Feed-forward and noise-tolerant detection of feature homogeneity in spiking networks with a latency code

Abstract

In studies of the visual system as well as in computer vision, the focus is often on contrast edges. However, the primate visual system contains a large number of cells that are insensitive to spatial contrast and, instead, respond to uniform homogeneous illumination of their visual field. The purpose of this information remains unclear. Here, we propose a mechanism that detects feature homogeneity in visual areas, based on latency coding and spike time coincidence, in a purely feed-forward and therefore rapid manner. We demonstrate how homogeneity information can interact with information on contrast edges to potentially support rapid image segmentation. Furthermore, we analyze how neuronal crosstalk (noise) affects the mechanism’s performance. We show that the detrimental effects of crosstalk can be partly mitigated through delayed feed-forward inhibition that shapes bi-phasic post-synaptic events. The delay of the feed-forward inhibition allows effectively controlling the size of the temporal integration window and, thereby, the coincidence threshold. The proposed model is based on single-spike latency codes in a purely feed-forward architecture that supports low-latency processing, making it an attractive scheme of computation in spiking neuronal networks where rapid responses and low spike counts are desired.

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References

  1. Arieli A, Sterkin A, Grinvald A, Aertsen A (1996) Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 273:1868–1871

    CAS  Article  Google Scholar 

  2. Borst JGG, Soria Van Hoeve J (2012) The calyx of held synapse: from model synapse to auditory relay. Annu Rev Physiol 74:199–224. https://doi.org/10.1146/annurev-physiol-020911-153236

    CAS  Article  PubMed  Google Scholar 

  3. Bostner Ž, Knoll G, Lindner B (2020) Information filtering by coincidence detection of synchronous population output: analytical approaches to the coherence function of a two-stage neural system. Biol Cybern 114:403–418. https://doi.org/10.1007/s00422-020-00838-6

    Article  PubMed  PubMed Central  Google Scholar 

  4. Braitenberg V, Schüz A (1991) Anatomy of the cortex: statistics and geometry. Springer, Berlin

    Google Scholar 

  5. Chance FS, Abbott LF, Reyes AD (2002) Gain modulation from background synaptic input. Neuron 35:773–782. https://doi.org/10.1016/S0896-6273(02)00820-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Christie O, Rego J, Jayasuria S (2020) Analyzing sensor quantization of raw images for visual SLAM. In: Proceedings of ICIP 2020, p 2484

  7. Dayan P, Abbott LF (2001) Theoretical neuroscience: Computational and mathematical modeling of neural systems. MIT Press, Cambridge

    Google Scholar 

  8. Delorme A (2003) Early cortical orientation selectivity: how fast inhibition decodes the order of spike latencies. J Comput Neurosci 15:357–365. https://doi.org/10.1023/A:1027420012134

    CAS  Article  PubMed  Google Scholar 

  9. Denman DJ, Contreras D (2016) On parallel streams through the mouse dorsal lateral geniculate nucleus. Front Neural Circuits. https://doi.org/10.3389/fncir.2016.00020

    Article  PubMed  PubMed Central  Google Scholar 

  10. Ding Y, Casagrande VA (1998) Synaptic and neurochemical characterization of parallel pathways to the cytochrome oxidase blobs of primate visual cortex. J Comp Neurol 391:429–443. https://doi.org/10.1002/(SICI)1096-9861(19980222)391:4%3c429::AID-CNE2%3e3.0.CO;2-2

    CAS  Article  PubMed  Google Scholar 

  11. Gewaltig M-O, Diesmann M (2007) NEST (NEural Simulation Tool). Scholarpedia 2:1430

    Article  Google Scholar 

  12. Gewaltig MO, Körner U, Körner E (2003) A model of surface detection and orientation tuning in primate visual cortex. Neurocomputing 52–54:519–524. https://doi.org/10.1016/S0925-2312(02)00767-1

