Diversity and overlap of parvalbumin and somatostatin expressing interneurons in mouse presubiculum

Frontiers in Neural Circuits

Volumn 9, Issue May, 2015, Pages

  Nassar, Merie ^a   Simonnet, Jean ^a,d   Lofredi, Roxanne ^a   Cohen, Ivan ^a   Savary, Etienne ^a   Yanagawa, Yuchio ^b,c   Miles, Richard ^a   Fricker, Desdemona ^a  

^a SORBONNE UNIVERSITÉ   (France)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Excitability; Head direction; Inhibition; Morphology; Postsubiculum

Indexed keywords

GREEN FLUORESCENT PROTEIN; PARVALBUMIN; SOMATOSTATIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; BRAIN REGION; BRAIN SLICE; CELL FUNCTION; CELL LABELING; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; GABAERGIC TRANSMISSION; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOUSE; NERVE CELL NETWORK; NERVE CONDUCTION; NONHUMAN; PRESUBICULUM; PROTEIN DETERMINATION; PROTEIN EXPRESSION; ANIMAL; BIOSYNTHESIS; CLUSTER ANALYSIS; CYTOLOGY; IMAGE PROCESSING; METABOLISM; PARAHIPPOCAMPAL GYRUS; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; THREE DIMENSIONAL IMAGING; TRANSGENIC MOUSE;

ANIMALS; CLUSTER ANALYSIS; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MICE; MICE, TRANSGENIC; PARAHIPPOCAMPAL GYRUS; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; SOMATOSTATIN;

EID: 84935906176     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2015.00020     Document Type: Article

References (85)

