Skip to main content
Top
Published in: Journal of Computational Neuroscience 2/2020

03-03-2020

A computational model for grid maps in neural populations

Authors: Fabio Anselmi, Micah M. Murray, Benedetta Franceschiello

Published in: Journal of Computational Neuroscience | Issue 2/2020

Log in

Activate our intelligent search to find suitable subject content or patents.

search-config
loading …

Abstract

Grid cells in the entorhinal cortex, together with head direction, place, speed and border cells, are major contributors to the organization of spatial representations in the brain. In this work we introduce a novel theoretical and algorithmic framework able to explain the optimality of hexagonal grid-like response patterns. We show that this pattern is a result of minimal variance encoding of neurons together with maximal robustness to neurons’ noise and minimal number of encoding neurons. The novelty lies in the formulation of the encoding problem considering neurons as an overcomplete basis (a frame) where the position information is encoded. Through the modern Frame Theory language, specifically that of tight and equiangular frames, we provide new insights about the optimality of hexagonal grid receptive fields. The proposed model is based on the well-accepted and tested hypothesis of Hebbian learning, providing a simplified cortical-based framework that does not require the presence of velocity-driven oscillations (oscillatory model) or translational symmetries in the synaptic connections (attractor model). We moreover demonstrate that the proposed encoding mechanism naturally explains axis alignment of neighbor grid cells and maps shifts, rotations and scaling of the stimuli onto the shape of grid cells’ receptive fields, giving a straightforward explanation of the experimental evidence of grid cells remapping under transformations of environmental cues.

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

  • über 102.000 Bücher
  • über 537 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Finance + Banking
  • Management + Führung
  • Marketing + Vertrieb
  • Maschinenbau + Werkstoffe
  • Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Springer Professional "Wirtschaft"

Online-Abonnement

Mit Springer Professional "Wirtschaft" erhalten Sie Zugriff auf:

  • über 67.000 Bücher
  • über 340 Zeitschriften

aus folgenden Fachgebieten:

  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Finance + Banking
  • Management + Führung
  • Marketing + Vertrieb
  • Versicherung + Risiko




Jetzt Wissensvorsprung sichern!

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

  • über 67.000 Bücher
  • über 390 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Maschinenbau + Werkstoffe




 

Jetzt Wissensvorsprung sichern!

