Differential wiring of layer 2/3 neurons drives sparse and reliable firing during neocortical development

Cerebral Cortex

Volumn 23, Issue 11, 2013, Pages 2690-2699

  Benedetti, Brett L ^a,b   Takashima, Yoshio ^a   Wen, Jing A ^a   Urban Ciecko, Joanna ^a   Barth, Alison L ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

activity dependent gene expression; AMPA receptors; critical period; somatosensory; subnetworks

Indexed keywords

6 NITRO 7 SULFAMOYLBENZO[F]QUINOXALINE 2,3 DIONE; GREEN FLUORESCENT PROTEIN;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN SLICE; CELL POPULATION; COMPARATIVE STUDY; IN VIVO STUDY; MOUSE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; ONCOGENE C FOS; POSTSYNAPTIC POTENTIAL SUMMATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENSORY DEPRIVATION; SENSORY STIMULATION; SPIKE; SYNAPTIC INHIBITION; TRANSGENIC MOUSE; VOLTAGE CLAMP; WHOLE CELL;

ACTIVITY-DEPENDENT GENE EXPRESSION; AMPA RECEPTORS; CRITICAL PERIOD; SOMATOSENSORY; SUBNETWORKS;

ANIMALS; ELECTRIC STIMULATION; MICE; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS; SOMATOSENSORY CORTEX; SYNAPTIC POTENTIALS;

EID: 84885929177     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs257     Document Type: Article

References (60)

