Determinants of different deep and superficial CA1 pyramidal cell dynamics during sharp-wave ripples

Nature Neuroscience

Volumn 18, Issue 9, 2015, Pages 1281-1290

  Valero, Manuel ^a   Cid, Elena ^a   Averkin, Robert G ^b   Aguilar, Juan ^c   Sanchez Aguilera, Alberto ^a,d   Viney, Tim J ^e   Gomez Dominguez, Daniel ^a   Bellistri, Elisa ^a   De La Prida, Liset Menendez ^a  

^a INSTITUTO CAJAL   (Spain)

^b UNIVERSITY OF SZEGED   (Hungary)

^c HOSPITAL NACIONAL DE PARAPLÉJICOS   (Spain)

^d SCHOOL OF MEDICINE   (Spain)

^e UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALBINDIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CURRENT CLAMP TECHNIQUE; DORSAL HIPPOCAMPUS; ELECTRICAL POTENTIAL PARAMETERS; ELECTROSTIMULATION; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPAL CA1 REGION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VITRO STUDY; MALE; MEMBRANE POTENTIAL; MEMBRANE STEADY POTENTIAL; NONHUMAN; PATCH CLAMP TECHNIQUE; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SHARP WAVE RIPPLE; STRATUM LACUNOSUM MOLECULARE; STRATUM PYRAMIDALE; STRATUM RADIATUM; ACTION POTENTIAL; ANIMAL; CYTOLOGY; NERVE CELL NETWORK; PHYSIOLOGY; PROCEDURES; WISTAR RAT;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; ELECTRIC STIMULATION; FEMALE; MALE; NERVE NET; PYRAMIDAL CELLS; RATS; RATS, WISTAR;

EID: 84940459507     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4074     Document Type: Article

References (64)

