Ketamine disrupts theta modulation of gamma in a computer model of hippocampus

Journal of Neuroscience

Volumn 31, Issue 32, 2011, Pages 11733-11743

  Neymotin, Samuel A ^a   Lazarewicz, Maciej T ^b   Sherif, Mohamed ^a   Contreras, Diego ^c   Finkel, Leif H ^b   Lytton, William W ^a,d  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d KINGS COUNTY HOSPITAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; BASKET CELL; COMPUTER MODEL; ELECTRIC CURRENT; GAMMA RHYTHM; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS THETA RHYTHM; IN VIVO STUDY; NERVE CELL; NERVE CELL STIMULATION; NEUROMODULATION; ORIENS LACUNOSUM MOLECULARE CELL; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SEPTUM PELLUCIDUM;

CA3 REGION, HIPPOCAMPAL; KETAMINE; NEURAL NETWORKS (COMPUTER); RANDOM ALLOCATION; THETA RHYTHM;

EID: 80051565535     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0501-11.2011     Document Type: Article

References (75)

1. Achim AM, Bertrand MC, Sutton H, Montoya A, Czechowska Y, Malla AK, Joober R, Pruessner JC, Lepage M (2007) Selective abnormal modulation of hippocampal activity during memory formation in first-episode psychosis. Arch Gen Psychiatry 64:999-1014.
2. Benes FM, Sorensen I, Bird ED (1991) Reduced neuronal size in posterior hippocampus of schizophrenic patients. Schizoph Bull 17:597-608.
3. Bleuler E (1911) Dementia Praecox oder Gruppe der Schizophrenien. In: Handbuch der Psychiatrie (Aschaffenburg G, ed). Leipzig: Deuticke.
4. Börgers C, Kopell N (2003) Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity. Neural Comput 15:509-538.
5. Bragin A, Jando ́ G, Na ́dasdy Z, Hetke J, Wise K, Buzsa ́ki G (1995) Gamma (40-100 hz) oscillation in the hippocampus of the behaving rat. J Neurosci 15:47-60.
6. Bresink I, Danysz W, Parsons CG, Mutschler E (1995) Different binding affinities of NMDA receptor channel blockers in various brain regions-indication of NMDA receptor heterogeneity. Neuropharmacology 34:533-540.
7. Bubeníkova ́-Valesova ́ V, Hora ́cek J, Vrajova ́ M, Höschl C (2008) Models of schizophrenia in humans and animals based on inhibition of NMDA receptors. Neurosci Biobehav Rev 32:1014-1023.
8. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phaselocked to theta oscillations in human neocortex. Science 313:1626-1628.
9. Cardin JA, Carle ́n M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI (2009) Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459:663-667.
10. Carnevale N, Hines M (2006) The NEURON book. New York: Cambridge UP.
11. Cobb SR, Halasy K, Vida I, Nyiri G, Tama ́s G, Buhl EH, Somogyi P (1997) Synaptic effects of identified interneurons innervating both interneurons and pyramidal cells in the rat hippocampus. Neuroscience 79:629-648.
12. Cull-Candy S, Brickley S, Farrant M (2001) NMDA receptor subunits: diversity, development and disease. Curr Opin Neurobiol 11:327-335.
13. Cutsuridis V, Cobb S, Graham BP (2010) Encoding and retrieval in a model of the hippocampal CA1 microcircuit. Hippocampus 20:423-446.
14. Dean B, Scarr E, Bradbury R, Copolov D (1999) Decreased hippocampal (CA3) NMDA receptors in schizophrenia. Synapse 32:67-69.
15. Destexhe A, Rudolph M, Pare ́ D (2003) The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4:739-751.
16. Ehrlichman RS, Gandal MJ, Maxwell CR, Lazarewicz MT, Finkel LH, Contreras D, Turetsky BI, Siegel SJ (2009) N-Methyl-D-aspartic acid receptor antagonist-induced frequency oscillations in mice recreate pattern of electrophysiological deficits in schizophrenia. Neuroscience 158:705-712.
17. Fries P, Nikolić D, Singer W (2007) The gamma cycle. Trends Neurosci 30:309-316.
18. Goldberger A, Amaral L, Hausdorff J, Ivanov P, Peng C, Stanley H (2002) Fractal dynamics in physiology: alterations with disease and aging. Proc Natl Acad Sci U S A 99S 1:2466-2472.
19. Goure ́vitch B, Eggermont JJ (2007) Evaluating information transfer between auditory cortical neurons. J Neurophysiol 97:2533-2543.
20. Goutagny R, Jackson J, Williams S (2009) Self-generated theta oscillations in the hippocampus. Nat Neurosci 12:1491-1493.
21. Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A 86:1698-1702.
22. Greene R (2001) Circuit analysis of NMDAR hypofunction in the hippocampus, in vitro, and psychosis of schizophrenia. Hippocampus 11:569-577.
