Thalamocortical Innervation Pattern in Mouse Auditory and Visual Cortex: Laminar and Cell-Type Specificity

Cerebral Cortex

Volumn 26, Issue 6, 2016, Pages 2612-2625

  Ji, Xu Ying ^a,b   Zingg, Brian ^b,d   Mesik, Lukas ^b,d   Xiao, Zhongju ^a   Zhang, Li I ^b,c   Tao, Huizhong W ^b,c  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

^b Zilkha Neurogenetic Institute   (China)

^c Department of Cell and Neurobiology ^*  (China)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Cortical inhibitory neuron; Laminar distribution; Pyramidal cell; Sensory cortex; SOM neuron; Thalamic innervation; Thalamocortical projection; VIP neuron

Indexed keywords

SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE; PARVALBUMIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXON; CONTROLLED STUDY; FEMALE; INNERVATION; MALE; MEDIAL GENICULATE BODY; MOUSE; NEOCORTICAL SLICE; NERVE CELL EXCITABILITY; NONHUMAN; OPTOGENETICS; ORGANUM VASCULOSUM OF THE LAMINA TERMINALIS; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; THALAMOCORTICAL TRACT; VISUAL CORTEX; ANIMAL; AUDITORY CORTEX; CYTOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; FLUORESCENCE MICROSCOPY; INHIBITORY POSTSYNAPTIC POTENTIAL; METABOLISM; NERVE CELL; NERVE TRACT; NEUROANATOMICAL TRACT TRACING; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; THALAMUS; TISSUE CULTURE TECHNIQUE; TRANSGENIC MOUSE;

ANIMALS; AUDITORY CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; NEURAL PATHWAYS; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONS; OPTOGENETICS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; SOMATOSTATIN; THALAMUS; TISSUE CULTURE TECHNIQUES; VASOACTIVE INTESTINAL PEPTIDE; VISUAL CORTEX;

EID: 84974575047     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhv099     Document Type: Article

References (89)

