Navigate the Unknown: Implications of Grid-Cells “Mental Travel” in Vicarious Trial and Error

  • Diogo Santos-Pata
  • Riccardo Zucca
  • Paul F. M. J. Verschure
Conference paper
Part of the Lecture Notes in Computer Science book series (LNCS, volume 9793)

Abstract

Rodents are able to navigate within dynamic environments by constantly adapting to their surroundings. Hippocampal place-cells encode the animals current location and fire in sequences during path planning events. Place-cells receive excitatory inputs from grid-cells whose metric system constitute a powerful mechanism for vector based navigation for both known and unexplored locations. However, neither the purpose or the behavioral consequences of such mechanism are fully understood. During early exploration of a maze with multiple discrimination points, rodents typically manifest a conflict-like behavior consisting of alternating head movements from one arm of the maze to the other be- fore making a choice, a behavior which is called vicarious trial and error (VTE). Here, we suggest that VTE is modulated by the learning process between spatial- and reward-tuned neuronal populations. We present a hippocampal model of place- and grid-cells for both space representation and mental travel that we used to control a robot solving a foraging task. We show that place-cells are able to represent the agents current location, whereas grid-cells encode the robots movement in space and project their activity over unexplored paths. Our results suggest a tight interaction between spatial and reward related neuronal activity in defining VTE behavior.

Keywords

Biomimetics Navigation Grid-cells Mental travel VTE 

References

  1. 1.
    Hafting, T., et al.: Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052), 801–806 (2005)CrossRefGoogle Scholar
  2. 2.
    Pata, D.S., Escuredo, A., Lallée, S., Verschure, P.F.M.J.: Hippocampal based model reveals the distinct roles of dentate gyrus and CA3 during robotic spatial navigation. In: Duff, A., Lepora, N.F., Mura, A., Prescott, T.J., Verschure, P.F.M.J. (eds.) Living Machines 2014. LNCS, vol. 8608, pp. 273–283. Springer, Heidelberg (2014)Google Scholar
  3. 3.
    Maffei, G., Santos-Pata, D., Marcos, E., Sanchez-Fibla, M., Verschure, P.F.: An embodied biologically constrained model of foraging: from classical and operant conditioning to adaptive real-world behavior in DAC-X. Neural Netw. 72, 88–108 (2015)CrossRefGoogle Scholar
  4. 4.
    Domnisoru, C., Kinkhabwala, A.A., Tank, D.W.: Membrane potential dynamics of grid cells. Nature 495(7440), 199–204 (2013)CrossRefGoogle Scholar
  5. 5.
    Johnson, A., David Redish, A.: Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J. Neurosci. 27(45), 12176–12189 (2007)CrossRefGoogle Scholar
  6. 6.
    Guanella, A., Kiper, D., Verschure, P.: A model of grid cells based on a twisted torus topology. Int. J. Neural Syst. 17(04), 231–240 (2007)CrossRefGoogle Scholar
  7. 7.
    Brun, V.H., et al.: Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18(12), 1200–1212 (2008)MathSciNetCrossRefGoogle Scholar
  8. 8.
    Tolman, E.C.: Cognitive maps in rats and men. Psychol. Rev. 55(4), 189 (1948)CrossRefGoogle Scholar
  9. 9.
    Redish, A.D.: Vicarious trial and error. Nat. Rev. Neurosci. 17(3), 147–159 (2016)CrossRefGoogle Scholar
  10. 10.
    Sanders, H., et al.: Grid cells and place cells: an integrated view of their navigational and memory function. Trends Neurosci. 38(12), 763–775 (2015)CrossRefGoogle Scholar
  11. 11.
    Bush, D., et al.: Using grid cells for navigation. Neuron 87(3), 507–520 (2015)CrossRefGoogle Scholar
  12. 12.
    van der Meer, M.A., et al.: Triple dissociation of information processing in dorsal striatum, ventral striatum, and hippocampus on a learned spatial decision task. Neuron 67(1), 25–32 (2010)CrossRefGoogle Scholar
  13. 13.
    Hebb, D.O.: The Organization of Behavior: A Neuropsychological Theory. Psychology Press, New York (2005)Google Scholar
  14. 14.
    de Almeida, L., Idiart, M., Lisman, J.E.: The input output transformation of the hippocampal granule cells: from grid cells to place fields. J. Neurosci. 29(23), 7504–7512 (2009)CrossRefGoogle Scholar
  15. 15.
    O’Keefe, J., Dostrovsky, J.: The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34(1), 171–175 (1971)CrossRefGoogle Scholar
  16. 16.
    Yoon, K.J., et al.: Specific evidence of low-dimensional continuous attractor dynamics in grid cells. Nat. Neurosci. 16(8), 1077–1084 (2013)CrossRefGoogle Scholar
  17. 17.
    Pfeiffer, B.E., Foster, D.J.: Hippocampal place-cell sequences depict future paths to remembered goals. Nature 497(7447), 74–79 (2013)CrossRefGoogle Scholar
  18. 18.
    Taube, J.S., Muller, R.U., Ranck, J.B.: Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10(2), 420–435 (1990)Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Diogo Santos-Pata
    • 1
  • Riccardo Zucca
    • 1
  • Paul F. M. J. Verschure
    • 1
    • 2
  1. 1.Universitat Pompeu Fabra, SPECS group, N-RASBarcelonaSpain
  2. 2.ICREABarcelonaSpain

Personalised recommendations