23. Grillner S, Markram H, De Schutter E, Silberberg G, LeBeau FE (2005) Microcircuits in action-from CPGs to neocortex. Trends Neurosci 28:525-533.
24. Ha ́jos N, Freund TF, Mody I (2002) Comparison of single NMDA receptor channels recorded on hippocampal principal cells and oriens/alveus interneurons projecting to stratum lacunosum-moleculare (O-LM cells). Acta Biol Hung 53:465-472.
25. Hangya B, Borhegyi Z, Szila ́gyi N, Freund TF, Varga V (2009) GABAergic neurons of the medial septum lead the hippocampal network during theta activity. J Neurosci 29:8094-8102.
26. Heckers S (2001) Neuroimaging studies of the hippocampus in schizophrenia. Hippocampus 11:520-528.
27. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
28. Hines ML, Carnevale NT (2001) NEURON: a tool for neuroscientists. Neuroscientist 7:123-135.
29. Hines ML, Davison AP, Muller E (2009) NEURON and Python. Front Neuroinform 3:1.
30. Holthausen EA, Wiersma D, Sitskoorn MM, Dingemans PM, Schene AH, van den Bosch RJ (2003) Long-term memory deficits in schizophrenia: primary or secondary dysfunction? Neuropsychology 17:539-547.
31. Homayoun H, Moghaddam B (2007) NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 27:11496-11500.
32. Honea R, Crow TJ, Passingham D, Mackay CE (2005) Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am J Psychiatry 162:2233-2245.
33. Hong LE, Summerfelt A, Buchanan RW, O'Donnell P, Thaker GK, Weiler MA, Lahti AC (2010) Gamma and delta neural oscillations and association with clinical symptoms under subanesthetic ketamine. Neuropsychopharmacology 35:632-640.
34. Jackson ME, Homayoun H, Moghaddam B (2004) NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc Natl Acad Sci U S A 101:8467-8472.
35. Jahr CE, Stevens CF (1990) Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics. J Neurosci 10:3178-3182.
36. Jessen F, Scheef L, Germeshausen L, Tawo Y, Kockler M, Kuhn KU, Maier W, Schild HH, Heun R (2003) Reduced hippocampal activation during encoding and recognition of words in schizophrenia patients. Am J Psychiatry 160:1305-1312.
37. Kelemen E, Fenton AA (2010) Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. PLoS Biol 8:e1000403.
38. Kiss T, Orba ́n G, Lengyel M, Erdi P (2001) Intrahippocampal gamma and theta rhythm generation in a network model of inhibitory interneurons. Neurocomputing 38:713-719.
39. Kolomeets NS, Orlovskaya DD, Uranova NA (2007) Decreased numerical density of CA3 hippocampal mossy fiber synapses in schizophrenia. Synapse 61:615-621.
40. Lazarewicz MT, Ehrlichman RS, Maxwell CR, Gandal MJ, Finkel LH, Siegel SJ (2010) Ketamine modulates theta and gamma oscillations. J Cogn Neurosci 22:1452-1464.
41. Lisman J, Buzsa ́ki G (2008) A neural coding scheme formed by the combined function of gamma and theta oscillations. Schizophr Bull 34:974-980.
42. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S, Grace AA (2008) Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 31:234-242.
43. Lytton WW (2006) Neural query system: data-mining from within the NEURON simulator. Neuroinformatics 4:163-176.
44. Lytton WW (2008) Computer modelling of epilepsy. Nat Rev Neurosci 9:626-637.
45. Lytton WW, Sejnowski TJ (1991) Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J Neurophysiol 66:1059-1079.
46. Malhotra AK, Pinals DA, Weingartner H, Sirocco K, Missar CD, Pickar D, Breier A (1996) NMDA receptor function and human cognition: the effects of ketamine in healthy volunteers. Neuropsychopharmacology 14:301-307.
47. Malhotra AK, Pinals DA, Adler CM, Elman I, Clifton A, Pickar D, Breier A (1997) Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology 17:141-150.
48. Narr KL, Thompson PM, Szeszko P, Robinson D, Jang S, Woods RP, Kim S, Hayashi KM, Asunction D, Toga AW, Bilder RM (2004) Regional specificity of hippocampal volume reductions in first-episode schizophrenia. Neuroimage 21:1563-1575.
49. Newcomer JW, Farber NB, Jevtovic-Todorovic V, Selke G, Melson AK, Hershey T, Craft S, Olney JW (1999) Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis. Neuropsychopharmacology 20:106-118.
50. Neymotin SA, Jacobs KM, Fenton AA, Lytton WW (2011a) Synaptic information transfer in computer models of neocortical columns. J Comput Neurosci 30:69-84.
