Interconnection and synchronization of neuronal populations in the mouse medial septum/diagonal band of Broca

Journal of Neurophysiology

Volumn 113, Issue 3, 2015, Pages 971-980

  Leão, Richardson N ^a,b   Targino, Zé H ^b   Colom, Luis V ^c   Fisahn, André ^d  

^a UPPSALA UNIVERSITY   (Sweden)

^b FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^c UNIVERSITY OF TEXAS AT BROWNSVILLE   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cholinergic neuron; GABAergic neuron; Glutamatergic neuron; Medial septum; Synchronization; Theta rhythm

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CELL POPULATION; CELL SYNCHRONIZATION; CHOLINERGIC NERVE CELL; COMPUTER MODEL; CONNECTOME; DIAGONAL BAND OF BROCA; HIPPOCAMPUS THETA RHYTHM; MOUSE; NERVE CELL; NONHUMAN; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; SEPTUM PELLUCIDUM; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; FEMALE; MALE; PHYSIOLOGY; SYNAPSE; THETA RHYTHM;

ACTION POTENTIALS; ANIMALS; CHOLINERGIC NEURONS; DIAGONAL BAND OF BROCA; FEMALE; GABAERGIC NEURONS; MALE; MICE; MODELS, NEUROLOGICAL; SEPTUM OF BRAIN; SYNAPSES; THETA RHYTHM;

EID: 84922243801     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00367.2014     Document Type: Article

References (48)

