Oscillatory activity in developing prefrontal networks results from theta-gamma-modulated synaptic inputs

Cell Reports

Volumn 11, Issue 3, 2015, Pages 486-497

  Bitzenhofer, Sebastian H ^a   Sieben, Kay ^a   Siebert, Kai D ^a   Spehr, Marc ^b   Hanganu Opatz, Ileana L ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL INTERACTION; GABAERGIC TRANSMISSION; GAMMA RHYTHM; HIGH FREQUENCY OSCILLATION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; INTERNEURON; NERVE CELL STIMULATION; NEWBORN; NONHUMAN; OSCILLATORY POTENTIAL; PATCH CLAMP TECHNIQUE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION; THETA RHYTHM; ANIMAL; CONFOCAL MICROSCOPY; GROWTH, DEVELOPMENT AND AGING; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

RATTUS;

ANIMALS; ANIMALS, NEWBORN; GAMMA RHYTHM; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MICROSCOPY, CONFOCAL; NEUROGENESIS; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RATS; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 84928214616     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.03.031     Document Type: Article

References (45)

1. Akam T., Kullmann D.M. Oscillatory multiplexing of population codes for selective communication in the mammalian brain. Nat. Rev. Neurosci. 2014, 15:111-122.
2. Bartos M., Vida I., Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 2007, 8:45-56.
3. Bitzenhofer S.H., Hanganu-Opatz I.L. Oscillatory coupling within neonatal prefrontal-hippocampal networks is independent of selective removal of GABAergic neurons in the hippocampus. Neuropharmacology 2014, 77:57-67.
4. Blaesse P., Airaksinen M.S., Rivera C., Kaila K. Cation-chloride cotransporters and neuronal function. Neuron 2009, 61:820-838.
5. Blatow M., Rozov A., Katona I., Hormuzdi S.G., Meyer A.H., Whittington M.A., Caputi A., Monyer H. A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 2003, 38:805-817.
6. Brockmann M.D., Pöschel B., Cichon N., Hanganu-Opatz I.L. Coupled oscillations mediate directed interactions between prefrontal cortex and hippocampus of the neonatal rat. Neuron 2011, 71:332-347.
7. Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
8. Buzsáki G., Wang X.J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 2012, 35:203-225.
9. Cardin J.A., Carlén M., Meletis K., Knoblich U., Zhang F., Deisseroth K., Tsai L.H., Moore C.I. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009, 459:663-667.
10. Chu J., Anderson S.A. Development of cortical interneurons. Neuropsychopharmacology 2015, 40:16-23.
11. Cichon N.B., Denker M., Grün S., Hanganu-Opatz I.L. Unsupervised classification of neocortical activity patterns in neonatal and pre-juvenile rodents. Front. Neural Circuits 2014, 8:50.
12. Clement E.A., Richard A., Thwaites M., Ailon J., Peters S., Dickson C.T. Cyclic and sleep-like spontaneous alternations of brain state under urethane anaesthesia. PLoS One 2008, 3:e2004.
13. Colonnese M.T. Rapid developmental emergence of stable depolarization during wakefulness by inhibitory balancing of cortical network excitability. J.Neurosci. 2014, 34:5477-5485.
14. Colonnese M.T., Khazipov R. "Slow activity transients" in infant rat visual cortex: a spreading synchronous oscillation patterned by retinal waves. J.Neurosci. 2010, 30:4325-4337.
15. Csicsvari J., Hirase H., Czurkó A., Mamiya A., Buzsáki G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J.Neurosci. 1999, 19:274-287.
16. Dupont E., Hanganu I.L., Kilb W., Hirsch S., Luhmann H.J. Rapid developmental switch in the mechanisms driving early cortical columnar networks. Nature 2006, 439:79-83.
17. Freund T.F., Antal M. GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 1988, 336:170-173.
18. Hafting T., Fyhn M., Molden S., Moser M.B., Moser E.I. Microstructure of a spatial map in the entorhinal cortex. Nature 2005, 436:801-806.
19. Hanganu I.L., Ben-Ari Y., Khazipov R. Retinal waves trigger spindle bursts in the neonatal rat visual cortex. J.Neurosci. 2006, 26:6728-6736.
20. Hanganu-Opatz I.L. Between molecules and experience: role of early patterns of coordinated activity for the development of cortical maps and sensory abilities. Brain Res. Brain Res. Rev. 2010, 64:160-176.