Literature
go back to reference Aapo, H., Hoyer, P.O., Hurri, J. (2009). Natural image statistics: a probabilistic approach to early computational vision. Book. Aapo, H., Hoyer, P.O., Hurri, J. (2009). Natural image statistics: a probabilistic approach to early computational vision. Book.
go back to reference Banino, A, & et al. (2018). Vector-based navigation using grid-like representations in artificial agents. Nature, 557, 05. Banino, A, & et al. (2018). Vector-based navigation using grid-like representations in artificial agents. Nature, 557, 05.
go back to reference Bicanski, A, & Burgess, N. (2019). A computational model of visual recognition memory via grid cells. Current Biology, 29(6), 979–990, e4.PubMedPubMedCentral Bicanski, A, & Burgess, N. (2019). A computational model of visual recognition memory via grid cells. Current Biology, 29(6), 979–990, e4.PubMedPubMedCentral
go back to reference Blair, H.T., Welday, A.C., Zhang, K. (2007). Scale-invariant memory representations emerge from moire interference between grid fields that produce theta oscillations: a computational model. Journal of Neuroscience, 27, 3211–3229.PubMed Blair, H.T., Welday, A.C., Zhang, K. (2007). Scale-invariant memory representations emerge from moire interference between grid fields that produce theta oscillations: a computational model. Journal of Neuroscience, 27, 3211–3229.PubMed
go back to reference Burak, Y., & Fiete, I.R. (2009). Accurate path integration in continuous attractor network models of grid cells. PLoS Computational Biology, 5. Burak, Y., & Fiete, I.R. (2009). Accurate path integration in continuous attractor network models of grid cells. PLoS Computational Biology, 5.
go back to reference Burgess, N., Barry, C., O’Keefe, J. (2007). An oscillatory interference model of grid cell firing. Hippocampus, 17, 801–812.PubMedPubMedCentral Burgess, N., Barry, C., O’Keefe, J. (2007). An oscillatory interference model of grid cell firing. Hippocampus, 17, 801–812.PubMedPubMedCentral
go back to reference Carandini, M, & Heeger, D.J. (2011). Normalization as a canonical neural computation. Nature Reviews Neuroscience, 13(1), 51–62.PubMedPubMedCentral Carandini, M, & Heeger, D.J. (2011). Normalization as a canonical neural computation. Nature Reviews Neuroscience, 13(1), 51–62.PubMedPubMedCentral
go back to reference Casazza, G.P., Fickus, M., Kovačević, J., Leon, M.T., Tremain, C.J. (2006). A physical interpretation of tight frames. Harmonic analysis and applications. Applied and Numerical Harmonic Analysis. Casazza, G.P., Fickus, M., Kovačević, J., Leon, M.T., Tremain, C.J. (2006). A physical interpretation of tight frames. Harmonic analysis and applications. Applied and Numerical Harmonic Analysis.
go back to reference Castro, L, & Aguiar, P. (2014). A feedforward model for the formation of a grid field where spatial information is provided solely from place cells. Biological Cybernetics, 108(2), 133–143.PubMed Castro, L, & Aguiar, P. (2014). A feedforward model for the formation of a grid field where spatial information is provided solely from place cells. Biological Cybernetics, 108(2), 133–143.PubMed
go back to reference Cheng, D. (2018). Hexadirectional modulation of theta power in human entorhinal cortex during spatial navigation. Current Biology, 28, 20, 3310–3315. Cheng, D. (2018). Hexadirectional modulation of theta power in human entorhinal cortex during spatial navigation. Current Biology, 28, 20, 3310–3315.
go back to reference Constantinescu, A.O., O’Reilly, J.X., Behrens, T.E.J. (2016). Organizing conceptual knowledge in humans with a gridlike code. Science, 352, 1464–1468.PubMedPubMedCentral Constantinescu, A.O., O’Reilly, J.X., Behrens, T.E.J. (2016). Organizing conceptual knowledge in humans with a gridlike code. Science, 352, 1464–1468.PubMedPubMedCentral
go back to reference Deneve, S., Peter, E., Latham, Alexandre, P. (1999). Reading population codes: a neural implementation of ideal observers. Nature Neuroscience, 2(8), 740–745.PubMed Deneve, S., Peter, E., Latham, Alexandre, P. (1999). Reading population codes: a neural implementation of ideal observers. Nature Neuroscience, 2(8), 740–745.PubMed
go back to reference Dordek, Y, Soudry, D, Meir, R, Derdikman, D. (2016). Extracting grid cell characteristics from place cell inputs using non-negative principal component analysis. eLife, 5, e10094.PubMedPubMedCentral Dordek, Y, Soudry, D, Meir, R, Derdikman, D. (2016). Extracting grid cell characteristics from place cell inputs using non-negative principal component analysis. eLife, 5, e10094.PubMedPubMedCentral