1. Adams, R. H., and Eichmann, A. (2010). Axon guidance molecules in vascular patterning. Cold Spring Harb. Perspect. Biol. 2:a001875. doi: 10.1101/cshper-spect.a001875.
2. Batista-Brito, R., and Fishell, G. (2009). The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 87, 81-118. doi: 10.1016/S0070-2153(09)01203-4
3. Battaglia, D., Karagiannis, A., Gallopin, T., Gutch, H. W., and Cauli, B. (2013). Beyond the frontiers of neuronal types. Front. Neural Circuits. 7:13. doi: 10.3389/fncir.2013.00013
4. Boccara, C. N., Sargolini, F., Thoresen, V. H., Solstad, T., Witter, M. P., Moser, E. I., et al. (2010). Grid cells in pre- and parasubiculum. Nat. Neurosci. 13, 987-994. doi: 10.1038/nn.2602
5. Bortone, D. S., Olsen, S. R., and Scanziani, M. (2014). Translaminar inhibitorycells recruited by layer 6 corticothalamic neurons suppress visual cortex. Neuron 82, 1-12. doi: 10.1016/j.neuron.2014.02.021
6. Cajal, R. S. (1911). Histologie du Systeme Nerveux De VHomme et des Vertebres. Paris: Maloine.
7. Calton, J. L., Stackman, R. W., Goodridge, J. P., Archey, W. B., Dudchenko, P. A., and Taube, J. S. (2003). Hippocampal place cell instability after lesions of the head direction cell network. J. Neurosci. 23, 9719-9731.
8. Cauli, B., Audinat, E., Lambolez, B., Angulo, M. C., Ropert, N., Tsuzuki, K., et al. (1997). Molecular and physiological diversity of cortical nonpyramidal cells. J. Neurosci. 17, 3894-3906.
9. Cauli, B., Porter, J. T., Tsuzuki, K., Lambolez, B., Rossier, J., Quenet, B., et al. (2000). Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc. Natl. Acad. Sci. U.S.A. 97, 6144-6149. doi: 10.1073/pnas.97.11.6144.
10. Chrobak, J. J., and Buzsaki, G. (1996). High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J. Neurosci. 16, 3056-3066.
11. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., and Somogyi, P. (1995). Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75-78. doi: 10.1038/378075a0
12. Cottam, J. C. H., Smith, S. L., and Hausser, M. (2013). Target-specific effects of somatostatin-expressing interneurons on neocortical visual processing. J. Neurosci. 33, 19567-19578. doi: 10.1523/JNEUR0SCI.2624-13.2013
13. Defelipe, J., Lopez-Cruz, P. L., Benavides-Piccione, R., Bielza, C., Larranaga, P., Anderson, S., et al. (2013). New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14, 202-216. doi: 10.1038/nrn3444.
14. Druckmann, S., Hill, S., Schurmann, F., Markram, H., and Segev, I. (2012). A hierarchical structure of cortical interneuron electrical diversity revealed by automated statistical analysis. Cereb. Cortex 23, 2994-3006. doi: 10.1093/cer-cor/bhs290.
15. Dumitriu, D., Cossart, R., Huang, J., and Yuste, R. (2006). Correlation between axonal morphologies and synaptic input kinetics of interneurons from mouse visual cortex. Cereb. Cortex 17, 81-91. doi: 10.1093/cercor/bhj126
16. Erisir, A., Lau, D., Rudy, B., and Leonard, C. S. (1999). Function of specific K(+) channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J. Neurophysiol. 82, 2476-2489.
17. Fino, E., and Yuste, R. (2011). Dense inhibitoryconnectivity in neocortex. Neuron 69, 1188-1203. doi: 10.1016/j.neuron.2011.02.025
18. Fishell, G., and Rudy, B. (2011). Mechanisms of inhibition within the telencephalon: “where the wild things are.” Annu. Rev. Neurosci. 34, 535-567. doi: 10.1146/annurev-neuro-061010-113717
19. Freund, T. F., and Buzsaki, G. (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470. doi: 10.1002/(SICI)1098-1063(1996)6:4<347::AID-HIP01>3.0.C0;2-I
20. Fricker, D., and Miles, R. (2000). EPSP amplification and the precision of spike timing in hippocampal neurons. Neuron 28, 559-569. doi: 10.1016/S0896-6273(00)00133-1.
21. Fricker, D., and Miles, R. (2001). Interneurons, spike timing, and perception. Neuron 32, 771-774. doi: 10.1016/S0896-6273(01)00528-1
22. Gabernet, L., Jadhav, S. P., Feldman, D. E., Carandini, M., and Scanziani, M. (2005). Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48, 315-327. doi: 10.1016/j.neuron.2005.09.022.
