Frequency-dependent disynaptic inhibition in the pyramidal network: A ubiquitous pathway in the developing rat neocortex

Journal of Physiology

Volumn 587, Issue 22, 2009, Pages 5411-5425

  Berger, Thomas K ^a   Perin, Rodrigo ^a   Silberberg, Gilad ^b   Markram, Henry ^a  

^a EPFL   (Switzerland)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; CLINICAL EFFECTIVENESS; CONTROLLED STUDY; FREQUENCY DEPENDENT DISYNAPTIC INHIBITION; MOTOR CORTEX; NEOCORTEX; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SOMATOSENSORY CORTEX; SYNAPSE; SYNAPTIC INHIBITION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; VISUAL CORTEX; BRAIN ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; JUVENILE ANIMAL; MEDIAL PREFRONTAL CORTEX; NERVOUS SYSTEM PARAMETERS; PRIMARY SOMATOSENSORY CORTEX; SECONDARY VISUAL CORTEX; SYNAPTIC FATIGUE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; NEOCORTEX; NERVE NET; NEURAL INHIBITION; NEURAL PATHWAYS; PRESYNAPTIC TERMINALS; PYRAMIDAL CELLS; RATS; RATS, WISTAR;

EID: 70649094100     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.176552     Document Type: Article

References (35)

1. Abrahamsson T, Gustafsson B, Hanse E. Synaptic fatigue at the naive perforant path-dentate granule cell synapse in the rat. J Physiol 2005, 569:737-750.
2. Arsiero M, Lüscher H-R, Lundstrom BN, Giugliano M. The impact of input fluctuations on the frequency-current relationships of layer 5 pyramidal neurons in the rat medial prefrontal cortex. J Neurosci 2007, 27:3274-3284.
3. Bacci A, Huguenard J, Prince D. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 2004, 431:312-316.
4. Berger T, Larkum ME, Lüscher HR. High Ih channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J Neurophysiol 2001, 85:855-868.
5. Braitenberg V, Schüz A. Cortex: Statistics and Geometry of Neuronal Connectivity 1998, 2nd edn, Springer, Berlin, Heidelberg, New York
6. Brodmann K. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues 1909, Barth, Leipzig
7. Brown SP, Hestrin S. Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 2009, 457:1133-1136.
8. DeFelipe J, Alonso-Nanclares L, Arellano JI. Microstructure of the neocortex: comparative aspects. J Neurocytol 2002, 31:299-316.
9. de Kock CPJ, Sakmann B. High frequency action potential bursts (≥ 100 Hz) in L2/3 and L5b thick tufted neurons in anaesthetized and awake rat primary somatosensory cortex. J Physiol 2008, 586:3353-3364.
10. Dong HW. The Allen Atlas: A Digital Color Brain Atlas of the C57BL/6J Male Mouse 2007, Wiley & Sons
11. Drummond GB. Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 2009, 587:713-719.
12. Holmgren C, Harkany T, Svennenfors B, Zilberter Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 2003, 551:139-153.
13. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 2007, 10:743-753.
14. Le Bé J, Silberberg G, Wang Y, Markram H. Morphological, electrophysiological, and synaptic properties of corticocallosal pyramidal cells in the neonatal rat neocortex. Cereb Cortex 2007, 17:2204-2213.
15. Lefort S, Tomm C, Floyd Sarria J-C, Petersen CCH. The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron 2009, 61:301-316.
16. Marinelli S, Pacioni S, Bisogno T, Marzo VD, Prince DA, Huguenard JR, Bacci A. The endocannabinoid 2-arachidonoylglycerol is responsible for the slow self-inhibition in neocortical interneurons. J Neurosci 2008, 28:13532-13541.
17. Markram H, Lübke J, Frotscher M, Roth A, Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 1997, 500:409-440.
18. Markram H, Wang Y, Tsodyks M. Differential signalling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 1998, 95:5323-5328.
19. Mercer A, West DC, Morris OT, Kirchhecker S, Kerkhoff JE, Thomson AM. Excitatory connections made by presynaptic cortico-cortical pyramidal cells in layer 6 of the neocortex. Cereb Cortex 2005, 15:1485-1496.
20. Molnár G, Oláh S, Komlósi G, Füle M, Szabadics J, Varga C, Barzó P, Tamás G. Complex events initiated by individual spikes in the human cerebral cortex. PLoS Biol 2008, 6:e222.
21. Morishima M, Kawaguchi Y. Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. J Neurosci 2006, 26:4394-4405.
22. Murayama M, Pérez-Garci E, Nevian T, Bock T, Senn W, Larkum ME. Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 2009, 457:1137-1141.
23. Paxinos G, Watson C. Theoretical Rat Brain in Stereotaxic Coordinates 1998, 4th edn, Academic Press
24. Ren M, Yoshimura Y, Takada N, Horibe S, Komatsu Y. Specialized inhibitory synaptic actions between nearby neocortical pyramidal neurons. Science 2007, 316:758-761.
25. Reyes A, Sakmann B. Developmental switch in the short-term modification of unitary EPSPs evoked in layer 2/3 and layer 5 pyramidal neurons of rat neocortex. J Neurosci 1999, 19:3827-3835.
26. Sherwood N, Timiras P. A Stereotaxic Atlas of the Developing Rat Brain 1970, University of California Press, Berkeley, CA, USA
27. Silberberg G, Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 2007, 53:735-746.
28. Sjöström PJ, Turrigiano GG, Nelson SB. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 2001, 32:1149-1164.
29. Song S, Sjöström PJ, Reigl M, Nelson S, Chklovskii DB. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol 2005, 3:e68.
30. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 2008, 9:206-221.
31. Stuart G, Spruston N. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 1998, 18:3501-3510.
32. Uziel A, Romand R, Marot M. Development of cochlear potentials in rats. Audiology 1981, 20:89-100.
33. Wang Y, Markram H, Goodman PH, Berger TK, Ma J, Goldman-Rakic PS. Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat Neurosci 2006, 9:534-542.
34. Williams SR. Encoding and decoding of dendritic excitation during active states in pyramidal neurons. J Neurosci 2005, 25:5894-5902.
35. Zar JH. Biostatistical Analysis 1999, 4th edn, Prentice Hall