Characterization of neuronal intrinsic properties and synaptic transmission in layer I of anterior cingulate cortex from adult mice

Molecular Pain

Volumn 8, Issue , 2012, Pages

  Li, Xiang Yao ^a,b   Chen, Tao ^b   Descalzi, Giannina ^b   Koga, Kohei ^b   Qiu, Shuang ^b   Zhuo, Min ^a,b  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Adult mice; Anterior cingulate cortex; Kainate receptor; Layer I; Spontaneous firing neurons

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ADENOSINE DIPHOSPHATE; ADENOSINE DIPHOSPHATE1; ADENOSINE DIPHOSPHATE2; AMPA RECEPTOR; KAINIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CELL FUNCTION; COGNITION; MALE; MOUSE; NEOCORTEX; NEOCORTEX LAYER I; NERVE CELL; NERVE CELL STIMULATION; NERVE CONDUCTION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENSORY NERVE; SYNAPTIC TRANSMISSION; WHOLE CELL;

ACTION POTENTIALS; AGING; ANIMALS; CLUSTER ANALYSIS; EXCITATORY POSTSYNAPTIC POTENTIALS; GYRUS CINGULI; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, AMPA; RECEPTORS, GABA-A; RECEPTORS, KAINIC ACID; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPTIC TRANSMISSION;

EID: 84869014343     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-8-53     Document Type: Article

References (62)

1. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, et al. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 2008, 9:557-568. 2868386, 18568015.
2. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 2004, 5:793-807. 10.1038/nrn1519, 15378039.
3. Zhuo M. Cortical plasticity as a new endpoint measurement for chronic pain. Mol Pain 2011, 7:54. 10.1186/1744-8069-7-54, 3157449, 21798042.
4. Zhuo M. Cortical excitation and chronic pain. Trends Neurosci 2008, 31:199-207. 10.1016/j.tins.2008.01.003, 18329111.
5. Zhuo M. Molecular mechanisms of pain in the anterior cingulate cortex. J Neurosci Res 2006, 84:927-933. 10.1002/jnr.21003, 16862566.
6. Toyoda H, Li XY, Wu LJ, Zhao MG, Descalzi G, Chen T, Koga K, Zhuo M. Interplay of amygdala and cingulate plasticity in emotional fear. Neural Plast 2011, 2011:813749. 3168900, 21912749.
7. Vann SD, Albasser MM. Hippocampus and neocortex: recognition and spatial memory. Curr Opin Neurobiol 2011, 21:440-445. 10.1016/j.conb.2011.02.002, 21353527.
8. Klausberger T, Somogyi P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 2008, 321:53-57. 10.1126/science.1149381, 18599766.
9. Soriano E, Del Rio JA. The cells of cajal-retzius: still a mystery one century after. Neuron 2005, 46:389-394. 10.1016/j.neuron.2005.04.019, 15882637.
10. Wu LJ, Li X, Chen T, Ren M, Zhuo M. Characterization of intracortical synaptic connections in the mouse anterior cingulate cortex using dual patch clamp recording. Mol Brain 2009, 2:32. 10.1186/1756-6606-2-32, 2770551, 19828050.
11. Wozny C, Williams SR. Specificity of synaptic connectivity between layer 1 inhibitory interneurons and layer 2/3 pyramidal neurons in the rat neocortex. Cereb Cortex 2011, 21(8):1818-1826. 10.1093/cercor/bhq257, 3138515, 21220765.
12. Carey RG, Fitzpatrick D, Diamond IT. Thalamic projections to layer I of striate cortex shown by retrograde transport of horseradish peroxidase. Science 1979, 203:556-559. 10.1126/science.760205, 760205.
13. Parnavelas JG, Chatzissavidou A, Burne RA. Subcortical projections to layer I of the visual cortex, area 17, of the rat. Exp Brain Res 1981, 41:184-187.
14. Cauller L. Layer I of primary sensory neocortex: where top-down converges upon bottom-up. Behav Brain Res 1995, 71:163-170. 10.1016/0166-4328(95)00032-1, 8747184.
15. Mitchell BD, Cauller LJ. Corticocortical and thalamocortical projections to layer I of the frontal neocortex in rats. Brain Res 2001, 921:68-77. 10.1016/S0006-8993(01)03084-0, 11720712.
16. Shlosberg D, Amitai Y, Azouz R. Time-dependent, layer-specific modulation of sensory responses mediated by neocortical layer 1. J Neurophysiol 2006, 96:3170-3182. 10.1152/jn.00520.2006, 17110738.
17. Galazo MJ, Martinez-Cerdeno V, Porrero C, Clasca F. Embryonic and postnatal development of the layer I-directed (" matrix" ) thalamocortical system in the rat. Cereb Cortex 2008, 18:344-363.
18. Kuhn B, Denk W, Bruno RM. In vivo two-photon voltage-sensitive dye imaging reveals top-down control of cortical layers 1 and 2 during wakefulness. Proc Natl Acad Sci U S A 2008, 105:7588-7593. 10.1073/pnas.0802462105, 2396672, 18508976.
19. Letzkus JJ, Wolff SB, Meyer EM, Tovote P, Courtin J, Herry C, Luthi A. A disinhibitory microcircuit for associative fear learning in the auditory cortex. Nature 2011, 480:331-335. 10.1038/nature10674, 22158104.
20. Karagiannis A, Gallopin T, David C, Battaglia D, Geoffroy H, Rossier J, Hillman EM, Staiger JF, Cauli B. Classification of NPY-expressing neocortical interneurons. J Neurosci 2009, 29:3642-3659. 10.1523/JNEUROSCI.0058-09.2009, 2750888, 19295167.
21. Yamazaki H, Sekiguchi M, Takamatsu M, Tanabe Y, Nakanishi S. Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis. Proc Natl Acad Sci U S A 2004, 101:14509-14514. 10.1073/pnas.0406295101, 521974, 15452350.
22. Soda T, Nakashima R, Watanabe D, Nakajima K, Pastan I, Nakanishi S. Segregation and coactivation of developing neocortical layer 1 neurons. J Neurosci 2003, 23:6272-6279.
23. Hestrin S, Armstrong WE. Morphology and physiology of cortical neurons in layer I. J Neurosci 1996, 16:5290-5300.
24. Zhou FM, Hablitz JJ. Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties. J Neurophysiol 1996, 76:651-667.
25. Chu Z, Galarreta M, Hestrin S. Synaptic interactions of late-spiking neocortical neurons in layer 1. J Neurosci 2003, 23:96-102.
26. Radnikow G, Feldmeyer D, Lubke J. Axonal projection, input and output synapses, and synaptic physiology of Cajal-Retzius cells in the developing rat neocortex. J Neurosci 2002, 22:6908-6919.
27. Anderson JC, Martin KA, Picanco-Diniz CW. The neurons in layer 1 of cat visual cortex. Proc Biol Sci 1992, 248:27-33. 10.1098/rspb.1992.0038, 1355908.
28. Kim SS, Wang H, Li XY, Chen T, Mercaldo V, Descalzi G, Wu LJ, Zhuo M. Neurabin in the anterior cingulate cortex regulates anxiety-like behavior in adult mice. Mol Brain 2011, 4:6. 10.1186/1756-6606-4-6, 3037880, 21247477.
29. Descalzi G, Li XY, Chen T, Mercaldo V, Koga K, Zhuo M. Rapid synaptic potentiation within the anterior cingulate cortex mediates trace fear learning. Mol Brain 2012, 5:6. 10.1186/1756-6606-5-6, 3395850, 22304729.
30. Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, et al. Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 2005, 47:859-872. 10.1016/j.neuron.2005.08.014, 16157280.
31. Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M. Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain 2005, 1:6. 10.1186/1744-8069-1-6, 1074356, 15813993.
