Skip to main content
SpringerLink
Log in

Integrating Top-Down and Bottom-Up Sensory Processing by Somato-Dendritic Interactions

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

Abstract

The classical view of cortical information processing is that of a bottom-up process in a feedforward hierarchy. However, psychophysical, anatomical, and physiological evidence suggests that top-down effects play a crucial role in the processing of input stimuli. Not much is known about the neural mechanisms underlying these effects. Here we investigate a physiologically inspired model of two reciprocally connected cortical areas. Each area receives bottom-up as well as top-down information. This information is integrated by a mechanism that exploits recent findings on somato-dendritic interactions. (1) This results in a burst signal that is robust in the context of noise in bottom-up signals. (2) Investigating the influence of additional top-down information, priming-like effects on the processing of bottom-up input can be demonstrated. (3) In accordance with recent physiological findings, interareal coupling in low-frequency ranges is characteristically enhanced by top-down mechanisms. The proposed scheme combines a qualitative influence of top-down directed signals on the temporal dynamics of neuronal activity with a limited effect on the mean firing rate of the targeted neurons. As it gives an account of the system properties on the cellular level, it is possible to derive several experimentally testable predictions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adelson EH (1993) Perceptual organization and the judgment of brightness. Science 262:2042–2044.

    Google Scholar 

  • Bar M, Ullman S (1996) Spatial context in recognition. Perception 25:343–352.

    Google Scholar 

  • Budd JM (1998) Extrastriate feedback to primary visual cortex in primates: A quantitative analysis of connectivity. Proc. R. Soc. Lond. B. Biol. Sci. 265:1037–1044.

    Google Scholar 

  • Buzsaki G, Kandel A (1998) Somadendritic backpropagation of action potentials in cortical pyramidal cells of the awake rat. J. Neurophysiol. 79:1587–1591.

    Google Scholar 

  • Buzsaki G, Penttonen M, Nadasdy Z, Bragin A (1996) Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc. Natl. Acad. Sci. USA 93:9921–9925.

    Google Scholar 

  • Carpenter G, Grossberg S (1987) A massively parallel architecture for a self-organizing neural pattern recognition machine. Comp. Vision Graphics Image Proc. 37:54–115.

    Google Scholar 

  • Connors BW (1992) GABAA-and GABAB-mediated processes in visual cortex. Prog. Brain Res. 90:335–348.

    Google Scholar 

  • Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Ann. Rev. Neurosci. 18:193–222.

    Google Scholar 

  • Downing CJ (1988) Expectancy and visual-spatial attention: Effects on perceptual quality. J. Exp. Psychol. Hum. Percept. Perform. 14:188–202.

    Google Scholar 

  • Driver J, Spence C (1998) Cross-modal links in spatial attention. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 353:1319–1331.

    Google Scholar 

  • Felleman DJ, Van Essen DC (1991) Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1:1–47.

    Google Scholar 

  • Finkel LH, Edelman GM (1989) Integration of distributed cortical systems by reentry: A computer simulation of interactive functionally segregated visual areas. J. Neurosci. 9:3188–3208.

    Google Scholar 

  • Goebel R, Khorram-Sefat D, Muckli L, Hacker H, Singer W (1998) The constructive nature of vision: Direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery. Eur. J. Neurosci. 10:1563–1573.

    Google Scholar 

  • Grossberg S (1980) How does a brain build a cognitive code? Psychol. Rev. 87:1–51.

    Google Scholar 

  • Hupe JM, James AC, Payne BR, Lomber SG, Girard P, Bullier J (1998) Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons. Nature 394:784–787.

    Google Scholar 

  • Johnson RR, Burkhalter A (1997) A polysynaptic feedback circuit in rat visual cortex. J. Neurosci. 17:7129–7140.

    Google Scholar 

  • Kim U, Sanchez-Vives MV, McCormick DA (1997) Functional dynamics of GABAergic inhibition in the thalamus. Science 278:130–134.

    Google Scholar 

  • Koch C, Poggio T (1992) Multiplying with Synapses and Neurons. In: McKenna T, Davis J, Zornetzer SF, eds. Single Neuron Computation. Academic Press, San Diego. pp. 315–345.

    Google Scholar 

  • König P, Luksch H (1998) Active sensing: Closing multiple loops. Z. Naturforsch. [C.] 53:542–549.

    Google Scholar 

  • Kosslyn SM, Thompson WL, Kim IJ, Alpert NM (1995) Topographical representations of mental images in primary visual cortex. Nature 378:496–498.

    Google Scholar 

  • Lamme VA (1995) The neurophysiology of figure-ground segregation in primary visual cortex. J. Neurosci. 15:1605–1615.

    Google Scholar 

  • Lamme VA, Super H, Spekreijse H (1998) Feedforward, horizontal, and feedback processing in the visual cortex. Curr. Opin. Neurobiol. 8:529–535.

    Google Scholar 

  • Larkum ME, Zhu JJ, Sakmann B (1999) A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 3</del>98:338–341.

    Google Scholar 

  • Lavie N, Driver J (1996) On the spatial extent of attention in object-based visual selection. Percept. Psychophys. 58:1238–1251.