go back to reference Eagleson, R. (1992). Measurement of the 2D affine Lie group parameters for visual motion analysis. Spatial Vision, 6, 3. Eagleson, R. (1992). Measurement of the 2D affine Lie group parameters for visual motion analysis. Spatial Vision, 6, 3.
go back to reference Field, D.J. (1999). Wavelets, vision and the statistics of natural scenes. Philosophical Transactions, Mathematical, Physical and Engineering Sciences, 357(1760), 2527. Field, D.J. (1999). Wavelets, vision and the statistics of natural scenes. Philosophical Transactions, Mathematical, Physical and Engineering Sciences, 357(1760), 2527.
go back to reference Fiete, I.R., Burak, Y, Brookings, T. (2008). What grid cells convey about rat location. Journal of Neuroscience, 28(27), 6858–6871.PubMed Fiete, I.R., Burak, Y, Brookings, T. (2008). What grid cells convey about rat location. Journal of Neuroscience, 28(27), 6858–6871.PubMed
go back to reference Franzius, M, Sprekeler, H, Wiskott, L. (2007). Slowness and sparseness lead to place, head-direction, and spatial-view cells. Plos Computational Biology, 3(8), 1605–1622. Franzius, M, Sprekeler, H, Wiskott, L. (2007). Slowness and sparseness lead to place, head-direction, and spatial-view cells. Plos Computational Biology, 3(8), 1605–1622.
go back to reference Fuhs, M.C., & Touretzky, D.S. (2006). A spin glass model of path integration in rat medial entorhinal cortex. Journal of Neuroscience, 6, 4266–4276. Fuhs, M.C., & Touretzky, D.S. (2006). A spin glass model of path integration in rat medial entorhinal cortex. Journal of Neuroscience, 6, 4266–4276.
go back to reference Goyal, V.K., & Kovacevic, J. (2001). Quantized frame expansions with erasures. Applied and Computational Harmonic Analysis, 10, 203–233. Goyal, V.K., & Kovacevic, J. (2001). Quantized frame expansions with erasures. Applied and Computational Harmonic Analysis, 10, 203–233.
go back to reference Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., Moser, E.I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436, 801–806.PubMed Hafting, T., Fyhn, M., Molden, S., Moser, M.-B., Moser, E.I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436, 801–806.PubMed
go back to reference Hasselmo, M.E., Giocomo, L.M., Zilli, E.A. (2007). Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus, 17, 1252–1271.PubMedPubMedCentral Hasselmo, M.E., Giocomo, L.M., Zilli, E.A. (2007). Grid cell firing may arise from interference of theta frequency membrane potential oscillations in single neurons. Hippocampus, 17, 1252–1271.PubMedPubMedCentral
go back to reference Hebb, D.O. (1949). The organization of behavior: a neuropsychological theory. Wiley. Hebb, D.O. (1949). The organization of behavior: a neuropsychological theory. Wiley.
go back to reference Heys, J.G., MacLeod, K.M., Moss, C.F., Hasselmo, M.E. (2013). Bat and rat neurons differ in theta frequency resonance despite similar coding of space. Science, 340, 363–367.PubMed Heys, J.G., MacLeod, K.M., Moss, C.F., Hasselmo, M.E. (2013). Bat and rat neurons differ in theta frequency resonance despite similar coding of space. Science, 340, 363–367.PubMed
go back to reference Hubel, DH, & Wiesel, TN. (1965). Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. Journal of Neurophysiology, 28(2), 229.PubMed Hubel, DH, & Wiesel, TN. (1965). Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. Journal of Neurophysiology, 28(2), 229.PubMed
go back to reference Hubel, DH, & Wiesel, TN. (1968). Receptive fields and functional architecture of monkey striate cortex. The Journal of Physiology, 195(1), 215.PubMedPubMedCentral Hubel, DH, & Wiesel, TN. (1968). Receptive fields and functional architecture of monkey striate cortex. The Journal of Physiology, 195(1), 215.PubMedPubMedCentral
go back to reference Jacobs, J. (2013). Direct recordings of grid-like neuronal activity in human spatial navigation. Nature Neuroscience, 16, 1188–1190.PubMedPubMedCentral Jacobs, J. (2013). Direct recordings of grid-like neuronal activity in human spatial navigation. Nature Neuroscience, 16, 1188–1190.PubMedPubMedCentral
go back to reference Kay, S.M. (1993). Fundamentals of statistical signal processing: estimation theory. New Jersey: Englewood Cliffs. Kay, S.M. (1993). Fundamentals of statistical signal processing: estimation theory. New Jersey: Englewood Cliffs.
