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Spontaneously emerging direction selectivity maps in visual cortex through STDP

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Abstract

It is still an open question as to whether, and how, direction-selective neuronal responses in primary visual cortex are generated by feedforward thalamocortical or recurrent intracortical connections, or a combination of both. Here we present an investigation that concentrates on and, only for the sake of simplicity, restricts itself to intracortical circuits, in particular, with respect to the developmental aspects of direction selectivity through spike-timing-dependent synaptic plasticity. We show that directional responses can emerge in a recurrent network model of visual cortex with spiking neurons that integrate inputs mainly from a particular direction, thus giving rise to an asymmetrically shaped receptive field. A moving stimulus that enters the receptive field from this (preferred) direction will activate a neuron most strongly because of the increased number and/or strength of inputs from this direction and since delayed isotropic inhibition will neither overlap with, nor cancel excitation, as would be the case for other stimulus directions. It is demonstrated how direction-selective responses result from spatial asymmetries in the distribution of synaptic contacts or weights of inputs delivered to a neuron by slowly conducting intracortical axonal delay lines. By means of spike-timing-dependent synaptic plasticity with an asymmetric learning window this kind of coupling asymmetry develops naturally in a recurrent network of stochastically spiking neurons in a scenario where the neurons are activated by unidirectionally moving bar stimuli and even when only intrinsic spontaneous activity drives the learning process. We also present simulation results to show the ability of this model to produce direction preference maps similar to experimental findings

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References

  • Anderson JC., Binzegger T., Kahana O., Martin KAC., Segev I. (1999). Dendritic asymmetry cannot account for directional responses of neurons in visual cortex. Nature 2(9):820–824

    CAS  Google Scholar 

  • Banton T., Bertenthal BI., Seaks J. (1999). Infants sensitivity to statistical distributions of motion direction and speed. Vision Research 39:3417–3430

    Article  PubMed  CAS  Google Scholar 

  • Bartsch AP., van Hemmen JL. (2001). Combined hebbian development of geniculocortical and lateral connectivity in a model of primary visual cortex. Biological Cybernetics 84(1):41–55

    Article  PubMed  CAS  Google Scholar 

  • Bi G., Poo M. (1998). Synaptic modifications in cultured hippocampal neurons: Dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18(24):10464–10472

    PubMed  CAS  Google Scholar 

  • Bringuier V., Chavane F., Glaeser L., Fregnac Y. (1999). Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283:695–699

    Article  PubMed  CAS  Google Scholar 

  • Buchs N., Senn W. (2002). Spike-based synaptic plasticity and the emergence of direction selective simple cells: simulation results. J Comput Neurosci 13(3):167–186

    Article  PubMed  CAS  Google Scholar 

  • Chapman B., Stryker MP., Bonhoeffer T. (1996). Development of orientation preference maps in ferret primary visual cortex. J Neurosci 16(20):6443–6453

    PubMed  CAS  Google Scholar 

  • Clifford CWG., Ibbotson MR. (2003). Fundamental mechanisms of visual motion detection: Models, cells and functions. Progress in Neurobiology 68:409–437

    Article  Google Scholar 

  • Crair MC., Gillespie DC., Stryker MP. (1998). The role of visual experience in the development of columns in cat visual cortex. Science 279(5350):566–570

    Article  PubMed  CAS  Google Scholar 

  • Engert F., Tao HW., Zhang LI., Poo M. (2002). Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons. Nature 419:470–475

    Article  PubMed  CAS  Google Scholar 

  • Feidler JC., Saul AB., Murthy A., Humphrey AL. (1997). Hebbian learning and the development of direction selectivity: the role of geniculate response timings. Network: Comput Neural Syst 8:195–214

    Article  Google Scholar 

  • Feldman DE. (2000). Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27:45–56

    Article  PubMed  CAS  Google Scholar 

  • Ferster D., Miller KD. (2000). Neural mechanisms of orientation selectivity in the visual cortex. Annual Reviews of Neurosci 23:441–471

    Article  CAS  Google Scholar 

  • Froemke RC., Dan Y. (2002). Spike-timing-dependent synaptic modification induced by natural spike trains. Nature 416:433–438

    Article  PubMed  CAS  Google Scholar 

  • Fu Y., Shen Y., Gao H., Dan Y. (2004). Asymmetry in visual cortical circuits underlying motion-induced perceptual mislocalization. J Neurosci 24(9):2165–2171

    Article  PubMed  CAS  Google Scholar 

  • Gerstner W., Kempter R., van Hemmen JL., Wagner H. (1996). A neuronal learning rule for sub-millisecond temporal coding. Nature 383(6595):76–81

    Article  PubMed  CAS  Google Scholar 

  • Gerstner W., van Hemmen JL. (1994). Models of Neural Networks II. Coding and Information Processing in Neural Networks, Springer, pp. 1–93

  • Issa NP., Trachtenberg JT., Chapman B., Zahs KR., Stryker MP. (1999). The critical period for ocular dominance plasticity in the ferret’s visual cortex. J Neurosci 19(16):6965–6978

