Hippocampal Theta Modulation of Neocortical Spike Times and Gamma Rhythm: A Biophysical Model Study

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Spaak, Eelke ^a   Zeitler, Magteld ^b   Gielen, Stan ^b  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b RADBOUD UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOPHYSICAL MODEL; CELL SYNCHRONIZATION; CONDUCTANCE; CONTROLLED STUDY; GABAERGIC SYSTEM; GAMMA RHYTHM; HIPPOCAMPUS THETA RHYTHM; INTERNEURON; MODEL; NEOCORTEX; NERVE CELL; OSCILLATION; PYRAMIDAL NERVE CELL; SPIKE; SPIKE WAVE;

ACTION POTENTIALS; ALGORITHMS; ANIMALS; BIOPHYSICAL PHENOMENA; HIPPOCAMPUS; HUMANS; INTERNEURONS; MODELS, NEUROLOGICAL; NEOCORTEX; NERVE NET; PYRAMIDAL CELLS; SYNAPSES; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 84867017354     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0045688     Document Type: Article

References (65)

1. Buzsáki G, (2002) Theta oscillations in the hippocampus. Neuron 33: 325-340.
2. Buzsáki G, Draguhn A, (2004) Neuronal oscillations in cortical networks. Science 304: 1926-1929.
3. OKeefe J, Recce ML, (1993) Phase relationship between hippocampal place units and the eeg theta rhythm. Hippocampus 3: 317-330.
4. 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: 853-866.
5. Harris KD, Henze DA, Hirase H, Leinekugel X, Dragoi G, et al. (2002) Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417: 738-741.
6. Fries P, (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends in Cognitive Sciences 9: 474-480.
7. Gray CM, König P, Engel AK, Singer W, (1989) Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reects global stimulus properties. Nature 338: 334-337.
8. Gray CM, Singer W, (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proceedings of the National Academy of Sciences 86: 1698-1702.
9. Lavenex P, Amaral DG (2000) Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus 10.
10. O′Reilly RC, Norman KA, (2002) Hippocampal and neocortical contributions to memory: Advances in the complementary learning systems framework. Trends in Cognitive Sciences 6: 505-510.
11. Dolan RJ, Fletcher PC, (1997) Dissociating prefrontal and hippocampal function in episodic memory encoding. Nature 388: 582-585.
12. Eichenbaum H, (2000) A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience 1: 41-50.
13. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, et al. (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60: 683-697.
14. Siapas AG, Lubenov EV, Wilson MA, (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46: 141-151.
15. Sirota A, Csicsvari J, Buhl D, Buzsáki G, (2003) Communication between neocortex and hippocampus during sleep in rodents. Proceedings of the National Academy of Sciences 100: 2065-2069.
16. Jones MW, Wilson MA, (2005) Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15: 867-873.
17. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, et al. (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313: 1626-1628.
18. Voytek B, Canolty RT, Shestyuk A, Crone NE, Parvizi J, et al. (2010) Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks. Frontiers in Human Neuroscience 4.
19. Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger C, et al. (2010) Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proceedings of the National Academy of Sciences 107: 3228.
20. Bartos M, Vida I, Jonas P, (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nature Reviews Neuroscience 8: 45-56.
21. Börgers C, Kopell N, (2003) Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity. Neural Computation 15: 509-538.
22. Tamás G, Buhl EH, Lörincz A, Somogyi P, (2000) Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nature Neuroscience 3: 366-371.
23. Galarreta M, Hestrin S, (1999) A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402: 72-75.
24. Gibson JR, Beierlein M, Connors BW, (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79.
25. Wang XJ, Buzsáki G, (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. Journal of Neuroscience 16: 6402-6413.
26. Sohal VS, Huguenard JR, (2005) Inhibitory coupling specifically generates emergent gamma oscillations in diverse cell types. Proceedings of the National Academy of Sciences 102: 18638-18643.
27. Cardin JA, Carlén M, Meletis K, Knoblich U, Zhang F, et al. (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459: 663-667.
28. Vida I, Bartos M, Jonas P, (2006) Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 49: 107-117.
29. Dégenètais E, Thierry AM, Glowinski J, Gioanni Y, (2003) Synaptic inuence of hippocampus on pyramidal cells of the rat prefrontal cortex: an in vivo intracellular recording study. Cerebral Cortex 13: 782-792.
30. Rosene DL, Van Hoesen GW, (1977) Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science 198: 315-317.
31. Tierney PL, Degenetais E, Thierry AM, Glowinski J, Gioanni Y, (2004) Inuence of the hippocampus on interneurons of the rat prefrontal cortex. European Journal of Neuroscience 20: 514.
32. Gabbott P, Headlam A, Busby S, (2002) Morphological evidence that CA1 hippocampal afferents monosynaptically innervate PV-containing neurons and NADPH-diaphorase reactive cells in the medial prefrontal cortex (areas 25/32) of the rat. Brain Research 946: 314-322.
