Skip to main content
Log in

An insect-inspired model for visual binding I: learning objects and their characteristics

  • Original Article
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Visual binding is the process of associating the responses of visual interneurons in different visual submodalities all of which are responding to the same object in the visual field. Recently identified neuropils in the insect brain termed optic glomeruli reside just downstream of the optic lobes and have an internal organization that could support visual binding. Working from anatomical similarities between optic and olfactory glomeruli, we have developed a model of visual binding based on common temporal fluctuations among signals of independent visual submodalities. Here we describe and demonstrate a neural network model capable both of refining selectivity of visual information in a given visual submodality, and of associating visual signals produced by different objects in the visual field by developing inhibitory neural synaptic weights representing the visual scene. We also show that this model is consistent with initial physiological data from optic glomeruli. Further, we discuss how this neural network model may be implemented in optic glomeruli at a neuronal level.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

References

  • Adelson EH, Bergen JR (1985) Spatiotemporal energy models for the perception of motion. J Opt Soc Am A 2:284–299

    Article  CAS  PubMed  Google Scholar 

  • Albrecht DG, Geisler WS (1991) Motion selectivity and the contrast-response function of simple cells in the visual cortex. Vis Neurosci 7(6):531–546

    Article  CAS  PubMed  Google Scholar 

  • Anderson JA (1995) An introduction to neural networks. MIT Press, Cambridge

    Google Scholar 

  • Arnett DW (1972) Spatial and temporal integration properties of units in first optic ganglion of dipterans. J Neurophysiol 35(4):429–444

    CAS  PubMed  Google Scholar 

  • Barlow HB (2001) Redundancy reduction revisited. Netw Comp Neural 12(3):241–253

    Article  CAS  Google Scholar 

  • Bazhenov M, Stopfer M, Rabinovich M, Abarbanel HD, Sejnowski TJ, Laurent G (2001) Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron 30(2):569–581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bi GQ, Poo MM (1998) Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci 18(24):10,464–10,472

    CAS  Google Scholar 

  • Borst A, Egelhaaf M (1989) Principles of visual motion detection. Trends Neurosci 12(8):297–306

    Article  CAS  PubMed  Google Scholar 

  • Carandini M, Heeger DJ (2012) Normalization as a canonical neural computation. Nat Rev Neurosci 13(1):51–62

    Article  CAS  Google Scholar 

  • Cichocki A, Bogner RE, Moszczyński L, Pope K (1997) Modified Herault–Jutten algorithms for blind separation of sources. Digit Signal Process 7(2):80–93

    Article  Google Scholar 

  • Crick F, Koch C (1990) Towards a neurobiological theory of consciousness. Semin Neurosci 2:263–275

    Google Scholar 

  • Douglass JK, Strausfeld NJ (2005) Sign-conserving amacrine neurons in the fly’s external plexiform layer. Vis Neurosci 22(03):345–358

    Article  PubMed  Google Scholar 

  • Eckhorn R, Reitboeck HJ, Arndt M, Dicke P (1990) Feature linking via synchronization among distributed assemblies: simulations of results from cat visual cortex. Neural Comput 2(3):293–307

    Article  Google Scholar 

  • Engel AK, Singer W (2001) Temporal binding and the neural correlates of sensory awareness. Trends Cognit Sci 5(1):16–25

    Article  Google Scholar 

  • Engel AK, König P, Kreiter AK, Schillen TB, Singer W (1992) Temporal coding in the visual cortex: new vistas on integration in the nervous system. Trends Neurosci 15(6):218–226

    Article  CAS  PubMed  Google Scholar 

  • Fonta C, Sun XJ, Masson C (1993) Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem Senses 18(2):101–119

    Article  Google Scholar 

  • Gerstner W, Kistler WM (2002) Mathematical formulations of Hebbian learning. Biol Cybern 87(5–6):404–415

    Article  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Hassenstein B, Reichardt W (1956) Systemtheoretische Analyse der Zeit-, Reihenfolgen- und Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Z Naturforsch B 11(9–10):513–524

    Google Scholar 

  • Hebb DO (1949) The organization of behavior: a neuropsychological theory. Wiley, New York

