Age-Dependent Specific Changes in Area CA2 of the Hippocampus and Social Memory Deficit in a Mouse Model of the 22q11.2 Deletion Syndrome

Neuron

Volumn 89, Issue 1, 2016, Pages 163-176

  Piskorowski, Rebecca A ^a   Nasrallah, Kaoutsar ^a   Diamantopoulou, Anastasia ^b   Mukai, Jun ^b   Hassan, Sami I ^b   Siegelbaum, Steven A ^b   Gogos, Joseph A ^b   Chevaleyre, Vivien ^a  

^a CNRS   (France)

^b Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PARVALBUMIN;

ACTION POTENTIAL; AGE; AMNESIA; ANIMAL MODEL; ARTICLE; CHROMOSOME DELETION 22Q11; COGNITIVE DEFECT; CONTROLLED STUDY; GENE DELETION; GENETIC RISK; GENOTYPE; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; INTERNEURON; LONG TERM DEPRESSION; MEMORY DISORDER; MENTAL DISEASE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; POSITIVE FEEDBACK; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RISK FACTOR; SCHIZOPHRENIA; SOCIAL DISABILITY; SOCIAL LEARNING; STRATUM ORIENS; STRATUM PYRAMIDALE; AGING; ANIMAL; DIGEORGE SYNDROME; DISEASE MODEL; GENETICS; HIPPOCAMPUS; MALE; MEMORY; NERVE CELL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SOCIAL BEHAVIOR; TRANSGENIC MOUSE;

ACTION POTENTIALS; AGING; ANIMALS; COGNITION DISORDERS; DIGEORGE SYNDROME; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; MALE; MEMORY; MICE, TRANSGENIC; NEURONS; PARVALBUMINS; SCHIZOPHRENIA; SOCIAL BEHAVIOR;

EID: 84953735154     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.11.036     Document Type: Article

References (56)