    Article  Google Scholar 

  13. Gollisch T, Meister M (2008) Rapid neural coding in the retina with relative spike latencies. Science 319:1108–1111. https://doi.org/10.1126/science.1149639

    CAS  Article  PubMed  Google Scholar 

  14. Hendry SHC, Reid RC (2000) The koniocellular pathway in primate vision. Annu Rev Neurosci 23:127–153. https://doi.org/10.1146/annurev.neuro.23.1.127

    CAS  Article  PubMed  Google Scholar 

  15. Hendry SHC, Yoshioka T (1994) A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264:575–577. https://doi.org/10.1126/science.8160015

    CAS  Article  PubMed  Google Scholar 

  16. Hernández-González A, Cavada C, Reinoso-Suárez F (1994) The lateral geniculate nucleus projects to the inferior temporal cortex in the macaque monkey. NeuroReport 5:2693–2696. https://doi.org/10.1097/00001756-199412000-00071

    Article  PubMed  Google Scholar 

  17. Hochstein S, Ahissar M (2002) View from the top: hierarchies and reverse hierarchies in the visual system. Neuron 36:791–804. https://doi.org/10.1016/S0896-6273(02)01091-7

    CAS  Article  PubMed  Google Scholar 

  18. Irvin GE, Norton TT, Sesma MA, Casagrande VA (1986) W-like response properties of intralaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Res 362:254–270

    CAS  Article  Google Scholar 

  19. Ito J, Maldonado P, Singer W, Grün S (2011) Saccade-related modulations of neuronal excitability support synchrony of visually elicited spikes. Cereb Cortex 21:2482–2497. https://doi.org/10.1093/cercor/bhr020

    Article  PubMed  PubMed Central  Google Scholar 

  20. Itti L, Koch C (2000) A saliency-based search mechanism for overt and covert shifts of visual attention. Vis Res 40:1489–1506. https://doi.org/10.1016/S0042-6989(99)00163-7

    CAS  Article  PubMed  Google Scholar 

  21. Jayakumar J, Roy S, Dreher B, Martin PR, Vidyasagar TR (2013) Multiple pathways carry signals from short-wavelength-sensitive (‘blue’) cones to the middle temporal area of the macaque. J Physiol 591:339–352. https://doi.org/10.1113/jphysiol.2012.241117

    CAS  Article  PubMed  Google Scholar 

  22. Johansson RS, Birznieks I (2004) First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat Neurosci 7:170–177. https://doi.org/10.1038/nn1177

    CAS  Article  PubMed  Google Scholar 

  23. Klein C, Evrard HC, Shapcott KA, Haverkamp S, Logothetis NK, Schmid MC (2016) Cell-targeted optogenetics and electrical microstimulation reveal the primate koniocellular projection to supra-granular visual cortex. Neuron 90:143–151. https://doi.org/10.1016/j.neuron.2016.02.036

    CAS  Article  PubMed  Google Scholar 

  24. Körner E, Gewaltig M-O, Körner U, Richter A, Rodemann T (1999) A model of computation in neocortical architecture. Neural Netw 12:989–1005. https://doi.org/10.1016/S0893-6080(99)00049-0

    Article  PubMed  Google Scholar 

  25. Kremkow J, Aertsen A, Kumar A (2010a) Gating of signal propagation in spiking neural networks by balanced and correlated excitation and inhibition. J Neurosci 30:15760–15768. https://doi.org/10.1523/JNEUROSCI.3874-10.2010

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. Kremkow J, Perrinet LU, Masson GS, Aertsen A (2010) Functional consequences of correlated excitatory and inhibitory conductances in cortical networks. J Comput Neurosci 28:579–594. https://doi.org/10.1007/s10827-010-0240-9

    Article  PubMed  Google Scholar 

  27. Kremkow J, Perrinet LU, Monier C, Alonso J-M, Aertsen A, Frégnac Y et al (2016) Push-pull receptive field organization and synaptic depression: mechanisms for reliably encoding naturalistic stimuli in V1. Front Neural Circuits 10:37. https://doi.org/10.3389/fncir.2016.00037