51. Neymotin SA, Lee H, Park E, Fenton AA, Lytton WW (2011b) Emergence of physiological oscillation frequencies in a computer model of neocortex. Front Comput Neurosci 5:19.
52. Nyíri G, Stephenson FA, Freund T, Somogyi P (2003) Large variability in synaptic N-methyl-D-aspartate receptor density on interneurons and a comparison with pyramidal-cell spines in the rat hippocampus. Neuroscience 119:347-363.
53. Olypher AV, Klement D, Fenton AA (2006) Cognitive disorganization in hippocampus: a physiological model of the disorganization in psychosis. J Neurosci 26:158-168.
54. Oppenheim A, Schafer R, Buck J (1999) Discrete-time signal processing, Ed 2. Upper Saddle River, NJ: Prentice Hall.
55. Orbán G, Kiss T, Erdi P (2006) Intrinsic and synaptic mechanisms determining the timing of neuron population activity during hippocampal theta oscillation. J Neurophysiol 96:2889-2904.
56. Parnas J, Bovet P, Zahavi D (2002) Schizophrenic autism: clinical phenomenology and pathogenetic implications. World Psychiatry 1:131-136.
57. Phillips W, Silverstein S (2003) Convergence of biological and psychological perspectives on cognitive coordination in schizophrenia. Behav Brain Sci 26:65-82.
58. Sabolek H, Penley S, Bunce J, Hinman J, Chrobak J (2006) Ketamine alters synchrony throughout the hippocampal formation. Soc Neurosci Abstr 32:751.12.
59. Silberberg G, Grillner S, LeBeau FE, Maex R, Markram H (2005) Synaptic pathways in neural microcircuits. Trends Neurosci 28:541-551.
60. Stacey WC, Lazarewicz MT, Litt B (2009) Synaptic noise and physiological coupling generate high-frequency oscillations in a hippocampal computational model. J Neurophysiol 102:2342-2357.
61. Stewart M, Fox SE (1990) Do septal neurons pace the hippocampal theta rhythm? Trends Neurosci 13:163-168.
62. Suzuki Y, Jodo E, Takeuchi S, Niwa S, Kayama Y (2002) Acute administration of phencyclidine induces tonic activation of medial prefrontal cortex neurons in freely moving rats. Neuroscience 114:769-779.
63. Szeszko PR, Goldberg E, Gunduz-Bruce H, Ashtari M, Robinson D, Malhotra AK, Lencz T, Bates J, Crandall DT, Kane JM, Bilder RM (2003) Smaller anterior hippocampal formation volume in antipsychotic-naive patients with first-episode schizophrenia. Am J Psychiatry 160:2190-2197.
64. Tamminga CA, Stan AD, Wagner AD (2010) The hippocampal formation in schizophrenia. Am J Psychiatry 167:1178-1193.
65. Tiesinga P, Sejnowski TJ (2009) Cortical enlightenment: are attentional gamma oscillations driven by ING or PING? Neuron 63:727-732.
66. Tort AB, Rotstein HG, Dugladze T, Gloveli T, Kopell NJ (2007) On the formation of gamma-coherent cell assemblies by oriens lacunosummoleculare interneurons in the hippocampus. Proc Natl Acad Sci U S A 104:13490-13495.
67. Uhlhaas PJ, Silverstein SM (2005) Perceptual organization in schizophrenia spectrum disorders: empirical research and theoretical implications. Psychol Bull 131:618-632.
68. Uhlhaas PJ, Singer W (2006) Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52:155-168.
69. Uhlhaas PJ, Phillips WA, Mitchell G, Silverstein SM (2006a) Perceptual grouping in disorganized schizophrenia. Psychiatry Res 145:105-117.
70. Uhlhaas PJ, Phillips WA, Schenkel LS, Silverstein SM (2006b) Theory of mind and perceptual context-processing in schizophrenia. Cogn Neuropsychiatry 11:416-436.
71. Wang XJ (2002) Pacemaker neurons for the theta rhythm and their synchronization in the septohippocampal reciprocal loop. J Neurophysiol 87:889-900.
72. Wang XJ, Buzsa ́ki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16:6402-6413.
73. White JA, Banks MI, Pearce RA, Kopell NJ (2000) Networks of interneurons with fast and slow GABA type A (GABAA) kinetics provide substrate for mixed gamma-theta rhythm. Proc Natl Acad Sci U S A 97:8128-8133.
74. Whittington MA, Traub RD, Kopell N, Ermentrout B, Buhl EH (2000) Inhibition-based rhythms: experimental and mathematical observations on network dynamics. Int J Psychophysiol 38:315-336.
75. Zaidel DW, Esiri MM, Harrison PJ (1997) Size, shape, and orientation of neurons in the left and right hippocampus: investigation of normal asymmetries and alterations in schizophrenia. Am J Psychiatry 154:812-818.