Advertisement

A Model for Grid Firing and Theta-Nested Gamma Oscillations in Layer 2 of the Medial Entorhinal Cortex

  • Matt NolanEmail author
Chapter
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI)

Abstract

Grid cell circuits in the superficial layers of the medial entorhinal cortex have become a focus of considerable experimental and theoretical attention as a model for investigating neural mechanisms of cognition. Together, grid firing and associated theta-nested gamma oscillations can be considered as a minimal set of phenomena which a satisfactory model of superficial entorhinal circuits should account for. The model presented here focuses on stellate cells in layer 2 (L2SCs) and their indirect interactions through inhibitory interneurons. In the model, L2SCs and inhibitory interneurons are represented as distinct excitatory and inhibitory cell populations. To enable investigation of network activity patterns as well as network computations, the model is implemented using spiking exponential integrate and fire neurons. The model demonstrates that indirect interactions between L2SCs mediated via inhibitory neurons are sufficient for emergence of grid firing and nested game oscillations.

Keywords

Attractor network Grid cell Path integration Neural computation Neural circuit Excitatory-inhibitory interaction Gamma oscillation Theta oscillation 

References

  1. Alonso A, Klink R (1993) Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol 70:128–143CrossRefGoogle Scholar
  2. Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687–2698CrossRefGoogle Scholar
  3. Beed P, Bendels MH, Wiegand HF, Leibold C, Johenning FW, Schmitz D (2010) Analysis of excitatory microcircuitry in the medial entorhinal cortex reveals cell-type-specific differences. Neuron 68:1059–1066CrossRefGoogle Scholar
  4. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser MB (2010) Grid cells in pre- and parasubiculum. Nat Neurosci 13:987–994CrossRefGoogle Scholar
  5. Bonnevie T, Dunn B, Fyhn M, Hafting T, Derdikman D, Kubie JL, Roudi Y, Moser EI, Moser MB (2013) Grid cells require excitatory drive from the hippocampus. Nat Neurosci 16:309–317CrossRefGoogle Scholar
  6. Burak Y, Fiete IR (2009) Accurate path integration in continuous attractor network models of grid cells. PLoS Comput Biol 5:e1000291CrossRefGoogle Scholar
  7. Bush D, Burgess N (2014) A hybrid oscillatory interference/continuous attractor network model of grid cell firing. J Neurosci 34:5065–5079CrossRefGoogle Scholar
  8. Chrobak JJ, Buzsaki G (1998) Gamma oscillations in the entorhinal cortex of the freely behaving rat. J Neurosci 18:388–398CrossRefGoogle Scholar
  9. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI (2009) Frequency of gamma oscillations routes flow of information in the hippocampus. Nature 462:353–357CrossRefGoogle Scholar
  10. Couey JJ, Witoelar A, Zhang SJ, Zheng K, Ye J, Dunn B, Czajkowski R, Moser MB, Moser EI, Roudi Y et al (2013) Recurrent inhibitory circuitry as a mechanism for grid formation. Nat Neurosci 16:318–324CrossRefGoogle Scholar
  11. Dhillon A, Jones RS (2000) Laminar differences in recurrent excitatory transmission in the rat entorhinal cortex in vitro. Neuroscience 99:413–422CrossRefGoogle Scholar
  12. Dickson CT, Magistretti J, Shalinsky MH, Fransen E, Hasselmo ME, Alonso A (2000) Properties and role of I(h) in the pacing of subthreshold oscillations in entorhinal cortex layer II neurons. J Neurophysiol 83:2562–2579CrossRefGoogle Scholar
  13. Dodson PD, Pastoll H, Nolan MF (2011) Dorsal-ventral organization of theta-like activity intrinsic to entorhinal stellate neurons is mediated by differences in stochastic current fluctuations. J Physiol 589:2993–3008CrossRefGoogle Scholar