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kuhn A, Aertsen A, Rotter S (2004) Neuronal integration of synaptic input in the fluctuation-driven regime. J Neurosci 24:2345–2356. https://doi.org/10.1523/JNEUROSCI.3349-03.2004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. Kupper R, Gewaltig M-O, Körner U, Körner E (2005) Spike-latency codes and the effect of saccades. Neurocomputing 65–66:189–194. https://doi.org/10.1016/j.neucom.2004.10.006

    Article  Google Scholar 

  30. Lagorce X, Orchard G, Galluppi F, Shi BE, Benosman RB (2017) HOTS: a hierarchy of event-based time-surfaces for pattern recognition. IEEE Trans Pattern Anal Mach Intell 39:1346–1359. https://doi.org/10.1109/TPAMI.2016.2574707

    Article  PubMed  Google Scholar 

  31. Lapicque L (1907) Recherches quantitatives sur l’excitation électrique des nerfs traitée comme une polarization. J Physiol Pathol générale 9:620–635

    Google Scholar 

  32. Livingstone M, Hubel D (1988) Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240:740–749. https://doi.org/10.1126/science.3283936

    CAS  Article  PubMed  Google Scholar 

  33. Lund JS, Yoshioka T, Levitt JB (1994) Substrates for interlaminar connections in area V1 of Macaque monkey cerebral cortex. In: Peters A, Rockland KS (eds) Cerebral cortex: primary visual cortex in primates. Plenum Press, New York, pp 37–60. doi:https://doi.org/10.1007/978-1-4757-9628-5_2.

  34. Masquelier T, Thorpe SJ (2007) Unsupervised learning of visual features through spike timing dependent plasticity. PLoS Comput Biol 3:e31. https://doi.org/10.1371/journal.pcbi.0030031

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Morand S, Thut G, De Peralta RG, Clarke S, Khateb A, Landis T et al (2000) Electrophysiological evidence for fast visual processing through the human koniocellular pathway when stimuli move. Cereb Cortex 10:817–825. https://doi.org/10.1093/cercor/10.8.817

    CAS  Article  PubMed  Google Scholar 

  36. Müller NG, Kleinschmidt A (2004) The attentional ‘spotlight’s’ penumbra: center-surround modulation in striate cortex. NeuroReport 15:977–980. https://doi.org/10.1097/00001756-200404290-00009

    Article  PubMed  Google Scholar 

  37. Nelken I, Chechik G, Mrsic-Flogel TD, King AJ, Schnupp JWH (2005) Encoding stimulus information by spike numbers and mean response time in primary auditory cortex. J Comput Neurosci 19:199–221. https://doi.org/10.1007/s10827-005-1739-3

    Article  PubMed  Google Scholar 

  38. Niemeyer JE, Paradiso MA (2018) Saccade-based termination responses in macaque V1 and visual perception. Vis Neurosci 35:E025. https://doi.org/10.1017/S0952523818000032

    Article  PubMed  PubMed Central  Google Scholar 

  39. Reinagel P, Reid RC (2000) Temporal coding of visual information in the Thalamus. J Neurosci 20:5392–5400. https://doi.org/10.1523/JNEUROSCI.20-14-05392.2000

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Sclar G, Maunsell JHR, Lennie P (1990) Coding of image contrast in central visual pathways of the macaque monkey. Vis Res 30:1–10. https://doi.org/10.1016/0042-6989(90)90123-3

    CAS  Article  PubMed  Google Scholar 

  41. Sincich LC, Park KF, Wohlgemuth MJ, Horton JC (2004) Bypassing V1: a direct geniculate input to area MT. Nat Neurosci 7:1123–1128. https://doi.org/10.1038/nn1318