go back to reference Keinath, A, Epstein, R.A., Balasubramanian, V. (2018). Environmental deformations dynamically shift the grid cell spatial metric. eLife, 7, 10. Keinath, A, Epstein, R.A., Balasubramanian, V. (2018). Environmental deformations dynamically shift the grid cell spatial metric. eLife, 7, 10.
go back to reference Kim, M. (2019). Can we study 3d grid codes non-invasively in the human brain? Methodological considerations and fmri findings. NeuroImage, 186, 667–678.PubMedPubMedCentral Kim, M. (2019). Can we study 3d grid codes non-invasively in the human brain? Methodological considerations and fmri findings. NeuroImage, 186, 667–678.PubMedPubMedCentral
go back to reference Kovacevic, J., & Chebira, A. (2007). Life beyond bases: the advent of frames (part i). IEEE Signal Processing Magazine, 24(4), 86–104. Kovacevic, J., & Chebira, A. (2007). Life beyond bases: the advent of frames (part i). IEEE Signal Processing Magazine, 24(4), 86–104.
go back to reference Kropff, E., & Treves, A. (2008). The emergence of grid cells: intelligent design or just adaptation? Hippocampus, 18, 1256–1269.PubMed Kropff, E., & Treves, A. (2008). The emergence of grid cells: intelligent design or just adaptation? Hippocampus, 18, 1256–1269.PubMed
go back to reference Krupic, J., Bauza, M., Burton, S., Lever, C., O’Keefe, J. (2014). How environment geometry affects grid cell symmetry and what we can learn from it. Philosophical Transactions of the Royal Society of London, 369. Krupic, J., Bauza, M., Burton, S., Lever, C., O’Keefe, J. (2014). How environment geometry affects grid cell symmetry and what we can learn from it. Philosophical Transactions of the Royal Society of London, 369.
go back to reference Krupic, J, Burgess, N, O’Keefe, J. (2012). Neural representations of location composed of spatially periodic bands. Science, 337(6096), 853–857.PubMedPubMedCentral Krupic, J, Burgess, N, O’Keefe, J. (2012). Neural representations of location composed of spatially periodic bands. Science, 337(6096), 853–857.PubMedPubMedCentral
go back to reference Mathis, A, Herz, A.V.M., Stemmler, M. (2012). Optimal population codes for space: grid cells outperform place cells. Neural Computation, 24(9), 2280–2317.PubMed Mathis, A, Herz, A.V.M., Stemmler, M. (2012). Optimal population codes for space: grid cells outperform place cells. Neural Computation, 24(9), 2280–2317.PubMed
go back to reference McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I., Moser, M.B. (2006). Path integration and the neural basis of the ’cognitive map’. Nature Reviews in the Neurosciences, 7, 663–678. McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I., Moser, M.B. (2006). Path integration and the neural basis of the ’cognitive map’. Nature Reviews in the Neurosciences, 7, 663–678.
go back to reference Mhatre, H, Gorchetchnikov, A, Grossberg, S. (2012). Grid cell hexagonal patterns formed by fast self-organized learning within entorhinal cortex. Hippocampus, 22(2), 320–334.PubMed Mhatre, H, Gorchetchnikov, A, Grossberg, S. (2012). Grid cell hexagonal patterns formed by fast self-organized learning within entorhinal cortex. Hippocampus, 22(2), 320–334.PubMed
go back to reference Moser, E.I., & Moser, M.-B. (2013). Grid cells and neural coding in high-end cortices. Neuron, 80. Moser, E.I., & Moser, M.-B. (2013). Grid cells and neural coding in high-end cortices. Neuron, 80.
go back to reference Moser, E.I., Roudi, Y., Witter, M.P., Kentros, C, Bonhoeffer, T, Moser, M.-B. (2014). Grid cells and cortical representation. Nature Reviews Neuroscience, 15, 466–481.PubMed Moser, E.I., Roudi, Y., Witter, M.P., Kentros, C, Bonhoeffer, T, Moser, M.-B. (2014). Grid cells and cortical representation. Nature Reviews Neuroscience, 15, 466–481.PubMed
go back to reference Oja, E. (1982). Simplified neuron model as a principal component analyzer. Journal of Mathematical Biology, 15(3), 267–273.PubMed Oja, E. (1982). Simplified neuron model as a principal component analyzer. Journal of Mathematical Biology, 15(3), 267–273.PubMed
go back to reference Oja, E. (1992). Principal components, minor components, and linear neural networks. Neural Networks, 5(6), 927–935. Oja, E. (1992). Principal components, minor components, and linear neural networks. Neural Networks, 5(6), 927–935.