32. Steenland HW, Li XY, Zhuo M. Predicting aversive events and terminating fear in the mouse anterior cingulate cortex during trace fear conditioning. J Neurosci 2012, 32:1082-1095. 10.1523/JNEUROSCI.5566-11.2012, 22262906.
33. Kim JI, Lee HR, Sim SE, Baek J, Yu NK, Choi JH, Ko HG, Lee YS, Park SW, Kwak C, et al. PI3Kgamma is required for NMDA receptor-dependent long-term depression and behavioral flexibility. Nat Neurosci 2011, 14:1447-1454. 10.1038/nn.2937, 22019731.
34. Wei F, Qiu CS, Liauw J, Robinson DA, Ho N, Chatila T, Zhuo M. Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat Neurosci 2002, 5:573-579. 10.1038/nn0602-855, 12006982.
35. Vogt BA. Pain and emotion interactions in subregions of the cingulate gyrus. Nat Rev Neurosci 2005, 6:533-544. 2659949, 15995724.
36. Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, Steenland HW, Zhuo M. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci 2008, 28:7445-7453. 10.1523/JNEUROSCI.1812-08.2008, 18632948.
37. Wu LJ, Toyoda H, Zhao MG, Lee YS, Tang J, Ko SW, Jia YH, Shum FW, Zerbinatti CV, Bu G, et al. Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation. J Neurosci 2005, 25:11107-11116. 10.1523/JNEUROSCI.1678-05.2005, 16319310.
38. Wei F, Wang GD, Kerchner GA, Kim SJ, Xu HM, Chen ZF, Zhuo M. Genetic enhancement of inflammatory pain by forebrain NR2B overexpression. Nat Neurosci 2001, 4:164-169. 10.1038/83993, 11175877.
39. Wei F, Li P, Zhuo M. Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J Neurosci 1999, 19:9346-9354.
40. Li XY, Ko HG, Chen T, Descalzi G, Koga K, Wang H, Kim SS, Shang Y, Kwak C, Park SW, et al. Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. Science 2010, 330:1400-1404. 10.1126/science.1191792, 21127255.
41. Li XY, Ko HG, Chen T, Collingridge GL, Kaang BK, Zhuo M. Erasing injury-related cortical synaptic potentiation as a new treatment for chronic pain. J Mol Med (Berl) 2011, 89:847-855.
42. Li P, Kerchner GA, Sala C, Wei F, Huettner JE, Sheng M, Zhuo M. AMPA receptor-PDZ interactions in facilitation of spinal sensory synapses. Nat Neurosci 1999, 2:972-977. 10.1038/14771, 10526335.
43. Cao XY, Xu H, Wu LJ, Li XY, Chen T, Zhuo M. Characterization of intrinsic properties of cingulate pyramidal neurons in adult mice after nerve injury. Mol Pain 2009, 5:73. 10.1186/1744-8069-5-73, 2807858, 20015370.
44. Gupta A, Wang Y, Markram H. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 2000, 287:273-278. 10.1126/science.287.5451.273, 10634775.
45. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J. Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 1997, 17:3894-3906.
46. Cauli B, Porter JT, Tsuzuki K, Lambolez B, Rossier J, Quenet B, Audinat E. Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci U S A 2000, 97:6144-6149. 10.1073/pnas.97.11.6144, 18572, 10823957.
47. Kawaguchi Y. Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 1995, 15:2638-2655.
48. Kawaguchi Y, Kubota Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 1997, 7:476-486. 10.1093/cercor/7.6.476, 9276173.
49. Zhu Y, Zhu JJ. Rapid arrival and integration of ascending sensory information in layer 1 nonpyramidal neurons and tuft dendrites of layer 5 pyramidal neurons of the neocortex. J Neurosci 2004, 24:1272-1279. 10.1523/JNEUROSCI.4805-03.2004, 14960597.
50. Wu LJ, Zhao MG, Toyoda H, Ko SW, Zhuo M. Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J Neurophysiol 2005, 94:1805-1813. 10.1152/jn.00091.2005, 15928066.
51. Wu LJ, Xu H, Ren M, Zhuo M. Genetic and pharmacological studies of GluR5 modulation of inhibitory synaptic transmission in the anterior cingulate cortex of adult mice. Dev Neurobiol 2007, 67:146-157. 10.1002/dneu.20331, 17443779.
52. Qiu S, Li XY, Zhuo M. Post-translational modification of NMDA receptor GluN2B subunit and its roles in chronic pain and memory. Semin Cell Dev Biol 2011, 22:521-529. 10.1016/j.semcdb.2011.06.003, 21704719.
53. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39. 10.1038/361031a0, 8421494.
54. Spruston N. Pyramidal neurons: dendritic structure and synaptic integration. Nat Rev Neurosci 2008, 9:206-221.
55. Larkum ME, Nevian T, Sandler M, Polsky A, Schiller J. Synaptic integration in tuft dendrites of layer 5 pyramidal neurons: a new unifying principle. Science 2009, 325:756-760. 10.1126/science.1171958, 19661433.
56. London M, Hausser M. Dendritic computation. Annu Rev Neurosci 2005, 28:503-532. 10.1146/annurev.neuro.28.061604.135703, 16033324.
57. Sjostrom PJ, Hausser M. A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron 2006, 51:227-238. 10.1016/j.neuron.2006.06.017, 16846857.
58. Bender VA, Feldman DE. A dynamic spatial gradient of Hebbian learning in dendrites. Neuron 2006, 51:153-155. 10.1016/j.neuron.2006.07.003, 16846850.
59. Perez-Garci E, Gassmann M, Bettler B, Larkum ME. The GABAB1b isoform mediates long-lasting inhibition of dendritic Ca2+ spikes in layer 5 somatosensory pyramidal neurons. Neuron 2006, 50:603-616. 10.1016/j.neuron.2006.04.019, 16701210.
60. Silberberg G, Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 2007, 53:735-746. 10.1016/j.neuron.2007.02.012, 17329212.
61. Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci 2007, 8:45-56. 10.1038/nrn2044, 17180162.
62. Zhao MG, Ko SW, Wu LJ, Toyoda H, Xu H, Quan J, Li J, Jia Y, Ren M, Xu ZC, Zhuo M. Enhanced presynaptic neurotransmitter release in the anterior cingulate cortex of mice with chronic pain. J Neurosci 2006, 26:8923-8930. 10.1523/JNEUROSCI.2103-06.2006, 16943548.