    CAS  Article  PubMed  Google Scholar 

  42. Solomon SG, Tailby C, Cheong SK, Camp AJ (2010) Linear and nonlinear contributions to the visual sensitivity of neurons in primate lateral geniculate nucleus. J Neurophysiol. https://doi.org/10.1152/jn.01118.2009

    Article  PubMed  Google Scholar 

  43. Solomon SG, White AJ, Martin PR (1999) Temporal contrast sensitivity in the lateral geniculate nucleus of a New World monkey, the marmoset Callithrix jacchus. J. Physiol. 517(3):907–917. https://doi.org/10.1111/j.1469-7793.1999.0907s.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. Szmajda BA, Buzás P, FitzGibbon T, Martin PR (2006) Geniculocortical relay of blue-off signals in the primate visual system. Proc Natl Acad Sci USA 103:19512–19517. https://doi.org/10.1073/pnas.0606970103.

    CAS  Article  PubMed  Google Scholar 

  45. Tailby C, Solomon SG, Dhruv NT, et al (2007) A new code for contrast in the primate visual pathway. J Neurosci 27:3904–3909. https://doi.org/10.1523/JNEUROSCI.5343-06.2007

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  46. Thomson AM, Lamy C (2007) Functional maps of neocortical local circuitry. Front Neurosci 1:19–42. https://doi.org/10.3389/neuro.01.1.1.002.2007

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  47. Thorpe S, Fize D, Marlot C (1996) Speed of processing in the human visual system. Nature 381:520–522. https://doi.org/10.1038/381520a0

    CAS  Article  PubMed  Google Scholar 

  48. Thorpe SJ, Imbert M (1989) Biological constraints on connectionist models. In: Pfeifer R, Fogelman-Soulié F (eds) Connectionism in perspective. Elsevier, Amsterdam, pp 63–92

    Google Scholar 

  49. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci 94:719–723. https://doi.org/10.1073/pnas.94.2.719

    CAS  Article  PubMed  Google Scholar 

  50. Tuckwell HC (1988) Introduction to theoretical neurobiology. Cambridge University Press, Cambridge. doi:https://doi.org/10.1017/cbo9780511623271

  51. Ullman S (2000) High-level vision: object recognition and visual cognition. MIT Press, Cambridge

    Google Scholar 

  52. Van Rullen R, Thorpe SJ (2001) Rate coding versus temporal order coding: what the retinal ganglion cells tell the visual cortex. Neural Comput 13:1255–1283. https://doi.org/10.1162/08997660152002852

    Article  PubMed  Google Scholar 

  53. VanRullen R, Guyonneau R, Thorpe SJ (2005) Spike times make sense. Trends Neurosci 28:1–4. https://doi.org/10.1016/j.tins.2004.10.010

    CAS  Article  PubMed  Google Scholar 

  54. White AJR, Solomon SG, Martin PR (2001) Spatial properties of koniocellular cells in the lateral geniculate nucleus of the marmoset Callithrix jacchus. J Physiol 533:519–535. https://doi.org/10.1111/j.1469-7793.2001.0519a.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. Xu X, Ichida JM, Allison JD, Boyd JD, Bonds AB, Casagrande VA (2001) A comparison of koniocellular, magnocellular and parvocellular receptive field properties in the lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). J Physiol 531:203–218. https://doi.org/10.1111/j.1469-7793.2001.0203j.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Dr. Ursula Körner for her help and support in compiling the evidence on koniocellular processing strategies across primate species that was instrumental in forming the hypothesis underlying this study. This work was supported by BMBF Grant 01GQ0420 to BCCN Freiburg and EU H2020 Grant 945539 (Human Brain Project SGA3) to the University of Hertfordshire.

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Schmuker, M., Kupper, R., Aertsen, A. et al. Feed-forward and noise-tolerant detection of feature homogeneity in spiking networks with a latency code. Biol Cybern 115, 161–176 (2021). https://doi.org/10.1007/s00422-021-00866-w

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