Distinct physiological and developmental properties of hippocampal CA2 subfield revealed by using anti-Purkinje cell protein 4 (PCP4) immunostaining

Journal of Comparative Neurology

Volumn 522, Issue 6, 2014, Pages 1333-1354

  San Antonio, Andrew ^a   Liban, Kristopher ^a   Ikrar, Taruna ^a   Tsyganovskiy, Eugene ^a   Xu, Xiangmin ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Irvine   (United States)

Author keywords

Circuit mapping; Electrophysiology; Immunochemical

Indexed keywords

CELL PROTEIN; PROTEIN ANTIBODY; PURKINJE CELL PROTEIN 4; PURKINJE CELL PROTEIN 4 ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; BRAIN NERVE CELL; CELL STRUCTURE; CONTROLLED STUDY; CYTOARCHITECTURE; DENDRITIC SPINE; DENTATE GYRUS; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; MOUSE; NEUROPHYSIOLOGY; NONHUMAN; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE FIBER; SPIKE; SYNAPSE;

CIRCUIT MAPPING; ELECTROPHYSIOLOGY; IMMUNOCHEMICAL;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CA2 REGION, HIPPOCAMPAL; CALBINDIN 2; CALCIUM-BINDING PROTEINS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; LUMINESCENT PROTEINS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS;

EID: 84896030778     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23486     Document Type: Article

References (46)

