Skip to main content
Log in

Two Cortical Circuits Control Propagating Waves in Visual Cortex

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

Visual stimuli produce waves of activity that propagate across the visual cortex of fresh water turtles. This study used a large-scale model of the cortex to examine the roles of specific types of cortical neurons in controlling the formation, speed and duration of these waves. The waves were divided into three components: initial depolarizations, primary propagating waves and secondary waves. The maximal conductances of each receptor type postsynaptic to each population of neurons in the model was systematically varied and the speed of primary waves, durations of primary waves and total wave durations were measured. The analyses indicate that wave formation and speed are controlled principally by feedforward excitation and inhibition, while wave duration is controlled principally by recurrent excitation and feedback inhibition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Blanton MG, Shen JM, Kriegstein AR (1987) Evidence for the inhibitory neurotransmitter gamma-aminobutyric acid in a spiny and sparsely spiny nonpyramidal neurons of turtle dorsal cortex. J. Comp. Neurol. 259: 277–297.

    Article  CAS  PubMed  Google Scholar 

  • Blanton MG, Kriegstein AR (1992) Properties of amino acid neurotransmitter receptors of embryonic cortical neurons when activated by exogenous and endogenous agonists. J. Neurophysiol. 67: 1185–1200.

    CAS  PubMed  Google Scholar 

  • Bringuier et 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  CAS  PubMed  Google Scholar 

  • Bower JM, Beeman D (1998) The Book of Genesis, 2nd ed. TELOS, New York.

    Google Scholar 

  • Chagnac-Amitai Y, Connors BW (1989) Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61: 747–758.

    CAS  PubMed  Google Scholar 

  • Chervin RD, Pierce PA, Connors BW (1988) Periodicity and directionality in the propagation of epileptiform dischargers across neocortex. J. Neurophysiol. 61: 747–758.

    Google Scholar 

  • Colombe JB, Sylvester J, Block J, Ulinski PS (2004) Subpial and stellate cells: Two populations of interneurons in turtle visual cortex. J. Comp. Neurol. 471: 333–351.

    Article  PubMed  Google Scholar 

  • Colombe JB, Ulinski PS (1999) Temporal dispersion windows in cortical neurons. J. Comput. Neurosci. 17: 3894–3906.

    Google Scholar 

  • Contreras D, Llinás R (2001) Voltage-sensitive dye imaging of neocortical spatiotemporal dynamics to afferent activation frequency. J. Neurosci. 21: 9403–9413.

    CAS  PubMed  Google Scholar 

  • Derdikman D, Hildesheim R, Ahissar E, Arieli A, Grinvald A (2003) Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex. J. Neurosci. 23: 3100–3105.

    CAS  PubMed  Google Scholar 

  • Du X, Ghosh BK, Ulinski PS (2005) Encoding and decoding target locations with waves in the turtle visual cortex. IEEE Trans. Biomed. Eng. 52: 566–577.

    Google Scholar 

  • Ermentrout B (1998) The analysis of synaptically generated traveling waves. J. Comput. Neurosci. 5: 191–208.

    Article  CAS  PubMed  Google Scholar 

  • Ghanzafar AA, Nicoleilis MAL (1999) Spatiotemporal properties of layer V neurons of the rat primary somatosensory cortex. Cerebral Cortex 9: 348–361.

    Google Scholar 

  • Golomb D, Amitai Y (1997) Propagating neuronal discharges in neocortical slices: Computational and experimental study. J. Neurophysiol. 78: 1199–1211.

    CAS  PubMed  Google Scholar 

  • Golomb D, Ermentrout GB (2001) Bistability in pulse propagation in networks of excitatory and inhibitory populations. Phys. Rev. Lett. 86: 4179–4182.

    Article  CAS  PubMed  Google Scholar 

  • Golomb D, Ermentrout GB (2002) Slow excitation supports propagation of slow pulses in networks of excitatory and inhibitory populations. Phys. Rev. E. 65: 061911–061916.

    Article  Google Scholar 

  • Grinvald A, Lieke EE, Frostig RD, Hidesheim R (1994) Cortical point spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex. J. Neurosci. 14: 2545–2568.

    CAS  PubMed  Google Scholar 

  • Heller SB, Ulinski PS (1987) Morphology of geniculocortical axons in turtles of the genera Pseudemys and Chrysemys. Anat. Embryol. 175: 505–515.

    Article  CAS  PubMed  Google Scholar 

  • Kleinfeld D, Delaney KR (1996) Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage-sensitive dyes. J. Comp. Neurol. 375: 89–108.