33. Hodgkin AL, Huxley AF, (1952) A quantitative description of membrane current and its applications to conduction and excitation in nerve. The Journal of Physiology 117: 500-544.
34. Hines ML, Carnevale NT, (1997) The NEURON simulation environment. Neural Computation 9: 1179-1209.
35. Kopell N, Ermentrout B, (2004) Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. Proceedings of the National Academy of Sciences 101: 15482-15487.
36. Gloveli T, Dugladze T, Saha S, Monyer H, Heinemann U, et al. (2005) Differential involvement of oriens/pyramidale interneurones in hippocampal network oscillations in vitro. The Journal of Physiology 562: 131-147.
37. Fries P, Nikolic' D, Singer W, (2007) The gamma cycle. Trends in Neurosciences 30: 309-316.
38. Csicsvari J, Jamieson B, Wise KD, Buzski G, (2003) Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37: 311-322.
39. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, et al. (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47: 423-435.
40. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, et al. (2002) Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proceedings of the National Academy of Sciences 99: 13222-13227.
41. Kahana MJ, Seelig D, Madsen JR, (2001) Theta returns. Current Opinion in Neurobiology 11: 739-744.
42. Pettersen KH, Lindén H, Dale AM, Einevoll GT (August 2012) Extracellular spikes and currentsource density. In: Handbook of neural activity measurement, Cambridge University Press.
43. Bdard C, Krger H, Destexhe A, (2004) Modeling extracellular field potentials and the Frequency-Filtering properties of extracellular space. Biophysical Journal 86: 1829-1842.
44. Izhikevich E, (2004) Which model to use for cortical spiking neurons? IEEE Transactions on Neural Networks 15: 1063-1070.
45. Mazzoni A, Whittingstall K, Brunel N, Logothetis NK, Panzeri S, (2010) Understanding the relationships between spike rate and delta/gamma frequency bands of LFPs and EEGs using a local cortical network model. NeuroImage 52: 956-972.
46. Baranauskas G, Maggiolini E, Vato A, Angotzi G, Bonfanti A, et al. (2012) Origins of 1/F2 scaling in the power spectrum of intracortical local field potential. Journal of Neurophysiology 107: 984-994.
47. Buhl EH, Tams G, Fisahn A, (1998) Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. The Journal of Physiology 513: 117-126.
48. Cunningham MO, Davies CH, Buhl EH, Kopell N, Whittington MA, (2003) Gamma oscillations induced by kainate receptor activation in the entorhinal cortex in vitro. The Journal of Neuroscience 23: 9761-9769.
49. Lin S, Gervasoni D, Nicolelis M, (2006) Fast modulation of prefrontal cortex activity by basal forebrain noncholinergic neuronal ensembles. Journal of Neurophysiology 96: 3209.
50. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, et al. (2005) An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. Journal of Neurophysiology 94: 1904-1911.
51. Canolty RT, Knight RT, (2010) The functional role of cross-frequency coupling. Trends in cognitive sciences 14: 506-515.
52. Jensen O, Bonnefond M, VanRullen R (2012) An oscillatory mechanism for prioritizing salient unattended stimuli. Trends in cognitive sciences.
53. Mathewson K, Gratton G, Fabiani M, Beck D, Ro T, (2009) To see or not to see: prestimulus _phase predicts visual awareness. The Journal of Neuroscience 29: 2725-2732.
54. Busch N, Dubois J, VanRullen R, (2009) The phase of ongoing eeg oscillations predicts visual perception. The Journal of Neuroscience 29: 7869-7876.
55. Osipova D, Hermes D, Jensen O, (2008) Gamma power is phase-locked to posterior alpha activity. PLoS ONE 3: e3990.
56. Händel B, Haarmeier T, Jensen O, (2011) Alpha oscillations correlate with the successful inhibition of unattended stimuli. Journal of Cognitive Neuroscience 23: 2494-2502.
57. Bartos M, Vida I, Frotscher M, Geiger JRP, Jonas P, (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. Journal of Neuroscience 21: 2687.
58. Buhl EH, Cobb SR, Halasy K, Somogyi P, (1995) Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus. European Journal of Neuroscience 7: 1989-2004.
59. Chance FS, Abbott LF, Reyes AD, (2002) Gain modulation from background synaptic input. Neuron 35: 773-782.
60. Kleppe IC, Robinson HPC, (1999) Determining the activation time course of synaptic AMPA receptors from openings of colocalized NMDA receptors. Biophysical Journal 77: 1418-1427.
61. Gabbiani F, Midtgaard J, Knopfel T, (1994) Synaptic integration in a model of cerebellar granule cells. Journal of Neurophysiology 72: 999-1009.
62. Venance L, Rozov A, Blatow M, Burnashev N, Feldmeyer D, et al. (2000) Connexin expression in electrically coupled postnatal rat brain neurons. Proceedings of the National Academy of Sciences 97: 10260-10265.
63. Traub RD, Kopell N, Bibbig A, Buhl EH, LeBeau FEN, et al. (2001) Gap junctions between interneuron dendrites can enhance synchrony of gamma oscillations in distributed networks. Journal of Neuroscience 21: 9478.
64. Hirase H, Leinekugel X, Czurkó A, Csicsvari J, Buzsáki G, (2001) Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience. Proceedings of the National Academy of Sciences 98: 9386.
65. Liley DTJ, Wright JJ, (1994) Intracortical connectivity of pyramidal and stellate cells: estimates of synaptic densities and coupling symmetry. Network: Computation in Neural Systems 5: 175-189.