1. Adesnik H, Bruns W, Taniguchi H, Huang ZJ, Scanziani M. 2012. A neural circuit for spatial summation in visual cortex. Nature. 490:226-231.
2. Agmon A, Connors BW. 1992. Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci. 12:319-329.
3. Agmon A, Connors BW. 1991. Thalamocortical responses of mice somatosensory (barrel) cortex in vitro. Neuroscience. 41:365-379.
4. Armstrong-James M, Fox K, Das-Gupta A. 1992. Flow of excitation within rat barrel cortex on striking a single vibrissa. J Neurophysiol. 68:1345-1358.
5. Barkat TR, Polley DB, Hensch TK. 2011. A critical period for auditory thalamocortical connectivity. Nat Neurosci. 14:1189-1194.
6. Beierlein M, Gibson JR, Connors BW. 2003. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol. 90:2987-3000.
7. Berger TK, Silberberg G, Perin R, Markram H. 2010. Brief bursts self-inhibit and correlate the pyramidal network. PLoS Biol. 8:e1000473.
8. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. 2005. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci. 8:1263-1268.
9. Callaway EM. 1998. Local circuits in primary visual cortex of the macaque monkey. Annu Rev Neurosci. 21:47-74.
10. Cardin JA, CarlenM, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 459:663-667.
11. Chung S, Ferster D. 1998. Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron. 20:1177-1189.
12. Citas JS, de Venecia RK, McMullen NT. 1999. Thalamocortical afferents of Lorente de Nó: medial geniculate axons that project to primary auditory cortex have collateral branches to layer I. Brain Res. 830:203-208.
13. Constantinople CM, Bruno RM. 2013. Deep cortical layers are activated directly by thalamus. Science. 340:1591-1594.
14. Cruikshank SJ, Ahmed OJ, Stevens TR, Patrick SL, Gonzalez AN, Elmaleh M, Connors BW. 2012. Thalamic control of layer 1 circuits in prefrontal cortex. J Neurosci. 32:17813-17823.
15. Cruikshank SJ, Lewis TJ, Connors BW. 2007. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci. 10:462-468.
16. Cruikshank SJ, Rose HJ, Metherate R. 2002. Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol. 87:361-384.
17. Cruikshank SJ, Urabe H, Nurmikko AV, Connors BW. 2010. Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron. 65:230-245.
18. Cruz-Martín A, El-Danaf RN, Osakada F, Sriram B, Dhande OS, Nguyen PL, Callaway EM, Ghosh A, Huberman AD. 2014. A dedicated circuit links direction-selective retinal ganglion cells to the primary visual cortex. Nature. 507:358-361.
19. Douglas RJ, Martin KA. 2004. Neuronal circuits of the neocortex. Annu Rev Neurosci. 27:419-451.
20. Feldmeyer D. 2012. Excitatory neuronal connectivity in the barrel cortex. Front Neuroanat. 6:24.
21. Ferster D, Lindström S. 1983. An intracellular analysis of geniculocortical connectivity in area 17 of the cat. J Physiol. 342:181-215.
22. Frost DO, Caviness VS Jr. 1980. Radial organization of thalamic projections to the neocortex in the mouse. J Comp Neurol. 194:369-393.
23. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M. 2005. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron. 48:315-327.
24. Gibson JR, Beierlein M, Connors BW. 1999. Two networks of electrically coupled inhibitory neurons in neocortex. Nature. 402:75-79.
25. Gilbert CD, Wiesel TN. 1979. Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature. 280:120-125.
26. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. 2009. Optical deconstruction of parkinsonian neural circuitry. Science. 324:354-359.
27. Hajós F, Staiger JF, Halasy K, Freund TF, Zilles K. 1997. Geniculocortical afferents form synaptic contacts with vasoactive intestinal polypeptide (VIP) immunoreactive neurons of the rat visual cortex. Neurosci Lett. 228:179-182.
28. Herkenham M. 1980. Laminar organization of thalamic projections to the rat neocortex. Science. 207:532-535.
29. Higley MJ, Contreras D. 2006. Balanced excitation and inhibition determine spike timing during frequency adaptation. J Neurosci. 26:448-457.
30. Huang CL, Winer JA. 2000. Auditory thalamocortical projections in the cat: laminar and areal patterns of input. J Comp Neurol. 427:302-331.
31. Inoue T, Imoto K. 2006. Feedforward inhibitory connections from multiple thalamic cells to multiple regular-spiking cells in layer 4 of the somatosensory cortex. J Neurophysiol. 96:1746-1754.
32. Jiang X, Wang G, Lee AJ, Stornetta RL, Zhu JJ. 2013. The organization of two new cortical interneuronal circuits. Nat Neurosci. 16:210-218.
33. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M. 2007. Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci. 10:743-753.
34. Kloc M, Maffei A. 2014. Target-specific properties of thalamocortical synapses onto layer 4 of mouse primary visual cortex. J Neurosci. 34:15455-15465.
35. Li LY, Ji XY, Liang F, Li YT, Xiao Z, Tao HW, Zhang LI. 2014. A feedforward inhibitory circuit mediates lateral refinement of sensory representation in upper layer 2/3 of mouse primary auditory cortex. J Neurosci. 34:13670-13683.
36. Li LY, Li YT, Zhou M, Tao HW, Zhang LI. 2013. Intracortical multiplication of thalamocortical signals in mouse auditory cortex. Nat Neurosci. 16:1179-1181.
37. Li LY, Xiong XR, Ibrahim LA, YuanW, Tao HW, Zhang LI. 2015. Differential receptive field properties of parvalbumin and somatostatin inhibitory neurons in mouse auditory cortex. Cereb Cortex. 25:1782-1791.
38. Li YT, Ibrahim LA, Liu BH, Zhang LI, Tao HW. 2013. Linear transformation of thalamocortical input by intracortical excitation. Nat Neurosci. 16:1324-1330.
39. Lien AD, Scanziani M. 2013. Tuned thalamic excitation is amplified by visual cortical circuits. Nat Neurosci. 16:1315-1323.
40. Linke R. 1999. Organization of projections to temporal cortex originating in the thalamic posterior intralaminar nucleus of the rat. Exp Brain Res. 127:314-320.
41. Linke R, Schwegler H. 2000. Convergent and complementary projections of the caudal paralaminar thalamic nuclei to rat temporal and insular cortex. Cereb Cortex. 10:753-771.
42. Liu BH, Wu GK, Arbuckle R, Tao HW, Zhang LI. 2007. Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci. 10:1594-1600.
43. Llano DA, Sherman SM. 2008. Evidence for nonreciprocal organization of the mouse auditory thalamocortical-corticothalamic projection systems. J Comp Neurol. 507:1209-1227.
44. Ma WP, Liu BH, Li YT, Huang ZJ, Zhang LI, Tao HW. 2010. Visual representations by cortical somatostatin inhibitory neurons-selective but with weak and delayed responses. J Neurosci. 30:14371-14379.
45. Madisen L, Mao T, Koch H, Zhuo JM, Berenyi A, Fujisawa S, Hsu YW, Garcia AJ 3rd, Gu X, Zanella S, et al. 2012. A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci. 15:793-802.
46. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, WuC. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci. 5:793-807.
47. Mitani A, Shimokouchi M, Itoh K, Nomura S, Kudo M, Mizuno N. 1985. Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat. J Comp Neurol. 235:430-447.
48. Moore AK, Wehr M. 2013. Parvalbumin-expressing inhibitory interneurons in auditory cortex are well-tuned for frequency. J Neurosci. 33:13713-13723.
49. Moore CI, Nelson SB. 1998. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J Neurophysiol. 80:2882-2892.
50. Nagel G, Szellas T, Huhn W, Kateriya S, Adeishvili N, Berthold P, Ollig D, Hegemann P, Bamberg E. 2003. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci USA. 100:13940-13945.
51. OberlaenderM, Ramirez A, Bruno RM. 2012. Sensory experience restructures thalamocortical axons during adulthood. Neuron. 74:648-655.
52. Petreanu L, Huber D, Sobczyk A, Svoboda K. 2007. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nat Neurosci. 10:663-668.
53. Petreanu L, Mao T, Sternson SM, Svoboda K. 2009. The subcellular organization of neocortical excitatory connections. Nature. 457:1142-1145.
54. Pfeffer CK, XueM, HeM, Huang ZJ, ScanzianiM. 2013. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci. 16:1068-1076.
55. Porter JT, Johnson CK, Agmon A. 2001. Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci. 21:2699-2710.
56. Richardson RJ, Blundon JA, Bayazitov IT, Zakharenko SS. 2009. Connectivity patterns revealed by mapping of active inputs on dendrites of thalamorecipient neurons in the auditory cortex. J Neurosci. 29:6406-6417.
57. Romanski LM, LeDoux JE. 1993. Organization of rodent auditory cortex: Anterograde transport of PHA-L from MGv to temporal neocortex. Cereb Cortex. 3:499-514.
58. Rose HJ, Metherate R. 2005. Auditory thalamocortical transmission is reliable and temporally precise. J Neurophysiol. 94:2019-2030.
59. Rudy B, Fishell G, Lee S, Hjerling-Leffler J. 2011. Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol. 71:45-61.
60. Ryugo DK, Killackey HP. 1974. Differential telencephalic projections of the medial and ventral divisions of the medial geniculate body of the rat. Brain Res. 82:173-177.
61. Schiff ML, Reyes AD. 2012. Characterization of thalamocortical responses of regular-spiking and fast-spiking neurons of the mouse auditory cortex in vitro and in silico. J Neurophysiol. 107:1476-1488.