1. Arieli A, Sterkin A, Grinvald A, Aertsen A. 1996. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science (New York, NY). 273:1868-1871. (Pubitemid 26322498)
2. Aronoff R, Matyas F, Mateo C, Ciron C, Schneider B, Petersen CC. 2010. Long-range connectivity of mouse primary somatosensory barrel cortex. Eur J Neurosci. 31:2221-2233.
3. Barth AL, Gerkin RC, Dean KL. 2004. Alteration of neuronal firing properties after in vivo experience in a FosGFP transgenic mouse. J Neurosci. 24:6466-6475. (Pubitemid 38971693)
4. Barth AL, Poulet JF. 2012. Experimental evidence for sparse firing in the neocortex. Trends Neurosci. 35:345-355.
5. Bender KJ, Allen CB, Bender VA, Feldman DE. 2006. Synaptic basis for whisker deprivation-induced synaptic depression in rat somatosensory cortex. J Neurosci. 26:4155-4165. (Pubitemid 44315375)
6. Bender KJ, Rangel J, Feldman DE. 2003. Development of columnar topography in the excitatory layer 4 to layer 2/3 projection in rat barrel cortex. J Neurosci. 23:8759-8770. (Pubitemid 37176657)
7. Benedetti BL, Glazewski S, Barth AL. 2009. Reliable and precise neuronal firing during sensory plasticity in superficial layers of primary somatosensory cortex. J Neurosci. 29:11817-11827.
8. Bi GQ, Poo MM. 1998. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci. 18:10464-10472.
9. Brecht M, Roth A, Sakmann B. 2003. Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of rat somatosensory barrel cortex. J Physiol. 553:243-265. (Pubitemid 37483932)
10. Brown SP, Hestrin S. 2009. Cell-type identity: a key to unlocking the function of neocortical circuits. Curr Opin Neurobiol. 19:415-421.
11. Bureau I, Shepherd GM, Svoboda K. 2004. Precise development of functional and anatomical columns in the neocortex. Neuron. 42:789-801. (Pubitemid 38748792)
12. Clem RL, Barth A. 2006. Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron. 49:663-670. (Pubitemid 43290126)
13. Clem RL, Celikel T, Barth AL. 2008. Ongoing in vivo experience triggers synaptic metaplasticity in the neocortex. Science (New York, NY). 319:101-104.
14. Constantinople CM, Bruno RM. 2011. Effects and mechanisms of wakefulness on local cortical networks. Neuron. 69:1061-1068.
15. Crochet S, Poulet JFA, Kremer Y, Petersen CH. 2011. Synaptic mechanisms underlying sparse coding of active touch. Neuron. 69:1-16.
16. de Kock CP, Bruno RM, Spors H, Sakmann B. 2007. Layer-and cell-type-specific suprathreshold stimulus representation in rat primary somatosensory cortex. J Physiol. 581:139-154. (Pubitemid 46712033)
17. Feldmeyer D, Lubke J, Sakmann B. 2006. Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats. J Physiol. 575:583-602. (Pubitemid 44270183)
18. Feldmeyer D, Lubke J, Silver RA, Sakmann B. 2002. Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J Physiol. 538:803-822. (Pubitemid 35190073)
19. Fields RD, Eshete F, Stevens B, Itoh K. 1997. Action potentialdependent regulation of gene expression: temporal specificity in ca2+, cAMP-responsive element binding proteins, and mitogenactivated protein kinase signaling. J Neurosci. 17:7252-7266. (Pubitemid 27413257)
20. Goda Y, Stevens CF. 1994. Two components of transmitter release at a central synapse. Proc Natl Acad Sci USA. 91:12942-12946.
21. Guzowski JF, Miyashita T, Chawla MK, Sanderson J, Maes LI, Houston FP, Lipa P, McNaughton BL, Worley PF, Barnes CA. 2006. Recent behavioral history modifies coupling between cell activity and Arc gene transcription in hippocampal CA1 neurons. Proc Natl Acad Sci USA. 103:1077-1082. (Pubitemid 43212224)
22. Hestrin S, Galarreta M. 2005. Electrical synapses define networks of neocortical GABAergic neurons. Trends Neurosci. 28:304-309. (Pubitemid 40775775)
23. Hromadka T, Deweese MR, Zador AM. 2008. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 6:e16.
24. Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A. 2003. Spontaneously emerging cortical representations of visual attributes. Nature. 425:954-956. (Pubitemid 37376925)
25. Kerr JN, de Kock CP, Greenberg DS, Bruno RM, Sakmann B, Helmchen F. 2007. Spatial organization of neuronal population responses in layer 2/3 of rat barrel cortex. J Neurosci. 27:13316-13328. (Pubitemid 350220486)
26. Kumar A, Rotter S, Aertsen A. 2010. Spiking activity propagation in neuronal networks: reconciling different perspectives on neural coding. Nat Rev Neurosci. 11:615-627.
27. Lefort S, Tomm C, Floyd Sarria JC, Petersen CC. 2009. The excitatory neuronal network of the C2 barrel column in mouse primary somatosensory cortex. Neuron. 61:301-316.
28. Luckman SM, Dyball RE, Leng G. 1994. Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity. J Neurosci. 14:4825-4830. (Pubitemid 24237904)
29. MacLean JN, Watson BO, Aaron GB, Yuste R. 2005. Internal dynamics determine the cortical response to thalamic stimulation. Neuron. 48:811-823. (Pubitemid 41759431)