go back to reference Orchard, J, Yang, H, Ji, X. (2013). Does the entorhinal cortex use the fourier transform? Frontiers in Computational Neuroscience, 7, 179.PubMedPubMedCentral Orchard, J, Yang, H, Ji, X. (2013). Does the entorhinal cortex use the fourier transform? Frontiers in Computational Neuroscience, 7, 179.PubMedPubMedCentral
go back to reference Renart, A., Song, P., Wang, X.J. (2003). Robust spatial working memory through homeostatic synaptic scaling in heterogeneous cortical networks. Neuron, 38, 473–485.PubMed Renart, A., Song, P., Wang, X.J. (2003). Robust spatial working memory through homeostatic synaptic scaling in heterogeneous cortical networks. Neuron, 38, 473–485.PubMed
go back to reference Domínguez, U.R., & Caplan, J.B. (2018). A hexagonal fourier model of grid cells. Hippocampus, 09. Domínguez, U.R., & Caplan, J.B. (2018). A hexagonal fourier model of grid cells. Hippocampus, 09.
go back to reference Sargolini, F, Fyhn, M, Hafting, T, McNaughton, B.L., Witter, M.P., Moser, M -B, Moser, E.I. (2006). Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science, 312(5774), 758–762.PubMed Sargolini, F, Fyhn, M, Hafting, T, McNaughton, B.L., Witter, M.P., Moser, M -B, Moser, E.I. (2006). Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science, 312(5774), 758–762.PubMed
go back to reference Schmidt-Hieber, C., & Häusser, M. (2013). Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nature Neuroscience, 16, 325–331.PubMed Schmidt-Hieber, C., & Häusser, M. (2013). Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nature Neuroscience, 16, 325–331.PubMed
go back to reference Botvinick, M. M., Stachenfeld, K. L., Gershman, S. J. (2017). The hippocampus as a predictive map. Nature Neuroscisnce. Botvinick, M. M., Stachenfeld, K. L., Gershman, S. J. (2017). The hippocampus as a predictive map. Nature Neuroscisnce.
go back to reference Stachenfeld, K.L., Botvinick, MM, Gershman, SJ. (2017). The hippocampus as a predictive map. Nature Neuroscience, 20, 1643–1653.PubMed Stachenfeld, K.L., Botvinick, MM, Gershman, SJ. (2017). The hippocampus as a predictive map. Nature Neuroscience, 20, 1643–1653.PubMed
go back to reference Staudigl, T, Leszczynski, M, Jacobs, J, Sheth, S.A., Schroeder, C.E., Jensen, O, Doeller, C.F. (2018). Hexadirectional modulation of high-frequency electrophysiological activity in the human anterior medial temporal lobe maps visual space. Current Biology, 28(20), 3325–3329.e4.PubMed Staudigl, T, Leszczynski, M, Jacobs, J, Sheth, S.A., Schroeder, C.E., Jensen, O, Doeller, C.F. (2018). Hexadirectional modulation of high-frequency electrophysiological activity in the human anterior medial temporal lobe maps visual space. Current Biology, 28(20), 3325–3329.e4.PubMed
go back to reference Urdapilleta, E., Troiani, F., Stella, F., Treves, A. (2015). Can rodents conceive hyperbolic spaces? Journal of the Royal Society Interface, 12, 107. Urdapilleta, E., Troiani, F., Stella, F., Treves, A. (2015). Can rodents conceive hyperbolic spaces? Journal of the Royal Society Interface, 12, 107.
go back to reference Vágó, L., & Ujfalussy, B.B. (2018). Robust and efficient coding with grid cells. PLOS Computational Biology, 14(1), 1–28. Vágó, L., & Ujfalussy, B.B. (2018). Robust and efficient coding with grid cells. PLOS Computational Biology, 14(1), 1–28.
go back to reference Yartsev, M.M., Witter, M.P., Ulanovsky, N. (2011). Grid cells without theta oscillations in the entorhinal cortex of bats. Nature, 479, 103–107.PubMed Yartsev, M.M., Witter, M.P., Ulanovsky, N. (2011). Grid cells without theta oscillations in the entorhinal cortex of bats. Nature, 479, 103–107.PubMed
go back to reference Yoon, H, & Sompolinsky, H. (1998). The effect of correlations on the fisher information of population codes. In Proceedings of the 11th International Conference on Neural Information Processing Systems, NIPS 98 (pp. 167–173). Cambridge: MIT Press. Yoon, H, & Sompolinsky, H. (1998). The effect of correlations on the fisher information of population codes. In Proceedings of the 11th International Conference on Neural Information Processing Systems, NIPS 98 (pp. 167–173). Cambridge: MIT Press.
Metadata
Title
A computational model for grid maps in neural populations
Authors
Fabio Anselmi
Micah M. Murray
Benedetta Franceschiello
Publication date
03-03-2020
Publisher
Springer US
Published in
Journal of Computational Neuroscience / Issue 2/2020
Print ISSN: 0929-5313
Electronic ISSN: 1573-6873
DOI
https://doi.org/10.1007/s10827-020-00742-9

Other articles of this Issue 2/2020

Journal of Computational Neuroscience 2/2020 Go to the issue

Premium Partner