Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex

Nature Neuroscience

Volumn 10, Issue 6, 2007, Pages 743-753

  Kapfer, Christoph ^a,b   Glickfeld, Lindsey L ^a   Atallah, Bassam V ^a   Scanziani, Massimo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

SOMATOSTATIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY JUNCTION POTENTIAL; INTERNEURON; NERVE CELL NETWORK; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SOMATOSENSORY CORTEX; SYNAPTIC INHIBITION;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; MODELS, NEUROLOGICAL; NERVE NET; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; QUINOXALINES; RATS; SOMATOSENSORY CORTEX;

EID: 34249736875     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1909     Document Type: Article

References (41)

1. Ferster, D. & Jagadeesh, B. EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. J. Neurosci. 12, 1262-1274 (1992).
2. Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442-446 (2003).
3. Zhu, J.J. & Connors, B.W. Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. J. Neurophysiol. 81, 1171-1183 (1999).
4. Wilent, W.B. & Contreras, D. Synaptic responses to whisker deflections in rat barrel cortex as a function of cortical layer and stimulus intensity. J. Neurosci. 24, 3985-3998 (2004).
5. Douglas, R.J., Martin, K.A. & Whitteridge, D. An intracellular analysis of the visual responses of neurones in cat visual cortex. J. Physiol. (Lond.) 440, 659-696 (1991).
6. Anderson, J.S., Carandini, M. & Ferster, D. Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909-926 (2000).
7. Wilent, W.B. & Contreras, D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat. Neurosci. 8, 1364-1370 (2005).
8. Gabernet, L., Jadhav, S.P., Feldman, D.E., Carandini, M. & Scanziani,M. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48, 315-327 (2005).
9. Dykes, R.W., Landry, P., Metherate, R. & Hicks, T.P. Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J. Neurophysiol. 52, 1066-1093 (1984).
10. Kyriazi, H.T., Carvell, G.E., Brumberg, J.C. & Simons, D.J. Quantitative effects of GABA and bicuculline methiodide on receptive field properties of neurons in real and simulated whisker barrels. J. Neurophysiol. 75, 547-560 (1996).
11. Sillito, A.M. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J. Physiol. (Lond.) 250, 305-329 (1975).
12. Pouille, F. & Scanziani, M. Routing of spike series by dynamic circuits in the hippocampus. Nature 429, 717-723 (2004).
13. Shu, Y., Hasenstaub, A. & McCormick, D.A. Turning on and off recurrent balanced cortical activity. Nature 423, 288-293 (2003).
14. Carandini, M., Heeger, D.J. & Movshon, J.A. Linearity and normalization in simple cells of the macaque primary visual cortex. J. Neurosci. 17, 8621-8644 (1997).
15. Douglas, R.J. & Martin, K.A. A functional microcircuit for cat visual cortex. J. Physiol. (Lond.) 440, 735-769 (1991).
16. Pinto, D.J., Hartings, J.A., Brumberg, J.C. & Simons, D.J. Cortical damping: analysis of thalamocortical response transformations in rodent barrel cortex. Cereb. Cortex 13, 33-44 (2003).
17. Pinto, D.J., Brumberg, J.C. & Simons, D.J. Circuit dynamics and coding strategies in rodent somatosensory cortex. J. Neurophysiol. 83, 1158-1166 (2000).
18. Brecht, M., Roth, A. & Sakmann, B. Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J. Physiol. (Lond.) 553, 243-265 (2003).
19. Kozloski, J., Hamzei-Sichani, F. & Yuste, R. Stereotyped position of local synaptic targets in neocortex. Science 293, 868-872 (2001).
20. Thomson, A.M. & Deuchars, J. Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. Cereb. Cortex 7, 510-522 (1997).
21. Reyes, A. et al. Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1, 279-285 (1998).
22. Galarreta, M., Erdelyi, F., Szabo, G. & Hestrin, S. Electrical coupling among irregularspiking GABAergic interneurons expressing cannabinoid receptors. J. Neurosci. 24, 9770-9778 (2004).
23. Blatow, M. et al. A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 38, 805-817 (2003).
24. Gupta, A., Wang, Y. & Markram, H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287, 273-278 (2000).
25. McCormick, D.A., Connors, B.W., Lighthall, J.W. & Prince, D.A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54, 782-806 (1985).
26. Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476-486 (1997).
27. Beierlein, M., Gibson, J.R. & Connors, B.W. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90, 2987-3000 (2003).
28. Gibson, J.R., Beierlein, M. & Connors, B.W. Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79 (1999).
29. Galarreta, M. & Hestrin, S. Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat. Neurosci. 1, 587-594 (1998).
30. Wang, Y. et al. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J. Physiol. (Lond.) 561, 65-90 (2004).
31. Svoboda, K., Denk, W., Kleinfeld, D. & Tank, D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161-165 (1997).
32. Svoboda, K., Helmchen, F., Denk, W. & Tank, D.W. Spread of dendritic excitation in layer 2/3 pyramidal neurons in rat barrel cortex in vivo. Nat. Neurosci. 2, 65-73 (1999).
33. Haider, B., Duque, A., Hasenstaub, A.R. & McCormick, D.A. Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J. Neurosci. 26, 4535-4545 (2006).
34. Chu, Z., Galarreta, M. & Hestrin, S. Synaptic interactions of late-spiking neocortical neurons in layer 1. J. Neurosci. 23, 96-102 (2003).
35. Yoshimura, Y. & Callaway, E.M. Fine-scale specificity of cortical networks depends on inhibitory cell type and connectivity. Nat. Neurosci. 8, 1552-1559 (2005).
36. Rozov, A., Jerecic, J., Sakmann, B. & Burnashev, N. AMPA receptor channels with long-lasting desensitization in bipolar interneurons contribute to synaptic depression in a novel feedback circuit in layer 2/3 of rat neocortex. J. Neurosci. 21, 8062-8071 (2001).
37. Thomson, A.M., West, D.C., Wang, Y. & Bannister, A.P. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb. Cortex 12, 936-953 (2002).
38. Ma, Y., Hu, H., Berrebi, A.S., Mathers, P.H. & Agmon, A. Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26, 5069-5082 (2006).
39. Fairén, A., DeFelipe, J. & Regidor, J. Nonpyramidal neurons: general account. in Cellular Components of the Cerebral Cortex (eds. Peters, A. & Jones, E.G.) 201-254 (Plenum, New York, 1984).
40. Azouz, R. & Gray, C.M. Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. Proc. Natl. Acad. Sci. USA 97, 8110-8115 (2000).
41. Biro, A.A., Holderith, N.B. & Nusser, Z. Quantal size is independent of the release probability at hippocampal excitatory synapses. J. Neurosci. 25, 223-232 (2005).