1. Andersen P, Bland HB, Myhrer T, Schwartzkroin PA. Septo-hippocampal pathway necessary for dentate theta production. Brain Res 165: 13–22, 1979.
2. Bañuelos C, LaSarge CL, McQuail JA, Hartman JJ, Gilbert RJ, Ormerod BK, Bizon JL. Age-related changes in rostral basal forebrain cholinergic and GABAergic projection neurons: relationship with spatial impairment. Neurobiol Aging 34: 845–862, 2013.
3. Birgner C, Nordenankar K, Lundblad M, Mendez JA, Smith C, le Grevès M, Galter D, Olson L, Fredriksson A, Trudeau LE, Kullander K, Wallén-Mackenzie A. VGLUT2 in dopamine neurons is required for psychostimulant-induced behavioral activation. Proc Natl Acad Sci USA 107: 389–394, 2010.
4. Bland BH. The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26: 1–54, 1986.
5. Bland BH, Colom LV. Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex. Prog Neurobiol 41: 157–208, 1993.
6. Bland BH, Oddie SD, Colom LV. Mechanisms of neural synchrony in the septohippocampal pathways underlying hippocampal theta generation. J Neurosci 19: 3223–3237, 1999.
7. Börgers C, Talei Franzesi G, Lebeau FE, Boyden ES, Kopell NJ. Minimal size of cell assemblies coordinated by gamma oscillations. PLoS Comput Biol 8: e1002362, 2012.
8. Borgius L, Restrepo CE, Leao RN, Saleh N, Kiehn O. A transgenic mouse line for molecular genetic analysis of excitatory glutamatergic neurons. Mol Cell Neurosci 45: 245–257, 2010.
9. Buzsáki G. Theta oscillations in the hippocampus. Neuron 33: 325–340, 2002.
10. Colom LV. Septal networks: relevance to theta rhythm, epilepsy and Alzheimer’s disease. J Neurochem 96: 609–624, 2006.
11. Colom LV, Castaneda MT, Reyna T, Hernandez S, Garrido-Sanabria E. Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 58: 151–164, 2005.
12. Diamond DM, Dunwiddie TV, Rose GM. Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat. J Neurosci 8: 4079–4088, 1988.
13. Faulkner HJ, Traub RD, Whittington MA. Disruption of synchronous gamma oscillations in the rat hippocampal slice: a common mechanism of anaesthetic drug action. Br J Pharmacol 125: 483–492, 1998.
14. Garner HL, Whittington MA, Henderson Z. Induction by kainate of theta frequency rhythmic activity in the rat medial septum-diagonal band complex in vitro. J Physiol 564: 83–102, 2005.
15. Garrido-Sanabria E., Perez-Cordova MG, Colom LV. Differential expression of voltage-gated K_ currents in medial septum/diagonal band complex neurons exhibiting distinct firing phenotypes. Neurosci Res 70: 361–369, 2011.
16. Gaspar P, Berger B, Lesur A, Borsotti JP, Febvret A. Somatostatin 28 and neuropeptide Y innervation in the septal area and related cortical and subcortical structures of the human brain. Distribution, relationships and evidence for differential coexistence. Neuroscience 22: 49–73, 1987.
17. Glasgow SD, Chapman CA. Conductances mediating intrinsic theta-frequency membrane potential oscillations in layer II parasubicular neurons. J Neurophysiol 100: 2746–2756, 2008.
18. Goodman D, Brette R. Brian: a simulator for spiking neural networks in Python. Front Neuroinformatics 2: 5, 2008.
19. Henderson Z, Lu CB, Janzsó G, Matto N, McKinley CE, Yanagawa Y, Halasy K. Distribution and role of Kv3.1b in neurons in the medial septum diagonal band complex. Neuroscience 166: 952–969, 2010.
20. Hilscher MM, Leão KE, Leão RN. Synchronization through nonreciprocal connections in a hybrid hippocampus microcircuit. Front Neural Circuits 7: 120, 2013.
21. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 500–544, 1952.
22. Hu H, Vervaeke K, Storm JF. Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na_ current in rat hippocampal pyramidal cells. J Physiol 545: 783–805, 2002.
23. Huh CY, Goutagny R, Williams S. Glutamatergic neurons of the mouse medial septum and diagonal band of Broca synaptically drive hippocampal pyramidal cells: relevance for hippocampal theta rhythm. J Neurosci 30: 15951–15961, 2010.
24. Hung CP, Ramsden BM, Roe AW. Weakly modulated spike trains: significance, precision, and correction for sample size. J Neurophysiol 87: 2542–2554, 2002.
25. Jensen O, Lisman JE. Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. J Neurophysiol 83: 2602–2609, 2000.
26. Kiss J, Csáki A, Bokor H, Shanabrough M, Leranth C. The supramammillo- hippocampal and supramammillo-septal glutamatergic/aspartatergic projections in the rat: a combined [3H]D-aspartate autoradiographic and immunohistochemical study. Neuroscience 97: 657–669, 2000.
27. Kocsis B, Li S. In vivo contribution of h-channels in the septal pacemaker to theta rhythm generation. Eur J Neurosci 20: 2149–2158, 2004.
28. Leao RN, Colom LV, Borgius L, Kiehn O, Fisahn A. Medial septal dysfunction by A_-induced KCNQ channel-block in glutamatergic neurons. Neurobiol Aging 33: 2046–2061, 2012.
29. Leao RN, Leao FN, Walmsley B. Non-random nature of spontaneous mIPSCs in mouse auditory brainstem neurons revealed by recurrence quantification analysis. Proc Biol Sci 272: 2551–2559, 2005.
30. Leao RN, Tan HM, Fisahn A. Kv7/KCNQ channels control action potential phasing of pyramidal neurons during hippocampal gamma oscillations in vitro. J Neurosci 29: 13353–13364, 2009.
31. Manseau F, Goutagny R, Danik M, Williams S. The hippocamposeptal pathway generates rhythmic firing of GABAergic neurons in the medial septum and diagonal bands: an investigation using a complete septohippocampal preparation in vitro. J Neurosci 28: 4096–4107, 2008.
32. Marwan N, Wessel N, Meyerfeldt U, Schirdewan A, Kurths J. Recurrenceplot- based measures of complexity and their application to heart-ratevariability data. Phys Rev E Stat Nonlin Soft Matter Phys 66: 026702, 2002.
33. Mehta MR. Role of rhythms in facilitating short-term memory. Neuron 45: 7–9, 2005.
34. Mitchell SJ, Rawlins JN, Steward O, Olton DS. Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial cortex and produce impaired radial arm maze behavior in rats. J Neurosci 2: 292–302, 1982.
35. Morris NP, Fyffe RE, Robertson B. Characterisation of hyperpolarizationactivated currents (Ih) in the medial septum/diagonal band complex in the mouse. Brain Res 1006: 74–86, 2004.
36. Osten P, Margrie TW. Mapping brain circuitry with a light microscope. Nat Methods 10: 515–523, 2013.
37. Simon AP, Poindessous-Jazat F, Dutar P, Epelbaum J, Bassant MH. Firing properties of anatomically identified neurons in the medial septum of anesthetized and unanesthetized restrained rats. J Neurosci 26: 9038–9046, 2006.
38. Sotty F, Danik M, Manseau F, Laplante F, Quirion R, Williams S. Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J Physiol 551: 927–943, 2003.
39. Stewart M, Fox SE. Firing relations of medial septal neurons to the hippocampal theta rhythm in urethane anesthetized rats. Exp Brain Res 77: 507–516, 1989.
40. Teles-Grilo Ruivo LM, Mellor JR. Cholinergic modulation of hippocampal network function. Front Synaptic Neurosci 5: 2, 2013.
41. Traub RD, Whittington MA, Colling SB, Buzsáki G, Jefferys JG. Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 493: 471–484, 1996.
42. Unal CT, Golowasch JP, Zaborszky L. Adult mouse basal forebrain harbors two distinct cholinergic populations defined by their electrophysiology. Front Behav Neurosci 6: 21, 2012.
43. Vandecasteele M, Varga V, Berenyi A, Papp E, Bartho P, Venance L, Freund TF, Buzsaki G. Optogenetic activation of septal cholinergic neu- rons suppresses sharp wave ripples and enhances theta oscillations in the hippocampus. Proc Natl Acad Sci USA 111: 13535–13540, 2014.
44. Varga V, Hangya B, Kránitz K, Ludányi A, Zemankovics R, Katona I, Shigemoto R, Freund TF, Borhegyi Z. The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J Physiol 586: 3893–3915, 2008.
45. Vinogradova OS. Expression, control, and probable functional significance of the neuronal theta-rhythm. Prog Neurobiol 45: 523–583, 1995.
46. Wang XJ. Pacemaker neurons for the theta rhythm and their synchronization in the septohippocampal reciprocal loop. J Neurophysiol 87: 889–900, 2002.
47. Wu M, Hajszan T, Xu C, Leranth C, Alreja M. Group I metabotropic glutamate receptor activation produces a direct excitation of identified septohippocampal cholinergic neurons. J Neurophysiol 92: 1216–1225, 2004.
48. Zbilut JP, Webber CL. Embeddings and delays as derived from quantification of recurrence plots. Phys Lett A 171: 199–203, 1992.