62. Sherman SM, Guillery RW. 2002. The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond B Biol Sci. 357:1695-1708.
63. Silberberg G, Markram H. 2007. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron. 53:735-746.
64. Simons DJ, Carvell GE. 1989. Thalamocortical response transformation in the rat vibrissa/barrel system. J Neurophysiol. 61:311-330.
65. Smith PH, Manning KA, Uhlrich DJ. 2010. Evaluation of inputs to rat primary auditory cortex fromthe suprageniculate nucleus and extrastriate visual cortex. J Comp Neurol. 518:3679-3700.
66. Smith PH, Uhlrich DJ, Manning KA, Banks MI. 2012. Thalamocortical projections to rat auditory cortex from the ventral and dorsal divisions of the medial geniculate nucleus. J Comp Neurol. 520:34-51.
67. Staiger JF, Zilles K, Freund TF. 1996. Innervation of VIP-immunoreactive neurons by the ventroposteromedial thalamic nucleus in the barrel cortex of the rat. J Comp Neurol. 367:194-204.
68. Sun QQ, Huguenard JR, Prince DA. 2006. Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci. 26:1219-1230.
69. Sun YJ, Kim YJ, Ibrahim LA, Tao HW, Zhang LI. 2013. Synaptic mechanisms underlying functional dichotomy between intrinsic-bursting and regular-spiking neurons in auditory cortical layer 5. J Neurosci. 33:5326-5339.
70. SwadlowHA. 1990. Efferent neurons and suspected interneurons in S-1 forelimb representation of the awake rabbit: receptive fields and axonal properties. J Neurophysiol. 63:1477-1498.
71. Swadlow HA. 1989. Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties. J Neurophysiol. 62:288-308.
72. Takesian AE, Kotak VC, Sharma N, Sanes DH. 2013. Hearing loss differentially affects thalamic drive to two cortical interneuron subtypes. J Neurophysiol. 110:999-1008.
73. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. 2003. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol. 467:60-479.
74. Tan Z, Hu H, Huang ZJ, Agmon A. 2008. Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc Natl Acad Sci USA. 105:2187-2192.
75. Taniguchi H, He M, Wu P, KimS, Paik R, Sugino K, Kvitsiani D, Fu Y, Lu J, Lin Y, et al. 2011. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron. 71:995-1013.
76. Viaene AN, Petrof I, Sherman SM. 2011. Synaptic properties of thalamic input to layers 2/3 and 4 of primary somatosensory and auditory cortices. J Neurophysiol. 105:279-292.
77. ViaeneAN, Petrof I, ShermanSM. 2011. Synapticpropertiesof thalamic input to the subgranular layers of primary somatosensory and auditory cortices in the mouse. J Neurosci. 31:12738-12747.
78. Wang Y, Toledo-Rodriguez M, Gupta A, Wu C, Silberberg G, Luo J, Markram H. 2004. Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol. 561:65-90.
79. Wehr M, ZadorAM. 2003. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature. 426:442-446.
80. White EL. 1978. Identified neurons in mouse Sml cortex which are postsynaptic to thalamocortical axon terminals: A combined Golgi-electron microscopic and degeneration study. J Comp Neurol. 181:627-661.
81. Winer JA, Miller LM, Lee CC, Schreiner CE. 2005. Auditory thalamocortical transformation: structure and function. Trends Neurosci. 28:255-263.
82. Wu GK, Arbuckle R, Liu BH, Tao HW, Zhang LI. 2008. Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron. 58:132-143.
83. Xu H, Jeong HY, Tremblay R, Rudy B. 2013. Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron. 77:155-167.
84. Yamamoto T, Samejima A, Oka H. 1990. The mode of synaptic activation of pyramidal neurons in the cat primary somatosensory cortex: An intracellular HRP study. Exp Brain Res. 80:12-22.
85. Zhang LI, Tan AY, Schreiner CE, Merzenich MM. 2003. Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature. 424:201-205.
86. Zhou M, Liang F, Xiong XR, Li L, Li H, Xiao Z, Tao HW, Zhang LI. 2014. Scaling down of balanced excitation and inhibition by active behavioral states in auditory cortex. Nat Neurosci. 17:841-850.
87. Zhou Y, Liu BH, Wu GK, Kim YJ, Xiao Z, Tao HW, Zhang LI. 2010. Preceding inhibition silences layer 6 neurons in auditory cortex. Neuron. 65:706-717.
88. Zhou Y, Mesik L, Sun YJ, Liang F, Xiao Z, Tao HW, Zhang LI. 2012. Generation of spike latency tuning by thalamocortical circuits in auditory cortex. J Neurosci. 32:9969-9980.
89. Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, FosterNN, Yamashita S, Bowman I, TogaAW, et al. 2014. Neural networks of the mouse neocortex. Cell. 156:1096-1111.