23. Gentet, L. J., Kremer, Y., Taniguchi, H., Huang, Z. J., Staiger, J. F., and Petersen, C. H. (2012). Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607-612. doi: 10.1038/nn.3051.
24. Golowasch, J., Thomas, G., Taylor, A. L., Patel, A., Pineda, A., Khalil, C., et al. (2009). Membrane capacitance measurements revisited: dependence of capacitance value on measurement method in nonisopotential neurons. J. Neurophysiol. 102, 2161-2175. doi: 10.1152/jn.00160.2009
25. Gonchar, Y., and Burkhalter, A. (1997). Three distinct families of GABAergic neurons in rat visual cortex. Cereb. Cortex 7, 347-358. doi: 10.1093/cercor/7.4.347
26. Gonchar, Y., Wang, Q., and Burkhalter, A. (2007). Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostain-ing. Front. Neuroanat. 1:3.doi: 10.3389/neuro.05.003.2007
27. Halabisky, B., Shen, F., Huguenard, J. R., and Prince, D. A. (2006). Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimotor cortex. J. Neurophysiol. 96, 834-845. doi: 10.1152/jn.01079.2005
28. Heffner, C. S., Pratt, C. H., Babiuk, R. P., Sharma, Y., Rockwood, S. F., Donahue, L. R., et al. (2012). Supporting conditional mouse mutagenesis with a comprehensive cre characterization resource. Nat. Comms. 3:1218. doi: 10.1038/ncomms2186
29. Helm, J., Akgul, G., and Wollmuth, L. P. (2013). Subgroups of parvalbumin-expressing interneurons in layers 2/3 of the visual cortex. J. Neurophysiol. 109, 1600-1613. doi: 10.1152/jn.00782.2012
30. Hippenmeyer, S., Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D. R., et al. (2005). A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3:e159. doi: 10.1371/jour-nal.pbio.0030159.
31. Honda, Y., and Ishizuka, N. (2004). Organization of connectivity of the rat presubiculum: I. Efferent projections to the medial entorhinal cortex. J. Comp. Neurol. 473, 463-484. doi: 10.1002/cne.20093
32. Hu, H., Cavendish, J. Z., and Agmon, A. (2013). Not all that glitters is gold: off-target recombination in the somatostatin-IRES-Cre mouse line labels a subset of fast-spiking interneurons. Front. Neural. Circuits. 7:195. doi: 10.3389/fncir.2013.00195
33. Isaacson, J. S., and Scanziani, M. (2011). How inhibition shapes cortical activity. Neuron 72, 231-243. doi: 10.1016/j.neuron.2011.09.027
34. Jinno, S., and Kosaka, T. (2000). Colocalization of parvalbumin and somatostatinlike immunoreactivity in the mouse hippocampus: quantitative analysis with optical dissector. J. Comp. Neurol. 428, 377-388. doi: 10.1002/1096-9861(20001218)428:3<377::AID-CNE1>3.0.C0;2-L
35. Karagiannis, A., Gallopin, T., David, C., Battaglia, D., Geoffroy, H., Rossier, J., et al. (2009). Classification of NPY-expressing neocortical interneurons. J. Neurosci. 29, 3642-3659. doi: 10.1523/JNEUR0SCI.0058-09.2009
36. Karnani, M. M., Agetsuma, M., and Yuste, R. (2014). Science Direct A blanket of inhibition: functional inferences from dense inhibitory connectivity. Curr. Opin. Neurobiol. 26, 96-102. doi: 10.1016/j.conb.2013.12.015
37. Karube, F., Kubota, Y., and Kawaguchi, Y. (2004). Axon branching and synaptic bouton phenotypes in GABAergic nonpyramidal cell subtypes. J. Neurosci. 24, 2853-2865. doi: 10.1523/JNEUROSCI.4814-03.2004
38. Katona, L., Lapray, D., Viney, T. J., Oulhaj, A., Borhegyi, Z., Micklem, B. R., et al. (2014). Sleep and movement differentiates actions of two types of somatostatin-expressing GABAergic interneuron in rat hippocampus. Neuron 82, 872-886. doi: 10.1016/j.neuron.2014.04.007
39. Kawaguchi, Y. (1995). Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J. Neurosci. 15, 2638-2655.
40. Kawaguchi, Y., Karube, F., and Kubota, Y. (2006). Dendritic branch typing and spine expression patterns in cortical nonpyramidal cells. Cereb. Cortex 16, 696-711. doi: 10.1093/cercor/bhj015
41. Kawaguchi, Y., and Kubota, Y. (1997). GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476-486. doi: 10.1093/cer-cor/7.6.476.
42. Kepecs, A., and Fishell, G. (2014). Interneuron cell types are fit to function. Nature 505, 318-326. doi: 10.1038/nature12983