  14. Domnisoru C, Kinkhabwala AA, Tank DW (2013) Membrane potential dynamics of grid cells. Nature 495:199–204CrossRefGoogle Scholar
  15. Dudman JT, Nolan MF (2009) Stochastically gating ion channels enable patterned spike firing through activity-dependent modulation of spike probability. PLoS Comput Biol 5:e1000290CrossRefGoogle Scholar
  16. Faisal AA, Selen LP, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9:292–303CrossRefGoogle Scholar
  17. Fourcaud-Trocme N, Hansel D, van Vreeswijk C, Brunel N (2003) How spike generation mechanisms determine the neuronal response to fluctuating inputs. J Neurosci 23:11628–11640CrossRefGoogle Scholar
  18. Fransen E, Alonso AA, Dickson CT, Magistretti J, Hasselmo ME (2004) Ionic mechanisms in the generation of subthreshold oscillations and action potential clustering in entorhinal layer II stellate neurons. Hippocampus 14:368–384CrossRefGoogle Scholar
  19. Fuchs EC, Neitz A, Pinna R, Melzer S, Caputi A, Monyer H (2016) Local and distant input controlling excitation in layer II of the medial entorhinal cortex. Neuron 89:194–208CrossRefGoogle Scholar
  20. Fuhs MC, Touretzky DS (2006) A spin glass model of path integration in rat medial entorhinal cortex. J Neurosci 26:4266–4276CrossRefGoogle Scholar
  21. Fyhn M, Molden S, Witter MP, Moser EI, Moser MB (2004) Spatial representation in the entorhinal cortex. Science 305:1258–1264CrossRefGoogle Scholar
  22. Garden DL, Dodson PD, O'Donnell C, White MD, Nolan MF (2008) Tuning of synaptic integration in the medial entorhinal cortex to the organization of grid cell firing fields. Neuron 60:875–889CrossRefGoogle Scholar
  23. Giocomo LM, Zilli EA, Fransen E, Hasselmo ME (2007) Temporal frequency of subthreshold oscillations scales with entorhinal grid cell field spacing. Science 315:1719–1722CrossRefGoogle Scholar
  24. Guanella A, Kiper D, Verschure P (2007) A model of grid cells based on a twisted torus topology. Int J Neural Syst 17:231–240CrossRefGoogle Scholar
  25. Hafting T, Fyhn M, Bonnevie T, Moser MB, Moser EI (2008) Hippocampus-independent phase precession in entorhinal grid cells. Nature 453:1248–1252CrossRefGoogle Scholar
  26. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806CrossRefGoogle Scholar
  27. Jones RS (1994) Synaptic and intrinsic properties of neurons of origin of the perforant path in layer II of the rat entorhinal cortex in vitro. Hippocampus 4:335–353CrossRefGoogle Scholar
  28. Kitamura T, Macdonald CJ, Tonegawa S (2015) Entorhinal-hippocampal neuronal circuits bridge temporally discontiguous events. Learn Mem 22:438–443CrossRefGoogle Scholar
  29. Kitamura T, Pignatelli M, Suh J, Kohara K, Yoshiki A, Abe K, Tonegawa S (2014) Island cells control temporal association memory. Science 343:896–901CrossRefGoogle Scholar
  30. Klink R, Alonso A (1997) Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex. Hippocampus 7:571–583CrossRefGoogle Scholar
  31. Kropff E, Carmichael JE, Moser MB, Moser EI (2015) Speed cells in the medial entorhinal cortex. Nature 523:419–424CrossRefGoogle Scholar
  32. McNaughton BL, Battaglia FP, Jensen O, Moser EI, Moser MB (2006) Path integration and the neural basis of the 'cognitive map'. Nat Rev Neurosci 7:663–678CrossRefGoogle Scholar
  33. Mizuseki K, Sirota A, Pastalkova E, Buzsaki G (2009) Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64:267–280CrossRefGoogle Scholar
  34. Moser EI, Moser MB (2013) Grid cells and neural coding in high-end cortices. Neuron 80:765–774CrossRefGoogle Scholar
  35. Navratilova Z, Giocomo LM, Fellous JM, Hasselmo ME, McNaughton BL (2012) Phase precession and variable spatial scaling in a periodic attractor map model of medial entorhinal grid cells with realistic after-spike dynamics. Hippocampus 22:772–789CrossRefGoogle Scholar