30. Maravall M, Stern EA, Svoboda K. 2004. Development of intrinsic properties and excitability of layer 2/3 pyramidal neurons during a critical period for sensory maps in rat barrel cortex. J Neurophysiol. 92:144-156. (Pubitemid 38802240)
31. Marder E, Goaillard JM. 2006. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci. 7:563-574. (Pubitemid 43995432)
32. Markram H, Lubke J, Frotscher M, Sakmann B. 1997. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science (New York, NY). 275:213-215. (Pubitemid 27034762)
33. Marre O, Yger P, Davison AP, Fregnac Y. 2009. Reliable recall of spontaneous activity patterns in cortical networks. J Neurosci. 29:14596-14606.
34. Metherate R, Cox CL, Ashe JH. 1992. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J Neurosci. 12:4701-4711.
35. Meyer HS, Wimmer VC, Hemberger M, Bruno RM, de Kock CP, Frick A, Sakmann B, Helmstaedter M. 2010. Cell type-specific thalamic innervation in a column of rat vibrissal cortex. Cereb Cortex. 20:2287-2303.
36. Oberlaender M, Boudewijns ZS, Kleele T, Mansvelder HD, Sakmann B, de Kock CP. 2011. Three-dimensional axon morphologies of individual layer 5 neurons indicate cell type-specific intracortical pathways for whisker motion and touch. Proc Natl Acad Sci USA. 108:4188-4193.
37. Ohki K, Chung S, Ch'ng YH, Kara P, Reid RC. 2005. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex. Nature. 433:597-603. (Pubitemid 40282986)
38. Otsuka T, Kawaguchi Y. 2011. Cell diversity and connection specificity between callosal projection neurons in the frontal cortex. J Neurosci. 31:3862-3870.
39. Padmanabhan K, Urban NN. 2010. Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat Neurosci. 13:1276-1282.
40. Perin R, Berger TK, Markram H. 2011. A synaptic organizing principle for cortical neuronal groups. Proc Natl Acad Sci USA. 108:5419-5424.
41. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B. 2003. Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci USA. 100:13638-13643. (Pubitemid 37444792)
42. Poo C, Isaacson JS. 2009. Odor representations in olfactory cortex: "sparse" coding, global inhibition, and oscillations. Neuron. 62:850-861.
43. Reyes AD. 2003. Synchrony-dependent propagation of firing rate in iteratively constructed networks in vitro. Nat Neurosci. 6:593-599. (Pubitemid 36648800)
44. Salinas E, Sejnowski TJ. 2001. Correlated neuronal activity and the flow of neural information. Nat Rev Neurosci. 2:539-550. (Pubitemid 33679827)
45. Schilling K, Luk D, Morgan JI, Curran T. 1991. Regulation of a fos-lacZ fusion gene: a paradigm for quantitative analysis of stimulus-transcription coupling. Proc Natl Acad Sci USA. 88:5665-5669. (Pubitemid 21914806)
46. Schoenenberger P, Gerosa D, Oertner TG. 2009. Temporal control of immediate early gene induction by light. PloS One. 4:e8185.
47. Sheng M, McFadden G, Greenberg ME. 1990. Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron. 4:571-582. (Pubitemid 20160846)
48. Song S, Sjostrom PJ, Reigl M, Nelson S, Chklovskii DB. 2005. Highly nonrandom features of synaptic connectivity in local cortical circuits. PLoS Biol. 3:e68.
49. Steriade M, Amzica F, Nunez A. 1993. Cholinergic and noradrenergic modulation of the slow (approximately 0.3 Hz) oscillation in neocortical cells. J Neurophysiol. 70:1385-1400. (Pubitemid 23326376)
50. Stern EA, Maravall M, Svoboda K. 2001. Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron. 31:305-315. (Pubitemid 32762982)
51. Stettler DD, Axel R. 2009. Representations of odor in the piriform cortex. Neuron. 63:854-864.
52. Thomas MJ, Beurrier C, Bonci A, Malenka RC. 2001. Long-term depression in the nucleus accumbens: a neural correlate of behavioral sensitization to cocaine. Nat Neurosci. 4:1217-1223. (Pubitemid 33135627)
53. Vijayan S, Hale GJ, Moore CI, Brown EN, Wilson M. 2010. Activity in the barrel cortex during active behavior and sleep. J Neurophysiol. 103:2074-2084.
54. Waites CL, Craig AM, Garner CC. 2005. Mechanisms of vertebrate synaptogenesis. Annu Rev Neurosci. 28:251-274. (Pubitemid 41098906)
55. Wen JA, Barth AL. 2011. Input-specific critical periods for experiencedependent plasticity in layer 2/3 pyramidal neurons. J Neurosci. 31:4456-4465.
56. Wolfe J, Houweling AR, Brecht M. 2010. Sparse and powerful cortical spikes. Curr Opin Neurobiol. 20:306-312.
57. Xu-Friedman MA, Regehr WG. 1999. Presynaptic strontium dynamics and synaptic transmission. Biophys J. 76:2029-2042. (Pubitemid 29266358)
58. Yang Y, DeWeese MR, Otazu GH, Zador AM. 2008. Millisecond-scale differences in neural activity in auditory cortex can drive decisions. Nat Neurosci. 11:1262-1263.
59. Yassin L, Benedetti BL, Jouhanneau JS, Wen JA, Poulet JFA, Barth AL. 2010. An embedded subnetwork of highly active neurons in the neocortex. Neuron. 68:1043-1050.
60. Yoshimura Y, Dantzker JL, Callaway EM. 2005. Excitatory cortical neurons form fine-scale functional networks. Nature. 433:868-873. (Pubitemid 40314895)