    PubMed  CAS  Google Scholar 

  • Katz LC., Shatz CJ. (1996). Synaptic activity and the construction of cortical circuits. Science 274:1133–1138

    Article  PubMed  CAS  Google Scholar 

  • Kempter R., Gerstner W., van Hemmen JL. (1999) Spike-based compared to rate-based Hebbian learning. In: Adv. in Neural Information Processing Systems, vol 11

  • Livingstone MS. (1998). Mechanisms of direction selectivity in macaque V1. Neuron 20:509–526

    Article  PubMed  CAS  Google Scholar 

  • Markram H., Lübke J., Sakmann B. (1997). Regulation of synaptic efficacy by coincidence of postsynaptic aps and epsps. Science 275(5297):213–215

    Article  PubMed  CAS  Google Scholar 

  • Mehta MR., Wilson MA. (2000). From hippocampus to V1: Effect of LTP on spatiotemporal dynamics of receptive fields. Neurocomputing 32:905–911

    Article  Google Scholar 

  • Mineiro P., Zipser D. (1998). Analysis of direction selectivity arising from recurrent cortical interactions. Neural Computation 10:353–371

    Article  PubMed  CAS  Google Scholar 

  • Ngezahayo A., Schachner M., Artola A. (2000). Synaptic activity modulates the induction of bidirectional synaptic changes in adult mouse hippocampus. J Neurosci (7):2451–2458

    Google Scholar 

  • Noll J., Wenisch OG., van Hemmen JL. (2002). Simulation of Neuronal Map Formation in the Primary Visual Cortex. High Performance Computing in Science and Engineering. Springer, pp 135–142

  • Rao RP., Sejnowski TJ. (2001). Predictive learning of temporal sequences in recurrent neocortical circuits. Novartis Found Symposium 239:208–229

    Article  CAS  Google Scholar 

  • Roerig B., Chen B., Kao JP. (2003). Different inhibitory synaptic input patterns in exc. and inhib layer 4 neurons of ferret visual cortex. Cereb Cortex 13(4):350–363

    Article  PubMed  Google Scholar 

  • Roerig B., Kao J. (1999). Organization of intracortical circuits in relation to direction preference maps in ferret visual cortex. J Neuronsci 24(19):RC44

    Google Scholar 

  • Sabatini SP., Solari F. (1999). An architectural hypothesis for direction selectivity in the visual cortex: The role of spatially asymmetric intracortical inhibition. Biological Cybernetics 80(3):171–183

    Article  PubMed  CAS  Google Scholar 

  • Schütt S., Bonhoeffer T., Hübener M. (2001). Pairing-induced changes of orientation maps in cat visual cortex. Neuron 32:325–337

    Article  Google Scholar 

  • Senn W., Schneider M., Ruf B. (2002). Activity-dependent development of axonal and dendritic delays, or, why synaptic transmission should be unreliable. Neural Computation 14:583–619

    Article  PubMed  Google Scholar 

  • Shmuel A., Grinvald A. (1996). Functional organization for direction of motion and its relationship to orientation maps in cat area 18. J Neurosci 16(21):6945–6964

    PubMed  CAS  Google Scholar 

  • Shon AP., Rao RPN., Sejnowski TJ. (2004). Motion detection and prediction through spike-timing dependent plasticity. Network: Comput Neural Syst 15:179–198

    Article  CAS  Google Scholar 

  • Suarez H., Koch C., Douglas R. (1995). Modeling direction selectivity of simple cells in striate visual cortex within the framework of the canonical microcircuit. J Neurosci 15(10):6700–6719

    PubMed  CAS  Google Scholar 

  • Sur M., Leamey CA. (2001). Development and plasticity of cortical areas and networks. Nature Reviews—Neuroscience. 2(4): 251–262

    PubMed  CAS  Google Scholar 

  • Weliky M., Bosking WH., Fitzpatrick D. (1996). A systematic map of direction preference in primary visual cortex. Nature 379(6567):725–728

    Article  PubMed  CAS  Google Scholar 

  • Wimbauer S., Wenisch OG., Miller KD., van Hemmen JL. (1997). Development of spatiotemporal receptive fields of simple cells: I. model formulation. Biological Cybernetics 77:453–461

    Article  PubMed  CAS  Google Scholar 

  • Yao H., Shen Y., Dan Y. (2004). Intracortical mechanism of stimulus-timing-dependent plasticity in visual cortical orientation tuning. In: Proceeding of the National Academy of Sciences 101:35081–5086

    Google Scholar 

  • Zhang LI., Tao HW., Holt CE., Harris WA., Poo M-M. (1998). A critical window for cooperation and competition among developing retinotectal synapses. Nature 395:37–44

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Oliver G. Wenisch.

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Wenisch, O.G., Noll, J. & Hemmen, J.L.v. Spontaneously emerging direction selectivity maps in visual cortex through STDP. Biol Cybern 93, 239–247 (2005). https://doi.org/10.1007/s00422-005-0006-z

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  • DOI: https://doi.org/10.1007/s00422-005-0006-z

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