43. Klausberger, T., Marton, L. F., Baude, A., Roberts, J. D. B., Magill, P. J., and Somogyi, P. (2003). Spike timing of dendrite-targeting bistratified cells during hippocampal network oscillations in vivo. Nat. Neurosci. 7, 41-47. doi: 10.1038/nn1159.
44. Kononenko, N. L., and Witter, M. P. (2012). Presubiculum layer III conveys retro-splenial input to the medial entorhinal cortex. Hippocampus 22, 881-895. doi: 10.1002/hipo.20949.
45. Kubota, Y. (2014). Untangling GABAergic wiring in the cortical microcircuit. Curr. Opin. Neurobiol. 26, 7-14. doi: 10.1016/j.conb.2013.10.003
46. Kubota, Y., Shigematsu, N., Karube, F., Sekigawa, A., Kato, S., Yamaguchi, N., et al. (2011). Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAergic neurons. Cereb. Cortex 21, 1803-1817. doi: 10.1093/cercor/bhq252
47. Kvitsiani, D., Ranade, S., Hangya, B., Taniguchi, H., Huang, J. Z., and Kepecs, A. (2013). Distinct behavioural and networkcorrelates of two interneuron types in prefrontal cortex. Nature 498, 363-366. doi: 10.1038/nature12176.
48. Lorente de No, R. (1933). Studies on the structure of the cerebral cortex. J. fur Psychol. Neurol. 45, 381-438.
49. Ma, Y., Hu, H., Berrebi, A. S., Mathers, P. H., and Agmon, A. (2006). Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26, 5069-5082. doi: 10.1523/JNEUROSCI.0661-06.2006
50. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., et al. (2010). A robust and high-throughput cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140. doi: 10.1038/nn.2467.
51. Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., and Wu, C. (2004). Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793-807. doi: 10.1038/nrn1519
52. Martina, M., Schultz, J. H., Ehmke, H., Monyer, H., and Jonas, P. (1998). Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J. Neurosci. 18, 8111-8125.
53. McGarry, L. M., Packer, A. M., Fino, E., Nikolenko, V., Sippy, T., and Yuste, R. (2010). Quantitative classification of somatostatin-positive neocortical interneurons identifies three interneuron subtypes. Front. Neural. Circuits. 4:12. doi: 10.3389/fncir.2010.00012
54. Miles, R., Toth, K., Gulyas, A. I., Hajos, N., and Freund, T. F. (1996). Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16, 815-823. doi: 10.1016/S0896-6273(00)80101-4
55. Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., et al. (2010). Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J. Neurosci. 30, 1582-1594. doi: 10.1523/JNEUROSCI.4515-09.2010.
56. O'Mara, S. M., Commins, S., Anderson, M., and Gigg, J. (2001). The subiculum: a review of form, physiology and function. Prog. Neurobiol. 64, 129-155. doi: 10.1016/S0301-0082(00)00054-X
57. Packer, A. M., and Yuste, R. (2011). Dense, unspecific connectivity of neocorti-cal parvalbumin-positive interneurons: a canonical microcircuit for inhibition? J. Neurosci. 31, 13260-13271. doi: 10.1523/JNEUR0SCI.3131-11.2011
58. Parra, P., Gulyas, A. I., and Miles, R. (1998). How many subtypes of inhibitory cells in the hippocampus? Neuron 20, 983-993. doi: 10.1016/S0896-6273(00)80479-1
59. Perrenoud, Q., Rossier, J., Geoffroy, H., Vitalis, T., and Gallopin, T. (2012). Diversity of GABAergic interneurons in layer VIa and VIb of mouse barrel cortex. Cereb. Cortex 23, 423-421. doi: 10.1093/cercor/bhs032
60. Petilla Interneuron Nomenclature Group, Ascoli, G. A., Alonso-Nanclares, L., Anderson, S. A., Barrionuevo, G., Benavides-Piccione, R., et al. (2008). Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat. Rev. Neurosci. 9, 557-568. doi: 10.1038/nrn2402
61. Pouille, F., and Scanziani, M. (2001). Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293, 1159-1163. doi: 10.1126/science.1060342
62. Rowland, D. C., Weible, A. P., Wickersham, I. R., Wu, H., Mayford, M., Witter, M. P., et al. (2013). Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J. Neurosci. 33, 14889-14898. doi: 10.1523/JNEUROSCI.1046-13.2013.