1. Buzsáki, G., Leung, L. W. S. & Vanderwolf, C. H. Cellular bases of hippocampal EEG in the behaving rat. Brain Res. 287, 139-171 (1983).
2. Skaggs, W. E. et al. EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. J. Neurophysiol. 98, 898-910 (2007).
3. Kamondi, A., Acsády, L. & Buzsáki, G. Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. J. Neurosci. 18, 3919-3928 (1998).
4. Csicsvari, J., Hirase, H., Mamiya, A. & Buzsáki, G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28, 585-594 (2000).
5. Ylinen, A. et al. Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30-46 (1995).
6. Klausberger, T. et al. Brain state-and cell type-specific firing of hippocampal interneurons in vivo. Nature 421, 844-848 (2003).
7. Klausberger, T. et al. Complementary roles of cholecystokinin-and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J. Neurosci. 25, 9782-9793 (2005).
8. Maier, N. et al. Coherent phasic excitation during hippocampal ripples. Neuron 72, 137-152 (2011).
9. English, D. F. et al. Excitation and inhibition compete to control spiking during hippocampal ripples: intracellular study in behaving mice. J. Neurosci. 34, 16509-16517 (2014).
10. Slomianka, L., Amrein, I., Knuesel, I., Sørensen, J. C. & Wolfer, D. P. Hippocampal pyramidal cells: the reemergence of cortical lamination. Brain Struct. Funct. 216, 301-317 (2011).
11. Dong, H.-W., Swanson, L. W., Chen, L., Fanselow, M. S. & Toga, A. W. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. USA 106, 11794-11799 (2009).
12. Baimbridge, K. G., Peet, M. J., McLennan, H. & Church, J. Bursting response to current-evoked depolarization in rat CA1 pyramidal neurons is correlated with lucifer yellow dye coupling but not with the presence of calbindin-D28k. Synapse 7, 269-277 (1991).
13. Bannister, N. J. & Larkman, A. U. Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus. I. Branching patterns. J. Comp. Neurol. 360, 150-160 (1995).
14. Nielsen, J. V., Blom, J. B., Noraberg, J. & Jensen, N. A. Zbtb20-Induced CA1 pyramidal neuron development and area enlargement in the cerebral midline cortex of mice. Cereb. Cortex 20, 1904-1914 (2010).
15. Kohara, K. et al. Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nat. Neurosci. 17, 269-279 (2014).
16. Lee, S. H. et al. Parvalbumin-positive basket cells differentiate among hippocampal pyramidal cells. Neuron 82, 1129-1144 (2014).
17. Mizuseki, K., Diba, K., Pastalkova, E. & Buzsáki, G. Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nat. Neurosci. 14, 1174-1181 (2011).
18. Senior, T. J., Huxter, J. R., Allen, K., O'Neill, J. & Csicsvari, J. Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. J. Neurosci. 28, 2274-2286 (2008).
19. Stark, E. et al. Pyramidal cell-interneuron interactions underlie hippocampal ripple oscillations. Neuron 83, 467-480 (2014).
20. O'Neill, J., Senior, T. & Csicsvari, J. Place-selective firing of CA1 pyramidal cells during sharp wave/ripple network patterns in exploratory behavior. Neuron 49, 143-155 (2006).
21. Fritschy, J. M., Harvey, R. J. & Schwarz, G. Gephyrin: where do we stand, where do we go? Trends Neurosci. 31, 257-264 (2008).
22. Freund, T. F. & Buzsáki, G. Interneurons of the hippocampus. Hippocampus 6, 347-470 (1996).
23. Katona, I. et al. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J. Neurosci. 19, 4544-4558 (1999).
24. Takács, V. T., Szonyi, A., Freund, T. F., Nyiri, G. & Gulyás, A. I. Quantitative ultrastructural analysis of basket and axo-axonic cell terminals in the mouse hippocampus. Brain Struct. Funct. 220, 919-940 (2015).
25. Glickfeld, L. L., Atallah, B. V. & Scanziani, M. Complementary modulation of somatic inhibition by opioids and cannabinoids. J. Neurosci. 28, 1824-1832 (2008).
26. Bartos, M. & Elgueta, C. Functional characteristics of parvalbumin-and cholecystokinin-expressing basket cells. J. Physiol. (Lond.) 590, 669-681 (2012).
27. Chevaleyre, V. & Siegelbaum, S. A. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 66, 560-572 (2010).
28. Tukker, J. J., Fuentealba, P., Hartwich, K., Somogyi, P. & Klausberger, T. Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo. J. Neurosci. 27, 8184-8189 (2007).
29. Korshunov, V. A. Miniature microdrive for extracellular recording of neuronal activity in freely moving animals. J. Neurosci. Methods 57, 77-80 (1995).
30. Lapray, D. et al. Behavior-dependent specialization of identified hippocampal interneurons. Nat. Neurosci. 15, 1265-1271 (2012).
31. Roumis, D. K. & Frank, L. M. Hippocampal sharp-wave ripples in waking and sleeping states. Curr. Opin. Neurobiol. 35, 6-12 (2015).
32. Varga, C., Golshani, P. & Soltesz, I. PNAS Plus: Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice. Proc. Natl. Acad. Sci. USA 109, E2726-E2734 (2012).
33. Katona, L. et al. Sleep and movement differentiates actions of two types of somatostatin-expressing gabaergic interneuron in rat hippocampus. Neuron 82, 872-886 (2014).