    Google Scholar 

  • Heisenberg M (2003) Mushroom body memoir: From maps to models. Nat Rev Neurosci 4(4):266–275

    Article  CAS  PubMed  Google Scholar 

  • Herault J, Jutten C (1986) Space or time adaptive signal processing by neural network models. In: AIP Conference Proceedings, Snowbird, vol 151. American Institute of Physics, pp 206–211

  • Hildebrand JG (1996) Olfactory control of behavior in moths: central processing of odor information and the functional significance of olfactory glomeruli. J Comp Physiol A 178(1):5–19

    Article  CAS  PubMed  Google Scholar 

  • Hildebrand JG, Shepherd GM (1997) Mechanisms of olfactory discrimination: Converging evidence for common principles across phyla. Annu Rev Neurosci 20(1):595–631

    Article  CAS  PubMed  Google Scholar 

  • Hopfield JJ (1991) Olfactory computation and object perception. Proc Natl Acad Sci USA 88(15):6462–6466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubel DH, Wiesel TN (1959) Receptive fields of single neurones in the cat’s striate cortex. J Physiol 148(3):574–591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hubel DH, Wiesel TN (1968) Receptive fields and functional architecture of monkey striate cortex. J Physiol 195(1):215–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hummel JE, Biederman I (1992) Dynamic binding in a neural network for shape recognition. Psychol Rev 99(3):480–517

    Article  CAS  PubMed  Google Scholar 

  • Hyvärinen A, Oja E (1998) Independent component analysis by general nonlinear Hebbian-like learning rules. Signal Process 64(3):301–313

    Article  Google Scholar 

  • Itti L, Koch C, Niebur E (1998) A model of saliency-based visual attention for rapid scene analysis. IEEE Trans Pattern Anal 11:1254–1259

    Article  Google Scholar 

  • Jefferis GSXE (2005) Insect olfaction: a map of smell in the brain. Curr Biol 15(17):R668–R670

    Article  CAS  PubMed  Google Scholar 

  • Joho M, Mathis H, Lambert RH (2000) Overdetermined blind source separation: Using more sensors than source signals in a noisy mixture. In: Proc. International Conference on Independent Component Analysis and Blind Signal Separation. Helsinki, pp 81–86

  • Jutten C, Herault J (1991) Blind separation of sources, part I: an adaptive algorithm based on neuromimetic architecture. Signal Process 24(1):1–10

    Article  Google Scholar 

  • Koch C (1999) Biophysics of computation: information processing in single neurons. Oxford University Press, New York

    Google Scholar 

  • Land MF, Nilsson DE (2002) Animal eyes. Oxford University Press, New York

    Google Scholar 

  • Laughlin S (1983) Matching coding to scenes to enhance efficiency. Proceedings of an International Symposium Organized by The Rank Prize Funds, Springer Series in Information Sciences. Springer, London, pp 42–52

    Google Scholar 

  • Linster C, Masson C (1996) A neural model of olfactory sensory memory in the honeybee’s antennal lobe. Neural Comput 8(1):94–114

    Article  Google Scholar 

  • Linster C, Smith BH (1997) A computational model of the response of honey bee antennal lobe circuitry to odor mixtures: overshadowing, blocking and unblocking can arise from lateral inhibition. Behav Brain Res 87(1):1–14

    Article  CAS  PubMed  Google Scholar 

  • von der Malsburg C (1994) The correlation theory of brain function. Springer, New York

    Google Scholar 

  • von der Malsburg C (1999) The what and why of binding: the modeler’s perspective. Neuron 24(1):95–104

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Martin AB, von der Heydt R (2015) Spike synchrony reveals emergence of proto-objects in visual cortex. J Neurosci 35(17):6860–6870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mu L, Ito K, Bacon JP, Strausfeld NJ (2012) Optic glomeruli and their inputs in Drosophila share an organizational ground pattern with the antennal lobes. J Neurosci 32(18):6061–6071

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakayama K, Silverman GH (1988) The aperture problem—I. Perception of nonrigidity and motion direction in translating sinusoidal lines. Vis Res 28(6):739–746