21. Hu H., Gan J., Jonas P. Interneurons. Fast-spiking, parvalbumin[U+207A] GABAergic interneurons: from cellular design to microcircuit function. Science 2014, 345:1255263.
22. Janiesch P.C., Krüger H.S., Pöschel B., Hanganu-Opatz I.L. Cholinergic control in developing prefrontal-hippocampal networks. J.Neurosci. 2011, 31:17955-17970.
23. Karube F., Kubota Y., Kawaguchi Y. Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. J.Neurosci. 2004, 24:2853-2865.
24. Khazipov R., Luhmann H.J. Early patterns of electrical activity in the developing cerebral cortex of humans and rodents. Trends Neurosci. 2006, 29:414-418.
25. Kilb W. Development of the GABAergic system from birth to adolescence. Neuroscientist 2012, 18:613-630.
26. Krüger H.S., Brockmann M.D., Salamon J., Ittrich H., Hanganu-Opatz I.L. Neonatal hippocampal lesion alters the functional maturation of the prefrontal cortex and the early cognitive development in pre-juvenile rats. Neurobiol. Learn. Mem. 2012, 97:470-481.
27. Krupa M., Gielen S., Gutkin B. Adaptation and shunting inhibition leads to pyramidal/interneuron gamma with sparse firing of pyramidal cells. J.Comput. Neurosci. 2014, 37:357-376.
28. Langston R.F., Ainge J.A., Couey J.J., Canto C.B., Bjerknes T.L., Witter M.P., Moser E.I., Moser M.B. Development of the spatial representation system in the rat. Science 2010, 328:1576-1580.
29. Lee A.T., Gee S.M., Vogt D., Patel T., Rubenstein J.L., Sohal V.S. Pyramidal neurons in prefrontal cortex receive subtype-specific forms of excitation and inhibition. Neuron 2014, 81:61-68.
30. Lisman J.E., Jensen O. The θ-γ neural code. Neuron 2013, 77:1002-1016.
31. Minlebaev M., Colonnese M., Tsintsadze T., Sirota A., Khazipov R. Early γ oscillations synchronize developing thalamus and cortex. Science 2011, 334:226-229.
32. Nimmrich V., Maier N., Schmitz D., Draguhn A. Induced sharp wave-ripple complexes in the absence of synaptic inhibition in mouse hippocampal slices. J.Physiol. 2005, 563:663-670.
33. Pernía-Andrade A.J., Jonas P. Theta-gamma-modulated synaptic currents in hippocampal granule cells invivo define a mechanism for network oscillations. Neuron 2014, 81:140-152.
34. Scheffer-Teixeira R., Belchior H., Leão R.N., Ribeiro S., Tort A.B. On high-frequency field oscillations (>100Hz) and the spectral leakage of spiking activity. J.Neurosci. 2013, 33:1535-1539.
35. Schmitz D., Schuchmann S., Fisahn A., Draguhn A., Buhl E.H., Petrasch-Parwez E., Dermietzel R., Heinemann U., Traub R.D. Axo-axonal coupling. a novel mechanism for ultrafast neuronal communication. Neuron 2001, 31:831-840.
36. Sohal V.S., Zhang F., Yizhar O., Deisseroth K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 2009, 459:698-702.
37. Stark E., Eichler R., Roux L., Fujisawa S., Rotstein H.G., Buzsáki G. Inhibition-induced theta resonance in cortical circuits. Neuron 2013, 80:1263-1276.
38. Vida I., Bartos M., Jonas P. Shunting inhibition improves robustness of gamma oscillations in hippocampal interneuron networks by homogenizing firing rates. Neuron 2006, 49:107-117.
39. Wang X.J. Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 2010, 90:1195-1268.
40. Wang Y., Markram H., Goodman P.H., Berger T.K., Ma J., Goldman-Rakic P.S. Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat. Neurosci. 2006, 9:534-542.
41. Womelsdorf T., Valiante T.A., Sahin N.T., Miller K.J., Tiesinga P. Dynamic circuit motifs underlying rhythmic gain control, gating and integration. Nat. Neurosci. 2014, 17:1031-1039.
42. Yang J.W., Hanganu-Opatz I.L., Sun J.J., Luhmann H.J. Three patterns of oscillatory activity differentially synchronize developing neocortical networks invivo. J.Neurosci. 2009, 29:9011-9025.
43. Yang J.W., An S., Sun J.J., Reyes-Puerta V., Kindler J., Berger T., Kilb W., Luhmann H.J. Thalamic network oscillations synchronize ontogenetic columns in the newborn rat barrel cortex. Cereb. Cortex 2013, 23:1299-1316.
44. Yang J.M., Zhang J., Yu Y.Q., Duan S., Li X.M. Postnatal development of 2 microcircuits involving fast-spiking interneurons in the mouse prefrontal cortex. Cereb. Cortex 2014, 24:98-109.
45. Zhang Z.W. Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. J.Neurophysiol. 2004, 91:1171-1182.