    Google Scholar 

  • Le Bihan D, Turner R, Zeffiro TA, Cuenod CA, Jezzard P, Bonnerot V (1993) Activation of human primary visual cortex during visual recall: A magnetic resonance imaging study. Proc. Natl. Acad. Sci. USA 90:11802–11805.

    Google Scholar 

  • Lisman JE (1997) Bursts as a unit of neural information: Making unreliable synapses reliable. Trends. Neurosci. 20:38–43.

    Google Scholar 

  • Livingstone MS, Freeman DC, Hubel DH (1996) Visual responses in V1 of freely viewing monkeys. Cold Spring Harb. Symp. Quant. Biol. 61:27–37.

    Google Scholar 

  • Luck SJ, Chelazzi L, Hillyard SA, Desimone R (1997) Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J. Neurophysiol. 77:24–42.

    Google Scholar 

  • Mignard M, Malpeli JG (1991) Paths of information flow through visual cortex. Science 251:1249–1251.

    Google Scholar 

  • Moran J, Desimone R (1985) Selective attention gates visual processing in the extrastriate cortex. Science 229:782–784.

    Google Scholar 

  • Mumford D (1992) On the computational architecture of the neocortex. II. The role of cortico-cortical loops. Biol. Cybern. 66:241–251.

    Google Scholar 

  • Oram MW, Perrett DI (1994) Modeling visual recognition from neurobiological constraints. Neural Networks 7: 945–972.

    Google Scholar 

  • Posner MI, Petersen SE (1990) The attention system of the human brain. Ann. Rev. Neurosci. 13:25–42.

    Google Scholar 

  • Rao RPM (1999) An optimal estimation approach to visual perception and learning. Vision Res. 39:1963–1989.

    Google Scholar 

  • Rao RPN, Ballard DH (1997) Dynamic model of visual recognition predicts neural response properties in the visual cortex. Neural Comp. 9:721–763.

    Google Scholar 

  • Rockland KS, Virga A (1989) Terminal arbors of individual “feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris-leucoagglutinin. J. Comp. Neurol. 285:54–72.

    Google Scholar 

  • Roelfsema PR, Lamme VA, Spekreijse H (1998) Object-based attention in the primary visual cortex of the macaque monkey. Nature 395:376–381.

    Google Scholar 

  • Salin PA, Bullier J (1995) Corticocortical connections in the visual system: Structure and function. Physiol. Rev. 75:107–154.

    Google Scholar 

  • Salin PA, Girard P, Bullier J (1993) Visuotopic organization of corticocortical connections in the visual system. Prog. Brain Res. 95:169–178.

    Google Scholar 

  • Sandell JH, Schiller PH (1982) Effect of cooling area 18 on striate cortex cells in the squirrel monkey. J. Neurophysiol. 48:38–48.

    Google Scholar 

  • Schiller J, Schiller Y, Stuart G, Sakmann B (1997) Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons. J. Physiol. (Lond.) 505:605–616.

    Google Scholar 

  • Stins JF, van Leeuwen C (1993) Context influence on the perception of figures as conditional upon perceptual organization strategies. Percept. Psychophys. 53:34–42.

    Google Scholar 

  • Stuart G, Schiller J, Sakmann B (1997a) Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. (Lond.) 505:617–632.

    Google Scholar 

  • Stuart G, Spruston N, Sakmann B, Hausser M (1997b) Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20:125–131.

    Google Scholar 

  • Stuart G, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69–72.

    Google Scholar 

  • Tsubokawa H, Ross WN (1997) Muscarinic modulation of spike backpropagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J. Neurosci. 17:5782–5791.

    Google Scholar 

  • Ullman S (1995) Sequence seeking and counter streams: A computational model for bidirectional information flow in the visual cortex. Cereb. Cortex. 5:1–11.

    Google Scholar 

  • Victor JD, Mehler F, Reich D, Purpura K (1998) Spatiotemporal origin of bursts and “reliable” spikes generated by neurons in V1. Soc. Neurosci. (Abstract) 24:497.5.

    Google Scholar 

  • von Stein A, Chiang C, König P (1998) Synchronization of activity between parietal cortex and primary visual cortex indicating the top-down processing of behaviorally significant stimuli. (submitted)

  • Watanabe T, Harner AM, Miyauchi S, Sasaki Y, Nielsen M, Palomo D, Mukai I (1998) Task-dependent influences of attention on the activation of human primary visual cortex. Proc. Natl. Acad. Sci. USA 95:11489–11492.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Neuroinformatics, ETH/University Zürich, Winterthurerstr. 190, CH-8057, Zürich

    Markus Siegel, Konrad P. Körding & Peter König

Authors
  1. Markus Siegel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Konrad P. Körding
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter König
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Siegel, M., Körding, K.P. & König, P. Integrating Top-Down and Bottom-Up Sensory Processing by Somato-Dendritic Interactions. J Comput Neurosci 8, 161–173 (2000). https://doi.org/10.1023/A:1008973215925

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1008973215925

Search

Navigation