Sensory experience is essential for the refinement of neuronal circuits during development and for learning and memory in the adult brain. Such experience-dependent plasticity is largely mediated by activity-dependent synaptic modification. In this review, we focus on a spike timing-dependent synaptic learning rule, in which the direction and magnitude of synaptic modification depend on the relative spike timing of presynaptic and postsynaptic neurons. We discuss a series of recent studies exploring the functional implications of this learning rule in the visual system. These studies show that temporally patterned visual stimuli can cause rapid changes in visual circuits, neuronal receptive fields, and visual perception, with a temporal specificity of tens of milliseconds. Particularly, motion stimuli that are common in natural scenes may interact strongly with the spike timing-dependent learning rule, leaving distinct marks in the perceptual function of the mature brain.
Abbott LF, Blum KI. 1996. Functional significance of long-term potentiation for sequence learning and prediction. Cereb Cortex6:406-416.
2.
Allen CB, Celikel T, Feldman DE. 2003. Long-term depression induced by sensory deprivation during cortical map plasticity in vivo. Nat Neurosci6:291-299.
3.
Bear MF. 1996. A synaptic basis for memory storage in the cerebral cortex. Proc Natl Acad Sci U S A93:13453-13459.
4.
Bell CC, Han VZ, Sugawara Y, Grant K.1997. Synaptic plasticity in a cerebellum-like structure depends on temporal order. Nature387:278-281.
5.
Ben-Yishai R, Bar-Or RL, Sompolinsky H.1995. Theory of orientation tuning in visual cortex. Proc Natl Acad Sci U S A92:3844-3848.
6.
Bi GQ, Poo MM. 1998. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci18:10464-10472.
7.
Bliss TV, Collingridge GL. 1993. A synaptic model of memory: long-term potentiation in the hippocampus. Nature361:31-39.
8.
Bliss TV, Lomo T.1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol232:331-356.
9.
Boettiger CA, Doupe AJ. 2001. Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron31:809-818.
10.
Buchs NJ, Senn W.2002. Spike-based synaptic plasticity and the emergence of direction selective simple cells: simulation results. J Comp Neurosci13:167-186.
11.
Buonomano DV, Merzenich MM. 1998. Cortical plasticity: from synapses to maps. Annu Rev Neurosci21:149-186.
12.
Celikel T, Szostak VA, Feldman DE. 2004. Modulation of spike timing by sensory deprivation during induction of cortical map plasticity. Nat Neurosci7:534-541.
13.
De Valois RL, De Valois KK. 1991. Vernier acuity with stationary moving Gabors. Vision Res31:1619-1626.
14.
Debanne D, Gahwiler BH, Thompson SM. 1998. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol507 (Pt 1):237-247.
15.
Deneve S, Latham PE, Pouget A.1999. Reading population codes: a neural implementation of ideal observers. Nat Neurosci2:740-745.
16.
Douglas RJ, Koch C, Mahowald M, Martin KA, Suarez HH. 1995. Recurrent excitation in neocortical circuits. Science269:981-985.
17.
Egger V, Feldmeyer D, Sakmann B.1999. Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nat Neurosci2:1098-1105.
18.
Eyding D, Schweigart G, Eysel UT. 2002. Spatio-temporal plasticity of cortical receptive fields in response to repetitive visual stimulation in the adult cat. Neuroscience112:195-215.
19.
Feldman DE. 2000. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron27:45-56.
20.
Felsen G, Shen YS, Yao H, Spor G, Li C, Dan Y.2002. Dynamic modification of cortical orientation tuning mediated by recurrent connections. Neuron36:945-954.
21.
Fregnac Y, Shulz D, Thorpe S, Bienenstock E.1988. A cellular analogue of visual cortical plasticity. Nature333:367-370.
22.
Fregnac Y, Shulz D, Thorpe S, Bienenstock E.1992. Cellular analogs of visual cortical epigenesis. I. Plasticity of orientation selectivity. J Neurosci12:1280-1300.
23.
Froemke RC, Dan Y.2002. Spike-timing-dependent synaptic modification induced by natural spike trains. Nature416:433-438.
24.
Fu YX, Djupsund K, Gao H, Hayden B, Shen K, Dan Y.2002. Temporal specificity in the cortical plasticity of visual space representation. Science296:1999-2003.
25.
Fu YX, Shen Y, Gao H, Dan Y.2004. Asymmetry in visual cortical circuits underlying motion-induced perceptual mislocalization. J Neurosci24:2165-2171.
Gustafsson B, Wigstrom H, Abraham WC, Huang YY. 1987. Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials. J Neurosci7:774-780.
28.
Hebb DO. 1949. Organization of behavior: a neuropsychological theory. New York: John Wiley.
29.