1. Bischofberger J, Engel D, Li L, Geiger JR, Jonas P. 2006. Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat Protoc 1:2075-2081.
2. Bland ST, Tamlyn JP, Barrientos RM, Greenwood BN, Watkins LR, Campeau S, Day HE, Maier SF. 2007. Expression of fibroblast growth factor-2 and brain-derived neurotrophic factor mRNA in the medial prefrontal cortex and hippocampus after uncontrollable or controllable stress. Neuroscience 144:1219-1228.
3. Brivanlou IH, Dantzker JL, Stevens CF, Callaway EM. 2004. Topographic specificity of functional connections from hippocampal CA3 to CA1. Proc Natl Acad Sci U S A 101:2560-2565.
4. Burkhalter A. 2008. Many specialists for suppressing cortical excitation. Front Neurosci 2:155-167.
5. Caruana DA, Alexander GM, Dudek SM. 2012. New insights into the regulation of synaptic plasticity from an unexpected place: hippocampal area CA2. Learn Mem 19:391-400.
6. Chevaleyre V, Siegelbaum SA. 2010. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 66:560-572.
7. Dailey ME, Buchanan J, Bergles DE, Smith SJ. 1994. Mossy fiber growth and synaptogenesis in rat hippocampal slices in vitro. J Neurosci 14:1060-1078.
8. Dantzker JL, Callaway EM. 2000. Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat Neurosci 3:701-707.
9. Fletcher TL, Cameron P, De Camilli P, Banker G. 1991. The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J Neurosci 11:1617-1626.
10. Forster E, Zhao S, Frotscher M. 2006. Laminating the hippocampus. Nat Rev Neurosci 7:259-267.
11. Grove EA, Tole S. 1999. Patterning events and specification signals in the developing hippocampus. Cereb Cortex 9:551-561.
12. Ishizuka N, Cowan WM, Amaral DG. 1995. A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. J Comp Neurol 362:17-45.
13. Jones MW, McHugh TJ. 2011. Updating hippocampal representations: CA2 joins the circuit. Trends Neurosci 34:526-535.
14. Jung MW, Wiener SI, McNaughton BL. 1994. Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat. J Neurosci 14:7347-7356.
15. Kawaguchi Y, Kondo S. 2002. Parvalbumin, somatostatin and cholecystokinin as chemical markers for specific GABAergic interneuron types in the rat frontal cortex. J Neurocytol 31:277-287.
16. Kleerekoper QK, Putkey JA. 2009. PEP-19, an intrinsically disordered regulator of calmodulin signaling. J Biol Chem 284:7455-7464.
17. Laeremans A, Nys J, Luyten W, D'Hooge R, Paulussen M, Arckens L. 2013. AMIGO2 mRNA expression in hippocampal CA2 and CA3a. Brain Struct Funct 218:123-130.
18. Lein ES, Zhao X, Gage FH. 2004. Defining a molecular atlas of the hippocampus using DNA microarrays and high-throughput in situ hybridization. J Neurosci 24:3879-3889.
19. Lein ES, Callaway EM, Albright TD, Gage FH. 2005. Redefining the boundaries of the hippocampal CA2 subfield in the mouse using gene expression and 3-dimensional reconstruction. J Comp Neurol 485:1-10.
20. Lorente de Nó R. 1934. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol (Lpz) 46:113-177.
21. Madisen L, Zwingman Ta, Sunkin SM, Oh SW, Zariwala Ha, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. 2010. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 13:133-140.
22. Mercer A, Trigg HL, Thomson AM. 2007. Characterization of neurons in the CA2 subfield of the adult rat hippocampus. J Neurosci 27:7329-7338.
23. Murphy GJ, Du LS. 2001. Postnatal development of spike generation in rat medial vestibular nucleus neurons. J Neurophysiol 85:1899-1906.
24. Ochiishi T, Saitoh Y, Yukawa A, Saji M, Ren Y, Shirao T, Miyamoto H, Nakata H, Sekino Y. 1999. High level of adenosine A1 receptor-like immunoreactivity in the CA2/CA3a region of the adult rat hippocampus. Neuroscience 93:955-967.
25. Putkey JA, Kleerekoper Q, Gaertner TR, Waxham MN. 2003. A new role for IQ motif proteins in regulating calmodulin function. J Biol Chem 278:49667-49670.
26. Romer B, Krebs J, Overall RW, Fabel K, Babu H, Overstreet-Wadiche L, Brandt MD, Williams RW, Jessberger S, Kempermann G. 2011. Adult hippocampal neurogenesis and plasticity in the infrapyramidal bundle of the mossy fiber projection: I. Co-regulation by activity. Front Neurosci 5:107.
27. Sahay A, Hen R. 2007. Adult hippocampal neurogenesis in depression. Nat Neurosci 10:1110-1115.
28. Shepherd GM, Svoboda K. 2005. Laminar and columnar organization of ascending excitatory projections to layer 2/3 pyramidal neurons in rat barrel cortex. J Neurosci 25:5670-5679.
29. Shepherd GM, Stepanyants A, Bureau I, Chklovskii D, Svoboda K. 2005. Geometric and functional organization of cortical circuits. Nat Neurosci 8:782-790.
30. Shi Y, Nenadic Z, Xu X. 2010. Novel use of matched filtering for synaptic event detection and extraction. PLoS One 5:e15517.
31. Simons SB, Escobedo Y, Yasuda R, Dudek SM. 2009. Regional differences in hippocampal calcium handling provide a cellular mechanism for limiting plasticity. Proc Natl Acad Sci U S A 106:14080-14084.
32. Sloviter RS. 1989. Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280:183-196.
33. Swanson LW, Wyss JM, Cowan WM. 1978. An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181:681-715.
34. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Fu Y, Lu J, Lin Y, Miyoshi G, Shima Y, Fishell G, Nelson SB, Huang ZJ. 2011. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:995-1013.
35. Tole S, Christian C, Grove EA. 1997. Early specification and autonomous development of cortical fields in the mouse hippocampus. Development 124:4959-4970.
36. Weiler N, Wood L, Yu J, Solla SA, Shepherd GM. 2008. Top-down laminar organization of the excitatory network in motor cortex. Nat Neurosci 11:360-366.
37. Xu X. 2011. "High precision and fast functional mapping of brain circuitry through laser scanning photostimulation and fast dye imaging, " In: Laser Scanning, Theory and Applications, editor Wang C.-C, Madrid: (Rijeka, Croatia: InTech), 113-132.
38. Xu X, Callaway EM. 2009. Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J Neurosci 29:70-85.
39. Xu X, Roby KD, Callaway EM. 2006. Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 499:144-160.
40. Xu X, Roby KD, Callaway EM. 2010. Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 518:389-404.
41. Young WS, Li J, Wersinger SR, Palkovits M. 2006. The vasopressin 1b receptor is prominent in the hippocampal area CA2 where it is unaffected by restraint stress or adrenalectomy. Neuroscience 143:1031-1039.
42. Zhang W, Huguenard JR, Buckmaster PS. 2012. Increased excitatory synaptic input to granule cells from hilar and CA3 regions in a rat model of temporal lobe epilepsy. J Neurosci 32:1183-1196.
43. Zhao M, Choi YS, Obrietan K, Dudek SM. 2007. Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons. J Neurosci 27:12025-12032.
44. Zhao X, Lein ES, He A, Smith SC, Aston C, Gage FH. 2001. Transcriptional profiling reveals strict boundaries between hippocampal subregions. J Comp Neurol 441:187-196.
45. Ziai MR, Sangameswaran L, Hempstead JL, Danho W, Morgan JI. 1988. An immunochemical analysis of the distribution of a brain-specific polypeptide, PEP-19. J Neurochem 51:1771-1776.
46. Zimmer J, Haug FM. 1978. Laminar differentiation of the hippocampus, fascia dentata and subiculum in developing rats, observed with the Timm sulphide silver method. J Comp Neurol 179:581-617.