Polysynaptic subcircuits in the neocortex: spatial and temporal diversity

Current Opinion in Neurobiology

Volumn 18, Issue 3, 2008, Pages 332-337

  Silberberg, Gilad ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

BRAIN FUNCTION; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; NEOCORTEX; NERVE CELL EXCITABILITY; NERVE CELL NETWORK; NERVE CELL PLASTICITY; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW; SPATIAL SUMMATION; SYNAPTIC POTENTIAL; TEMPORAL SUMMATION;

ANIMALS; NEOCORTEX; NERVE NET; SYNAPSES;

EID: 53949093694     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2008.08.009     Document Type: Review

References (52)

1. Douglas R., and Martin K.A.C. Neocortex. In: Shepherd G.M. (Ed). The synaptic organization of the brain (1998), Oxford University Press 459-511
2. DeFelipe J., Alonso-Nanclares L., and Arellano J.I. Microstructure of the neocortex: comparative aspects. J Neurocytol 31 (2002) 299-316
3. Monier C., Chavane F., Baudot P., Graham L.J., and Fregnac Y. Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37 (2003) 663-680
4. Zhu Y., Stornetta R.L., and Zhu J.J. Chandelier cells control excessive cortical excitation: characteristics of whisker-evoked synaptic responses of layer 2/3 nonpyramidal and pyramidal neurons. J Neurosci 24 (2004) 5101-5108
5. Wehr M., and Zador A.M. Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47 (2005) 437-445
6. Markram H., Toledo-Rodriguez M., Wang Y., Gupta A., Silberberg G., and Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5 (2004) 793-807
7. Gupta A., Wang Y., and Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287 (2000) 273-278
8. Fairen A., DeFelipe J., and Regidor J. Nonpyramidal Neurons; general account. In: Peters A., and Jones E.G. (Eds). Cellular Components of the Cerebral Cortex (1984), Plenum Press Cerebral Cortex, vol. 1
9. Somogyi P., Tamas G., Lujan R., and Buhl E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res Rev 26 (1998) 113-135
10. Kawaguchi Y., and Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7 (1997) 476-486
11. Toledo-Rodriguez M., Goodman P., Illic M., Wu C., and Markram H. Neuropeptide and calcium-binding protein gene expression profiles predict neuronal anatomical type in the juvenile rat. J Physiol 567 (2005) 401-413
12. Somogyi P. A specific 'axo-axonal' interneuron in the visual cortex of the rat. Brain Res 136 (1977) 345-350
13. Thomson A.M., West D.C., Wang Y., and 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 (2002) 936-953
14. Wang Y., Toledo-Rodriguez M., Gupta A., Wu C., Silberberg G., Luo J., and Markram H. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol 561 (2004) 65-90
15. Koch C., Poggio T., and Torre V. Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. Proc Natl Acad Sci U S A 80 (1983) 2799-2802
16. Liu G. Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites. Nat Neurosci 7 (2004) 373-379
17. Thomson A.M., Deuchars J., and West D.C. Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation. Neuroscience 54 (1993) 347-360
18. •]).
19. Silberberg G., Wu C., and Markram H. Synaptic dynamics control the timing of neuronal excitation in the activated neocortical microcircuit. J Physiol 556 (2004) 19-27
20. Markram H., Wang Y., and Tsodyks M. Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 95 (1998) 5323-5328. In this paper the authors show that synaptic transmission from the same presynaptic pyramidal cell displays different dynamics depending on the identity of the postsynaptic cell and is unique for each synaptically connected pair. The different dynamics are captured by a model that quantifies the time-constants of recovery from depression and facilitation as well as the utilization factor (equivalent to the release probability) of the synapses.
21. Beierlein M., Gibson J.R., and Connors B.W. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90 (2003) 2987-3000
22. Galarreta M., and Hestrin S. Spike transmission and synchrony detection in networks of GABAergic interneurons. Science 292 (2001) 2295-2299
23. Silberberg G., and Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53 (2007) 735-746. This study describes a disynaptic inhibitory subcircuit between pyramidal cells mediated by a well-defined interneuron type, the Martinotti cell. The inhibitory interaction is frequency-dependent and activated by bursts of action-potentials in the presynaptic pyramidal cell. The paper describes the frequency dependence, the location of inhibitory synapses, characterization of the intermediate cell, and analysis of synaptic connectivity properties in the subcircuit.
24. Klausberger T., Magill P.J., Marton L.F., Roberts J.D., Cobden P.M., Buzsaki G., and Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421 (2003) 844-848
25. Kozloski J., Hamzei-Sichani F., and Yuste R. Stereotyped position of local synaptic targets in neocortex. Science 293 (2001) 868-872
26. Szabadics J., Varga C., Molnar G., Olah S., Barzo P., and Tamas G. Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 311 (2006) 233-235. In this paper, the authors present intriguing findings in rat and human neocortex regarding the effect of axo-axonic cells on pyramidal cells. The paper shows that due to a depolarized chloride reversal potential at the axon initial segment the effect of synaptic input from axo-axonic cells onto pyramidal cells is excitatory. This excitatory effect is sufficient to induce polysynaptic activity sequences triggered by a single axo-axonic cell.