    Article  CAS  PubMed  Google Scholar 

  • Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenböck G (2002) Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36(3):463–474

    Article  CAS  PubMed  Google Scholar 

  • Northcutt BD, Higgins CM (2017) An insect-inspired model for visual binding II: Functional analysis and visual attention. Biol Cybern. doi:10.1007/s00422-017-0716-z

  • Okamura JY, Strausfeld NJ (2007) Visual system of calliphorid flies: motion- and orientation-sensitive visual interneurons supplying dorsal optic glomeruli. J Comp Neurol 500(1):189–208

    Article  PubMed  Google Scholar 

  • Paulk AC, Dacks AM, Phillips-Portillo J, Fellous JM, Gronenberg W (2009) Visual processing in the central bee brain. J Neurosci 29(32):9987–9999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rivera-Alvidrez Z, Lin I, Higgins CM (2011) A neuronally based model of contrast gain adaptation in fly motion vision. Vis Neurosci 28(5):419–431

    Article  PubMed  Google Scholar 

  • Rodieck RW (1965) Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vis Res 5(12):583–601

    Article  CAS  PubMed  Google Scholar 

  • van Santen JPH, Sperling G (1985) Elaborated Reichardt detectors. J Opt Soc Am A 2(5):300–320

    Article  PubMed  Google Scholar 

  • Schillen TB, König P (1994) Binding by temporal structure in multiple feature domains of an oscillatory neuronal network. Biol Cybern 70(5):397–405

    Article  CAS  PubMed  Google Scholar 

  • Schwartz O, Simoncelli EP (2001) Natural signal statistics and sensory gain control. Nat Neurosci 4(8):819–825

    Article  CAS  PubMed  Google Scholar 

  • Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24(1):1193–1216

    Article  CAS  PubMed  Google Scholar 

  • Snyder AW (1979) Physics of vision in compound eyes. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6A. Springer, Berlin, pp 225–313 (chap 5)

    Google Scholar 

  • Song S, Miller KD, Abbott LF (2000) Competitive Hebbian learning through spike-timing-dependent synaptic plasticity. Nat Neurosci 3(9):919–926

    Article  CAS  PubMed  Google Scholar 

  • Srinivasan MV, Zhang SW, Witney K (1994) Visual discrimination of pattern orientation by honeybees: performance and implications for ‘cortical’ processing. Philos Trans R Soc B 343(1304):199–210

    Article  Google Scholar 

  • Stavenga DG (1979) Pseudopupils of compound eyes. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6A. Springer, Berlin, pp 357–439 (chap 7)

    Google Scholar 

  • Strausfeld NJ, Okamura JY (2007) Visual system of calliphorid flies: organization of optic glomeruli and their lobula complex efferents. J Comp Neurol 500(1):166–188

    Article  PubMed  Google Scholar 

  • Strausfeld NJ, Sinakevitch I, Okamura JY (2007) Organization of local interneurons in optic glomeruli of the dipterous visual system and comparisons with the antennal lobes. Dev Neurobiol 67(10):1267–1288

    Article  PubMed  Google Scholar 

  • Trentelman H, Stoorvogel AA, Hautus M (2012) Control theory for linear systems. Springer Science & Business Media, Berlin

    Google Scholar 

  • Yang EC, Maddess T (1997) Orientation-sensitive neurons in the brain of the honey bee (Apis mellifera). J Insect Physiol 43(4):329–336

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Air Force Office of Scientific Research for early support of this project with Grant Number FA9550-07-1-0165, and the Air Force Research Laboratories for supporting this research to maturity with STTR Phase I Award Number FA8651-13-M-0085 and Phase II Award Number FA8651-14-C-0108, both in collaboration with Spectral Imaging Laboratory (Pasadena, CA). We would also like to thank the reviewers, whose input greatly enhanced this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brandon D. Northcutt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Northcutt, B.D., Dyhr, J.P. & Higgins, C.M. An insect-inspired model for visual binding I: learning objects and their characteristics. Biol Cybern 111, 185–206 (2017). https://doi.org/10.1007/s00422-017-0715-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-017-0715-0

Keywords

Navigation