Kempter R, Leibold C, Wagner H, van Hemmen JL. 2001. Formation of temporal-feature maps by axonal propagation of synaptic learning. Proc Natl Acad Sci U S A98:4166-4171.
30.
Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A.2003. Spontaneously emerging cortical representations of visual attributes. Nature425:954-956.
31.
Kirkwood A, Bear MF. 1994. Homosynaptic long-term depression in the visual cortex. J Neurosci14:3404-3412.
32.
Kistler WM, van Hemmen JL. 2000. Modeling synaptic plasticity in conjuction with the timing of pre- and postsynaptic action potentials. Neural Comp12:385-405.
33.
Levy WB, Steward O.1983. Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience8:791-797.
34.
Magee JC, Johnston D.1997. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science275:209-213.
35.
Malenka RC, Nicoll RA. 1999. Long-term potentiation—a decade of progress?Science285:1870-1874.
36.
Markram H, Lubke J, Frotscher M, Sakmann B.1997. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science275:213-215.
37.
Marlin SG, Hasan SJ, Cynader MS. 1988. Direction-selective adaptation in simple and complex cells in cat striate cortex. J Neurophysiol59:1314-1330.
38.
McLean J, Palmer LA. 1998. Plasticity of neuronal response properties in adult cat striate cortex. Vis Neurosci15:177-196.
39.
Mehta MR, Barnes CA, McNaughton BL. 1997. Experience-dependent, asymmetric expansion of hippocampal place fields. Proc Natl Acad Sci U S A94:8918-8921.
40.
Mehta MR, Quirk MC, Wilson MA. 2000. Experience-dependent asymmetric shape of hippocampal receptive fields. Neuron25:707-715.
41.
Miller KD. 1994. A model for the development of simple cell receptive fields and the ordered arrangement of orientation columns through activity-dependent competition between ON- and OFF-center inputs. J Neurosci14:409-441.
42.
Miller KD, Keller JB, Stryker MP. 1989. Ocular dominance column development: analysis and simulation. Science245:605-615.
43.
Mulkey RM, Malenka RC. 1992. Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron9:967-975.
44.
Nishida S, Johnston A.1999. Influence of motion signals on the perceived position of spatial pattern. Nature397:610-612.
45.
Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K.2000. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature408:584-588.
46.
Ramachandran VS, Anstis SM. 1990. Illusory displacement of equiluminous kinetic edges. Perception19:611-616.
47.
Rao RPN, Sejnowski TJ. 2000. Predictive sequence learning in recurrent neocortical circuits. In: Solla SA, Leen TK, Muller KR, editors. Advances in neural information processing systems 12 (NIPS*99). Cambridge, MA: MIT Press. p 164-170.
48.
Schuett S, Bonhoeffer T, Hubener M.2001. Pairing-induced changes of orientation maps in cat visual cortex. Neuron32:325-337.
49.
Shulz D, Fregnac Y.1992. Cellular analogs of visual cortical epigenesis. II. Plasticity of binocular integration. J Neurosci12:1301-1318.
50.
Sillito AM. 1975. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol250:305-329.
51.
Sjostrom PJ, Turrigiano GG, Nelson SB. 2001. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron32:1149-1164.
52.
Snowden RJ. 1998. Shifts in perceived position following adaptation to visual motion. Curr Biol8:1343-1345.
53.
Softky WR, Koch C.1993. The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs. J Neurosci13:334-350.
54.
Somers DC, Nelson SB, Sur M.1995. An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci15:5448-5465.
55.
Song S, Abbott LF. 2001. Cortical development and remapping through spike timing-dependent plasticity. Neuron32:339-350.
56.
Song S, Miller KD, Abbott LF. 2000. Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci3:919-926.
57.
Treue S, Hol K, Rauber HJ. 2000. Seeing multiple directions of motion-physiology and psychophysics. Nat Neurosci3:270-276.
58.
Whitaker D, McGraw PV, Pearson S.1999. Non-veridical size perception of expanding and contracting objects. Vision Res39: 2999-3009.
59.
Wiesel TN, Hubel DH. 1965. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol28:1029-1040.
60.
Woodin MA, Ganguly K, Poo MM. 2003. Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl-transporter activity. Neuron39:807-820.
61.
Yao H, Dan Y.2001. Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron32:315-323.
62.
Yao H, Shen Y, Dan Y.2004. Intracortical mechanism of stimulus-timing-dependent plasticity in visual cortical orientation tuning. Proc Natl Acad Sci U S A101:5081-5086.
63.
Zhang LI, Tao HW, Holt CE, Harris WA, Poo M.1998. A critical window for cooperation and competition among developing retinotectal synapses. Nature395:37-44.
64.
Zhou Q, Tao HW, Poo MM. 2003. Reversal and stabilization of synaptic modifications in a developing visual system. Science300:1953-1957.