27. Kapfer C., Glickfeld L.L., Atallah B.V., and Scanziani M. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 10 (2007) 743-753. In this paper the authors describe a disynaptic inhibitory pathway between layer 2/3 pyramidal cells in the somatosensory cortex. The inhibition is mediated by somatostatin expressing interneurons both in layer 2/3 and in infragranular layers. A model incorporating the connectivity properties between pyramidal cells and interneurons is presented, predicting the recruitment of inhibition as a function of the number of presynaptic pyramidal cells.
28. Ren M., Yoshimura Y., Takada N., Horibe S., and Komatsu Y. Specialized inhibitory synaptic actions between nearby neocortical pyramidal neurons. Science 316 (2007) 758-761. This study describes a novel disynaptic mechanism for inhibition between pyramidal cells, in which inhibition is mediated by axo-axonic interactions independent of interneuron discharge. The authors first report inhibitory interactions between neighboring pyramidal cells, and then show that these events are mediated by local excitation of GABAergic terminals targeting the somatic regions (for review, see reference [30]).
29. Brecht M., Schneider M., Sakmann B., and Margrie T.W. Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427 (2004) 704-710
30. Connors B.W., and Cruikshank S.J. Bypassing interneurons: inhibition in neocortex. Nat Neurosci 10 (2007) 808-810
31. Khirug S., Yamada J., Afzalov R., Voipio J., Khiroug L., and Kaila K. GABAergic depolarization of the axon initial segment in cortical principal neurons is caused by the Na-K-2Cl cotransporter NKCC1. J Neurosci 28 (2008) 4635-4639
32. Molnar G., Olah S., Komlosi G., Fule M., Szabadics J., Varga C., Barzo P., and Tamas G. Complex events initiated by individual spikes in the human cerebral cortex. PLoS Biol 6 (2008) e222. This paper describes novel findings from human neocortex, in which single spikes in pyramidal cells initiate polysynaptic cascades of mixed excitatory and inhibitory events. Interestingly, GABAergic neurons of different classes induce inhibitory as well as excitatory responses in pyramidal cells. The GABAergic axo-axonic cell (AAC, or chandelier cell) produces a strong excitatory response in its postsynaptic targets, sufficient to induce pyramidal cell discharge.
33. Holmgren C.D., Harkany T., Svennenfors B., and Zilberter Y. Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 551 (2003) 139-153
34. Freund T.F., and Buzsaki G. Interneurons of the hippocampus. Hippocampus 6 (1996) 347-470
35. Pouille F., and Scanziani M. Routing of spike series by dynamic circuits in the hippocampus. Nature 429 (2004) 717-723. In this paper the authors show two inhibitory pathways that target CA1 hippocampal pyramidal neurons. By using simultaneous somatic and dendritic recordings the authors describe a fast 'onset' pathway that targets the perisomatic regions and a delayed, frequency-dependent pathway that targets distal dendrites. By using morphological reconstructions the authors show that the delayed inhibitory input to the dendrites is mediated by OLM cells.
36. Thomson A.M., and Deuchars J. Synaptic interactions neocortical local circuits: dual intracellular recordings in vitro. Cereb Cortex 7 (1997) 510-522
37. Miles R. Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea-pig in vitro. J Physiol 428 (1990) 61-77
38. Tan Z., Hu H., Huang Z.J., and Agmon A. Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc Natl Acad Sci U S A 105 (2008) 2187-2192. In this study, the authors show that excitatory input from the thalamus to the neocortex has different dynamics depending on the type of postsynaptic cortical interneuron. Parvalbumin expressing interneurons received strongly depressing excitation while somatostatin expressing interneurons received facilitating input, similar to the dynamics of excitatory input from neighboring pyramidal cells.
39. Markram H., Lübke J., Frotscher M., Roth A., and Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500 (1997) 409-440
40. Feldmeyer D., Lübke J., and Sakmann B. Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats. J Physiol 575 (2006) 583-602
41. Kim H.G., and Connors B.W. Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology. J Neurosci 13 (1993) 5301-5311
42. Larkum M.E., Waters J., Sakmann B., and Helmchen F. Dendritic spikes in apical dendrites of neocortical layer 2/3 pyramidal neurons. J Neurosci 27 (2007) 8999-9008
43. Miles R., Toth K., Gulyas A.I., Hajos N., and Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16 (1996) 815-823
44. Pouille F., and Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293 (2001) 1159-1163
45. Kim H.G., Beierlein M., and Connors B.W. Inhibitory control of excitable dendrites in neocortex. J Neurophysiol 74 (1995) 1810-1814
46. Larkum M.E., Zhu J.J., and Sakmann B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398 (1999) 338-341. This study demonstrated that inhibitory input from a single interneuron is sufficient to regulate the generation of a dendritic calcium spike. GABAergic synaptic input to the distal dendrites of a layer 5 pyramidal cell could eliminate the generation of a calcium spike depending on the relative timing of the events.
47. Okun M., and Lampl I. Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat Neurosci 11 (2008) 535-537
48. Cauller L. Layer I of primary sensory neocortex: where top-down converges upon bottom-up. Behav. Brain Res 71 (1995) 163-170
49. Bureau I., von Saint Paul F., and Svoboda K. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol 4 (2006) e382
50. Letzkus J.J., Kampa B.M., and Stuart G.J. Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. J Neurosci 26 (2006) 10420-10429
51. Sjostrom P.J., and Hausser M. A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron 51 (2006) 227-238
52. Rinaldi T., Silberberg G., and Markram H. Hyperconnectivity of local neocortical microcircuitry induced by prenatal exposure to valproic acid. Cereb Cortex 18 (2008) 763-770