63. Rudy, B., Fishell, G., Lee, S., and Hjerling-Leffler, J. (2010). Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev. Neurobio. 71, 45-61. doi: 10.1002/dneu.20853
64. Schlingloff, D., Kali, S., Freund, T. F., Hajos, N., and Gulyas, A. I. (2014). Mechanisms of sharp wave initiation and ripple generation. J. Neurosci. 34, 11385-11398. doi: 10.1523/JNEUR0SCI.0867-14.2014
65. Silberberg, G., and Markram, H. (2007). Disynaptic inhibition between neocor-tical pyramidal cells mediated by Martinotti cells. Neuron 53, 735-746. doi: 10.1016/j.neuron.2007.02.012
66. Simonnet, J., Eugene, E., Cohen, I., Miles, R., and Fricker, D. (2013). Cellular neuroanatomy of rat presubiculum. Eur. J. Neurosci. 37, 583-597. doi: 10.1111/ejn.12065.
67. Somogyi, P., and Klausberger, T. (2005). Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. (Lond) 562, 9-26. doi: 10.1113/jphysiol.2004.078915
68. Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J.-I., Obata, K., and 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, 60-79. doi: 10.1002/cne.10905
69. Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., et al. (2011). A resource of cre driver lines for genetic targeting of GABAergic eurons in cerebral cortex. Neuron 71, 995-1013. doi: 10.1016/j.neuron.2011.07.026
70. Taube, J. S. (2007). The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181-207. doi: 10.1146/annurev.neuro.29.051605.112854
71. Taube, J. S., Muller, R. U., and Ranck, J. B. (1990). Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10, 436-447.
72. Thorndike, R. L. (1953). Who belongs in the family? Psychometrika 18, 267-276. doi: 10.1007/BF02289263
73. Uematsu, M., Hirai, Y., Karube, F., Ebihara, S., Kato, M., Abe, K., et al. (2007). Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb. Cortex 18, 315-330. doi: 10.1093/cer-cor/bhm056.
74. van Groen, T., and Wyss, J. M. (1990a). The connections of presubiculum and parasubiculum in the rat. Brain Res. 518, 227-243. doi: 10.1016/0006-8993(90)90976-Iv
75. an Groen, T., and Wyss, J. M. (1990b).The postsubicularcortex in the rat: characterization of the fourth region of the subicular cortex and its connections. Brain Res. 529, 165-177. doi: 10.1016/0006-8993(90)90824-U
76. van Haeften, T., Wouterlood, F. G., Jorritsma-Byham, B., and Witter, M. P. (1997). GABAergic presubicular projections to the medial entorhinal cortex of the rat. J. Neurosci. 17, 862-874.
77. Van Strien, N. M., Cappaert, N. L. M., and Witter, M. P. (2009). The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat. Rev. Neurosci. 10, 272-282. doi: 10.1038/nrn2614
78. Wang, Y., Gupta, A., Toledo-Rodriguez, M., Wu, C. Z., and Markram, H. (2002). Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb. Cortex 12, 395-410. doi: 10.1093/cercor/12.4.395
79. Wang, Y., Toledo-Rodriguez, M., Gupta, A., Wu, C., Silberberg, G., Luo, J., et al. (2004). Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J. Physiol. (Lond) 561, 65-90. doi: 10.1113/jphysiol.2004.073353
80. Ward, J. H. Jr. (1963). Hierarchical grouping to optimize an objective function. J. Am. Stat. Assoc. 58, 236-244. doi: 10.1080/01621459.1963.10500845
81. Wonders, C. P., and Anderson, S. A. (2006). The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 7, 687-696. doi: 10.1038/nrn1954.
82. Xu, H., Jeong, H.-Y, Tremblay, R., and Rudy, B. (2013). Neocortical somatostatin-expressing GABAergic interneurons disinhibit the thalamorecipient layer 4. Neuron 77, 155-167. doi: 10.1016/j.neuron.2012.11.004
83. Xu, Q., Cobos, I., La Cruz De, E., Rubenstein, J. L., and Anderson, S. A. (2004). Origins of cortical interneuron subtypes. J. Neurosci. 24, 2612-2622. doi: 10.1523/JNEUROSCI.5667-03.2004
84. Xu, X., Roby, K. D., and Callaway, E. M. (2010). Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitorycells. J. Comp. Neurol. 518, 389-404. doi: 10.1002/cne.22229
85. Yoder, R. M., Clark, B. J., and Taube, J. S. (2011). Origins oflandmarkencoding in the brain. Trends Neurosci. 34, 561-571. doi: 10.1016/j.tins.2011.08.004