  36. Nolan MF, Dudman JT, Dodson PD, Santoro B (2007) HCN1 channels control resting and active integrative properties of stellate cells from layer II of the entorhinal cortex. J Neurosci 27:12440–12451CrossRefGoogle Scholar
  37. O'Keefe J, Burgess N (2005) Dual phase and rate coding in hippocampal place cells: theoretical significance and relationship to entorhinal grid cells. Hippocampus 15:853–866CrossRefGoogle Scholar
  38. Pastoll H, Ramsden HL, Nolan MF (2012) Intrinsic electrophysiological properties of entorhinal cortex stellate cells and their contribution to grid cell firing fields. Front Neural Circuits 6:17CrossRefGoogle Scholar
  39. Pastoll H, Solanka L, van Rossum MC, Nolan MF (2013) Feedback inhibition enables theta-nested gamma oscillations and grid firing fields. Neuron 77:141–154CrossRefGoogle Scholar
  40. Raudies F, Brandon MP, Chapman GW, Hasselmo ME (2015) Head direction is coded more strongly than movement direction in a population of entorhinal neurons. Brain Res 1621:355–367CrossRefGoogle Scholar
  41. Ray S, Naumann R, Burgalossi A, Tang Q, Schmidt H, Brecht M (2014) Grid-layout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex. Science 343:891–896CrossRefGoogle Scholar
  42. Rowland DC, Weible AP, Wickersham IR, Wu H, Mayford M, Witter MP, Kentros CG (2013) Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J Neurosci 33:14889–14898CrossRefGoogle Scholar
  43. Samsonovich A, McNaughton BL (1997) Path integration and cognitive mapping in a continuous attractor neural network model. J Neurosci 17:5900–5920CrossRefGoogle Scholar
  44. Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–762CrossRefGoogle Scholar
  45. Schmidt-Hieber C, Hausser M (2013) Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat Neurosci 16:325–331CrossRefGoogle Scholar
  46. Solanka L, van Rossum MC, Nolan MF (2015) Noise promotes independent control of gamma oscillations and grid firing within recurrent attractor networks. elife 4:e06444CrossRefGoogle Scholar
  47. Steffenach HA, Witter M, Moser MB, Moser EI (2005) Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45:301–313CrossRefGoogle Scholar
  48. Sürmeli G, Marcu D-C, McClure C, Garden DLF, Pastoll H, Nolan MF (2015) Molecularly defined circuitry reveals input-output segregation in deep layers of the medial entorhinal cortex. Neuron 88(5):1040–1053CrossRefGoogle Scholar
  49. Tiesinga P, Sejnowski TJ (2009) Cortical enlightenment: are attentional gamma oscillations driven by ING or PING? Neuron 63:727–732CrossRefGoogle Scholar
  50. Tocker G, Barak O, Derdikman D (2015) Grid cells correlation structure suggests organized feedforward projections into superficial layers of the medial entorhinal cortex. Hippocampus 25:1599CrossRefGoogle Scholar
  51. Uhlhaas PJ, Singer W (2012) Neuronal dynamics and neuropsychiatric disorders: toward a translational paradigm for dysfunctional large-scale networks. Neuron 75:963–980CrossRefGoogle Scholar
  52. Varga C, Lee SY, Soltesz I (2010) Target-selective GABAergic control of entorhinal cortex output. Nat Neurosci 13:822–824CrossRefGoogle Scholar
  53. Whittington MA, Cunningham MO, LeBeau FE, Racca C, Traub RD (2011) Multiple origins of the cortical gamma rhythm. Dev Neurobiol 71:92–106CrossRefGoogle Scholar
  54. Widloski J, Fiete IR (2014) A model of grid cell development through spatial exploration and spike time-dependent plasticity. Neuron 83:481–495CrossRefGoogle Scholar
  55. Zhang K (1996) Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory. J Neurosci 16:2112–2126CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Centre for Integrative PhysiologyUniversity of EdinburghEdinburghUK

Personalised recommendations