTION; SPIKE WAVE; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; VOLTAGE CLAMP; ZEBRA FISH;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BIOPHYSICS; BRAIN MAPPING; COMPUTER SIMULATION; ELECTRIC STIMULATION; FUNCTIONAL LATERALITY; GABA ANTAGONISTS; MODELS, NEUROLOGICAL; MORPHOLINES; NERVE NET; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PHOTIC STIMULATION; RETINAL GANGLION CELLS; SENSORY RECEPTOR CELLS; SUPERIOR COLLICULI; SYNAPTIC TRANSMISSION; VISUAL FIELDS; ZEBRAFISH;

EID: 79955727151     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6220-10.2011     Document Type: Article

References (46)

1. Akerman CJ, Cline HT (2006) Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. J Neurosci 26:5117-5130.
2. Antonini A, Stryker MP (1993) Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade. J Neurosci 13:3549-3573.
3. Baier H (2000) Zebrafish on the move: towards a behavior-genetic analysis of vertebrate vision. Curr Opin Neurobiol 10:451-455.
4. Ben-Ari Y (2002) Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 3:728-739.
5. Bureau I, Shepherd GM, Svoboda K (2004) Precise development of functional and anatomical columns in the neocortex. Neuron 42:789-801.
6. Chen C, Regehr WG (2000) Developmental remodeling of the retinogeniculate synapse. Neuron 28:955-966.
7. Dong W, Lee RH, Xu H, Yang S, Pratt KG, Cao V, Song YK, Nurmikko A, Aizenman CD (2009) Visual avoidance in Xenopus tadpoles is correlated with the maturation of visual responses in the optic tectum. J Neurophysiol 101:803-815.
8. Ebihara S, Shirato K, Harata N, Akaike N (1995) Gramicidin-perforated patch recording: GABA response in mammalian neurones with intact intracellular chloride. J Physiol 484:77-86.
9. Engert F, Tao HW, Zhang LI, Poo MM (2002) Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons. Nature 419: 470-475.
10. Fagiolini M, Pizzorusso T, Berardi N, Domenici L, Maffei L (1994) Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res 34:709-720.
11. Hooks BM, Chen C (2006) Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse. Neuron 52:281-291.
12. Huang L, Pallas SL (2001) NMDA antagonists in the superior colliculus prevent developmental plasticity but not visual transmission or map compression. J Neurophysiol 86:1179-1194.
13. Katz LC, Shatz CJ (1996) Synaptic activity and the construction of cortical circuits. Science 274:1133-1138.
14. Liu BH, Wu GK, Arbuckle R, Tao HW, Zhang LI (2007) Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci 10:1594-1600.
15. Liu BH, Li P, Sun YJ, Li YT, Zhang LI, Tao HW (2010) Intervening inhibition underlies simple-cell receptive field structure in visual cortex. Nat Neurosci 13:89-96.
16. Liu Y, Zhang LI, Tao HW (2007) Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage. J Neurosci 27:5301-5312.
17. Mata ML, Ringach DL (2005) Spatial overlap of ON and OFF subregions and its relation to response modulation ratio in macaque primary visual cortex. J Neurophysiol 93:919-928.
18. McLaughlin T, Torborg CL, Feller MB, O'Leary DD (2003) Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 40:1147-1160.
19. Meyer MP, Smith SJ (2006) Evidence from in vivo imaging that synaptogenesis guides the growth and branching of axonal arbors by two distinct mechanisms. J Neurosci 26:3604-3614.
20. Nakamura H, O'Leary DD (1989) Inaccuracies in initial growth and arborization of chick retinotectal axons followed by course corrections and axon remodeling to develop topographic order. J Neurosci 9:3776-3795.
21. Niell CM, Smith SJ (2005) Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron 45:941-951.
22. Niell CM, Meyer MP, Smith SJ (2004) In vivo imaging of synapse formation on a growing dendritic arbor. Nat Neurosci 7:254-260.
23. Owens DF, Kriegstein AR (2002) Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3:715-727.
24. Pratt KG, Aizenman CD (2007) Homeostatic regulation of intrinsic excitability and synaptic transmission in a developing visual circuit. J Neurosci 27:8268-8277.
25. Pratt KG, Dong W, Aizenman CD (2008) Development and spike timingdependent plasticity of recurrent excitation in the Xenopus optic tectum. Nat Neurosci 11:467-475.
26. Priebe NJ, Ferster D (2008) Inhibition, spike threshold, and stimulus selectivity in primary visual cortex. Neuron 57:482-497.
27. Priebe NJ, Mechler F, Carandini M, Ferster D (2004) The contribution of spike threshold to the dichotomy of cortical simple and complex cells. Nat Neurosci 7:1113-1122.
28. Ramdya P, Engert F (2008) Emergence of binocular functional properties in a monocular neural circuit. Nat Neurosci 11:1083-1090.
29. Ruthazer ES, Cline HT (2004) Insights into activity-dependent map formation from the retinotectal system: a middle-of-the-brain perspective. J Neurobiol 59:134-146.
30. Sakaguchi DS, Murphey RK (1985) Map formation in the developing Xenopus retinotectal system: an examination of ganglion cell terminal arborizations. J Neurosci 5:3228-3245.
31. Sanes DH, Constantine-Paton M (1985) The sharpening of frequency tuning curves requires patterned activity during development in the mouse, Mus musculus. J Neurosci 5:1152-1166.
32. Schmidt JT, Buzzard M, Borress R, Dhillon S (2000) MK801 increases retinotectal arbor size in developing zebrafish without affecting kinetics of branch elimination and addition. J Neurobiol 42:303-314.
33. Simon DK, O'Leary DD (1992) Development of topographic order in the mammalian retinocollicular projection. J Neurosci 12:1212-1232.
34. Smear MC, Tao HW, Staub W, Orger MB, Gosse NJ, Liu Y, Takahashi K, Poo MM, Baier H (2007) Vesicular glutamate transport at a central synapse limits the acuity of visual perception in zebrafish. Neuron 53:65-77.
35. Spruston N, Jaffe DB, Williams SH, Johnston D (1993) Voltage- and spaceclamp errors associated with the measurement of electrotonically remote synaptic events. J Neurophysiol 70:781-802.
36. Sun YJ, Wu GK, Liu BH, Li P, Zhou M, Xiao Z, Tao HW, Zhang LI (2010) Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development. Nature 465:927-931.
37. Tan AY, Zhang LI, Merzenich MM, Schreiner CE (2004) Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J Neurophysiol 92:630-643.
38. Tao HW, Poo MM (2005) Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45:829-836.
39. Tavazoie SF, Reid RC (2000) Diverse receptive fields in the lateral geniculate nucleus during thalamocortical development. Nat Neurosci 3:608-616.
40. Troyer TW, Krukowski AE, Priebe NJ, Miller KD (1998) Contrast-invariant orientation tuning in cat visual cortex: thalamocortical input tuning and correlation-based intracortical connectivity. J Neurosci 18:5908-5927.
41. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446.
42. Westerfield M (1993) The zebrafish book. Eugene, OR: Institute of Neuroscience, University of Oregon.
43. Wu GK, Arbuckle R, Liu BH, Tao HW, Zhang LI (2008) Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 58:132-143.
44. Xiao T, Roeser T, Staub W, Baier H (2005) A GFP-based genetic screen reveals mutations that disrupt the architecture of the zebrafish retinotectal projection. Development 132:2955-2967.
45. Zhang LI, Poo MM (2001) Electrical activity and development of neural circuits. Nat Neurosci 4:1207-1214.
46. Zhang LI, Bao S, Merzenich MM (2001) Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci 4:1123-1130.