    Article  CAS  PubMed  Google Scholar 

  • Larson-Prior LJ, Ulinski PS, Slater NT (1991) Excitatory amino acid receptor-mediated transmission in geniculocortical and intracortical pathways within visual cortex. J. Neurophysiol. 66: 293–306.

    CAS  PubMed  Google Scholar 

  • Mancilla JG, Fowler MH, Ulinski PS (1998) Responses of regular spiking and fast spiking cells in turtle visual cortex to light flashes. Vis. Neurosci. 15: 979–993.

    Article  CAS  PubMed  Google Scholar 

  • Mancilla JG, Ulinski PS (2001) Role of GABAA-mediated inhibition in controlling the responses of regular spiking cells in turtle visual cortex. Vis. Neurosci. 18: 9–24.

    Article  CAS  PubMed  Google Scholar 

  • Mulligan K, Ulinski PS (1990) Organization of the geniculocortical projection in turtles: Isoazimuth lamellae in the visual cortex. J. comp. Neurol. 296: 531–547.

    Article  CAS  PubMed  Google Scholar 

  • Nenadic Z, Ghosh BK, Ulinski PS (2002) Modelling and estimation problems in the turtle visual cortex. IEEE Trans. Biomed. Eng. 49: 753–762.

    Article  PubMed  Google Scholar 

  • Nenadic Z, Ghosh BK, Ulinski PS (2003) Propagating waves in visual cortex: A large-scale model of turtle visual cortex. J. Comput. Neurosci. 14: 161–184.

    Article  PubMed  Google Scholar 

  • Petersen CCH, Sakmann B (2001) Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging. J. Neurosci. 21: 8435–8446.

    CAS  PubMed  Google Scholar 

  • Petersen CCH, Grinvald A, Sakmann B (2003) Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J. Neurosci. 23: 1298–1309.

    CAS  PubMed  Google Scholar 

  • Prechtl JC, Bullock TH, Kleinfeld D (2000) Direct evidence for local oscillatory current sources and intracortical phase gradients in turtle visual cortex. Proc. Natl. Acad. Sci. 97: 877–882.

    Article  CAS  PubMed  Google Scholar 

  • Prechtl JC, Cohen LB, Mitra PP, Pesaran B, Kleinfeld D (1997) Visual stimuli induce waves of electrical activity in turtle visual cortex. Proc. Natl. Acad. Sci. 94: 7621–7626.

    Article  CAS  PubMed  Google Scholar 

  • Robbins KA, Senseman DM (2004) Extracting wave structure from biological data with application to responses in turtle visual cortex. J. Comput. Neurosci. 16: 267–298.

    Article  PubMed  Google Scholar 

  • Seidemann E, Arieli A, Grinvald A, Slovin H (2002) Dynamics of depolarization and hyperpolarization in the frontal cortex and saccade goal. Science 305: 862–865.

    Google Scholar 

  • Senseman DM (1999) Spatiotemporal structure of depolarization spread in cortical pyramidal cell populations evoked by diffuse retinal light flashes. Vis. Neurosci. 16: 65–79.

    Article  CAS  PubMed  Google Scholar 

  • Senseman DM, Robbins KA (2002) High-speed VSD imaging of visually evoked cortical waves: decomposition into intra- and intercortical wave motions. J. Neurophysiol. 87: 1499–1514.

    PubMed  Google Scholar 

  • Traub RD, Wong RKS, Miles R, Michelson H (1991) A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J. Neurophysiol. 66: 635–650.

    CAS  PubMed  Google Scholar 

  • Traub RD, Jefferys JGR, Miles R, Michelson H (1993) Analysis of the propagation of disinhibition-induced afer-discharges along the guine-pig hippocampual slice in vitro. J. Physiol. (Lond.) 472: 267–287.

    CAS  Google Scholar 

  • Ulinski PS (1986) Organization of the corticogeniculate projections in the turtle, Pseudemys scripta. J. Comp. Neurol. 254: 529–542.

    Article  CAS  PubMed  Google Scholar 

  • Ulinski PS (1999) Neural mechanisms underlying the analysis of moving visual stimuli. In: Ulinski PS, Jones EG, Peters A, eds. Cerebral Cortex. Vol. 13. Models of Cortical Circuitry. Plenum Press, New York, pp. 283–399.

    Google Scholar 

  • Wang W (2006) Dynamics of the turtle visual cortex and design of sensor networks. D.Sc. thesis. Washington University, Saint Louis, MO.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wenxue Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, W., Campaigne, C., Ghosh, B.K. et al. Two Cortical Circuits Control Propagating Waves in Visual Cortex. J Comput Neurosci 19, 263–289 (2005). https://doi.org/10.1007/s10827-005-2288-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-005-2288-5

Keywords

Navigation