34. Ellender, T. J., Nissen, W., Colgin, L. L., Mann, E. O. & Paulsen, O. Priming of hippocampal population bursts by individual perisomatic-targeting interneurons. J. Neurosci. 30, 5979-5991 (2010).
35. Bähner, F. et al. Cellular correlate of assembly formation in oscillating hippocampal networks in vitro. Proc. Natl. Acad. Sci. USA 108, E607-E616 (2011).
36. Aivar, P., Valero, M., Bellistri, E. & Menendez de la Prida, L. Extracellular calcium controls the expression of two different forms of ripple-like hippocampal oscillations. J. Neurosci. 34, 2989-3004 (2014).
37. Lee, D., Lin, B.-J. & Lee, A. K. Hippocampal place fields emerge upon single-cell manipulation of excitability during behavior. Science 337, 849-853 (2012).
38. Bland, B. H., Konopacki, J. & Dyck, R. Heterogeneity among hippocampal pyramidal neurons revealed by their relation to theta-band oscillation and synchrony. Exp. Neurol. 195, 458-474 (2005).
39. Bodor, A. L. et al. Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J. Neurosci. 25, 6845-6856 (2005).
40. Glickfeld, L. L. & Scanziani, M. Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat. Neurosci. 9, 807-815 (2006).
41. Lenkey, N. et al. Tonic endocannabinoid-mediated modulation of GABA release is independent of the CB1 content of axon terminals. Nat. Commun. 6, 6557 (2015).
42. Cea-del Rio, C. A. et al. M3 muscarinic acetylcholine receptor expression confers differential cholinergic modulation to neurochemically distinct hippocampal basket cell subtypes. J. Neurosci. 30, 6011-6024 (2010).
43. Dupret, D., O'Neill, J., Pleydell-Bouverie, B. & Csicsvari, J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 13, 995-1002 (2010).
44. Mercer, A., Trigg, H. L. & Thomson, A. M. Characterization of neurons in the CA2 subfield of the adult rat hippocampus. J. Neurosci. 27, 7329-7338 (2007).
45. Viney, T. J. et al. Network state-dependent inhibition of identified hippocampal CA3 axo-axonic cells in vivo. Nat. Neurosci. 16, 1802-1811 (2013).
46. Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53-57 (2008).
47. Worrell, G. A. et al. High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings. Brain 131, 928-937 (2008).
48. Jefferys, J. G. R. et al. Mechanisms of physiological and epileptic HFO generation. Prog. Neurobiol. 98, 250-264 (2012).
49. Alvarado-Rojas, C. et al. Different mechanisms of ripple-like oscillations in the human epileptic subiculum. Ann. Neurol. 77, 281-290 (2015).
50. Morris, M. E., Baimbridge, K. G., El-Beheiry, H., Obrocea, G. V. & Rosen, A. S. Correlation of anoxic neuronal responses and calbindin-D(28k) localization in stratum pyramidale of rat hippocampus. Hippocampus 5, 25-39 (1995).
51. Pinault, D. A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin. J. Neurosci. Methods 65, 113-136 (1996).
52. Sloviter, R. S. 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 (1989).
53. Airaksinen, M. S. et al. Ataxia and altered dendritic calcium signaling in mice carrying a targeted null mutation of the calbindin D28k gene. Proc. Natl. Acad. Sci. USA 94, 1488-1493 (1997).
54. Celio, M. R. et al. Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k. Cell Calcium 11, 599-602 (1990).
55. San Antonio, A., Liban, K., Ikrar, T., Tsyganovskiy, E. & Xu, X. Distinct physiological and developmental properties of hippocampal CA2 subfield revealed by using anti-Purkinje cell protein 4 (PCP4) immunostaining. J. Comp. Neurol. 522, 1333-1354 (2014).
56. Pfeiffer, F., Simler, R., Grenningloh, G. & Betz, H. Monoclonal antibodies and peptide mapping reveal structural similarities between the subunits of the glycine receptor of rat spinal cord. Proc. Natl. Acad. Sci. USA 81, 7224-7227 (1984).
57. Feng, G. et al. Dual requirement for gephyrin in glycine receptor clustering and molybdoenzyme activity. Science 282, 1321-1324 (1998).
58. Schwaller, B. et al. Prolonged contraction-relaxation cycle of fast-twitch muscles in parvalbumin knockout mice. Am. J. Physiol. 276, C395-C403 (1999).
59. Fukudome, Y. et al. Two distinct classes of muscarinic action on hippocampal inhibitory synapses: M2-mediated direct suppression and M1/M3-mediated indirect suppression through endocannabinoid signalling. Eur. J. Neurosci. 19, 2682-2692 (2004).
60. Takeda, K. et al. WFS1 (Wolfram syndrome 1) gene product: predominant subcellular localization to endoplasmic reticulum in cultured cells and neuronal expression in rat brain. Hum. Mol. Genet. 10, 477-484 (2001).
61. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates, 5th edn. (Elsevier, London, 2005).
62. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675 (2012).
63. van Betteray, J. N., Vossen, J. M. & Coenen, A. M. Behavioural characteristics of sleep in rats under different light/dark conditions. Physiol. Behav. 50, 79-82 (1991).
64. Pérez-Escudero, A., Vicente-Page, J., Hinz, R. C., Arganda, S. & de Polavieja, G. G. idTracker: tracking individuals in a group by automatic identification of unmarked animals. Nat. Methods 11, 743-748 (2014).