1. Andrioli A., Alonso-Nanclares L., Arellano J.I., DeFelipe J. Quantitative analysis of parvalbumin-immunoreactive cells in the human epileptic hippocampus. Neuroscience 2007, 149:131-143.
2. Basu J., Srinivas K.V., Cheung S.K., Taniguchi H., Huang Z.J., Siegelbaum S.A. A cortico-hippocampal learning rule shapes inhibitory microcircuit activity to enhance hippocampal information flow. Neuron 2013, 79:1208-1221.
3. Benes F.M., Kwok E.W., Vincent S.L., Todtenkopf M.S. A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol. Psychiatry 1998, 44:88-97.
4. Berretta S., Gisabella B., Benes F.M. A rodent model of schizophrenia derived from postmortem studies. Behav. Brain Res. 2009, 204:363-368.
5. Botcher N.A., Falck J.E., Thomson A.M., Mercer A. Distribution of interneurons in the CA2 region of the rat hippocampus. Front. Neuroanat. 2014, 8:104.
6. Brady D.R., Mufson E.J. Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer's diseased brain. Neuroscience 1997, 80:1113-1125.
7. Brüne M. Emotion recognition, 'theory of mind,' and social behavior in schizophrenia. Psychiatry Res. 2005, 133:135-147.
8. Campbell L.E., McCabe K.L., Melville J.L., Strutt P.A., Schall U. Social cognition dysfunction in adolescents with 22q11.2 deletion syndrome (velo-cardio-facial syndrome): relationship with executive functioning and social competence/functioning. J. Intellect. Disabil. Res. 2015, 59:845-859.
9. Chevaleyre V., Siegelbaum S.A. Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron 2010, 66:560-572.
10. Churchyard A., Lees A.J. The relationship between dementia and direct involvement of the hippocampus and amygdala in Parkinson's disease. Neurology 1997, 49:1570-1576.
11. Cohen-Gadol A.A., Pan J.W., Kim J.H., Spencer D.D., Hetherington H.H. Mesial temporal lobe epilepsy: a proton magnetic resonance spectroscopy study and a histopathological analysis. J. Neurosurg. 2004, 101:613-620.
12. Cui Z., Gerfen C.R., Young W.S. Hypothalamic and other connections with dorsal CA2 area of the mouse hippocampus. J. Comp. Neurol. 2013, 521:1844-1866.
13. Donato F., Rompani S.B., Caroni P. Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 2013, 504:272-276.
14. Drew L.J., Stark K.L., Fénelon K., Karayiorgou M., Macdermott A.B., Gogos J.A. Evidence for altered hippocampal function in a mouse model of the human 22q11.2 microdeletion. Mol. Cell. Neurosci. 2011, 47:293-305.
15. Earls L.R., Bayazitov I.T., Fricke R.G., Berry R.B., Illingworth E., Mittleman G., Zakharenko S.S. Dysregulation of presynaptic calcium and synaptic plasticity in a mouse model of 22q11 deletion syndrome. J. Neurosci. 2010, 30:15843-15855.
16. Foussias G., Agid O., Fervaha G., Remington G. Negative symptoms of schizophrenia: clinical features, relevance to real world functioning and specificity versus other CNS disorders. Eur. Neuropsychopharmacol. 2014, 24:693-709.
17. Fuchs E.C., Zivkovic A.R., Cunningham M.O., Middleton S., Lebeau F.E.N., Bannerman D.M., Rozov A., Whittington M.A., Traub R.D., Rawlins J.N.P., Monyer H. Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 2007, 53:591-604.
18. Hitti F.L., Siegelbaum S.A. The hippocampal CA2 region is essential for social memory. Nature 2014, 508:88-92.
19. Honoré E. The neuronal background K2P channels: focus on TREK1. Nat. Rev. Neurosci. 2007, 8:251-261.
20. Rare chromosomal deletions and duplications increase risk of schizophrenia. Nature 2008, 455:237-241. International Schizophrenia Consortium.
21. Jones M.W., McHugh T.J. Updating hippocampal representations: CA2 joins the circuit. Trends Neurosci. 2011, 34:526-535.
22. Kalaitzakis M.E., Christian L.M., Moran L.B., Graeber M.B., Pearce R.K.B., Gentleman S.M. Dementia and visual hallucinations associated with limbic pathology in Parkinson's disease. Parkinsonism Relat. Disord. 2009, 15:196-204.
23. Karayiorgou M., Morris M.A., Morrow B., Shprintzen R.J., Goldberg R., Borrow J., Gos A., Nestadt G., Wolyniec P.S., Lasseter V.K., et al. Schizophrenia susceptibility associated with interstitial deletions of chromosome 22q11. Proc. Natl. Acad. Sci. USA 1995, 92:7612-7616.
24. Karayiorgou M., Simon T.J., Gogos J.A. 22q11.2 microdeletions: linking DNA structural variation to brain dysfunction and schizophrenia. Nat. Rev. Neurosci. 2010, 11:402-416.
25. Kennard L.E., Chumbley J.R., Ranatunga K.M., Armstrong S.J., Veale E.L., Mathie A. Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine. Br. J. Pharmacol. 2005, 144:821-829.
26. Knable M.B., Barci B.M., Webster M.J., Meador-Woodruff J., Torrey E.F. Molecular abnormalities of the hippocampus in severe psychiatric illness: postmortem findings from the Stanley Neuropathology Consortium. Mol. Psychiatry 2004, 9:609-620. Stanley Neuropathology Consortium, 544.
27. Kohara K., Pignatelli M., Rivest A.J., Jung H.-Y., Kitamura T., Suh J., Frank D., Kajikawa K., Mise N., Obata Y., et al. Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nat. Neurosci. 2014, 17:269-279.
28. Korotkova T., Fuchs E.C., Ponomarenko A., von Engelhardt J., Monyer H. NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 2010, 68:557-569.
29. Lee S.E., Simons S.B., Heldt S.A., Zhao M., Schroeder J.P., Vellano C.P., Cowan D.P., Ramineni S., Yates C.K., Feng Y., et al. RGS14 is a natural suppressor of both synaptic plasticity in CA2 neurons and hippocampal-based learning and memory. Proc. Natl. Acad. Sci. USA 2010, 107:16994-16998.
30. Lee H., Wang C., Deshmukh S.S., Knierim J.J. Neural population evidence of functional heterogeneity along the CA3 transverse axis: pattern completion versus pattern separation. Neuron 2015, 87:1093-1105.
31. Lu L., Igarashi K.M., Witter M.P., Moser E.I., Moser M.-B. Topography of place maps along the CA3-to-CA2 axis of the hippocampus. Neuron 2015, 87:1078-1092.
32. Mankin E.A., Diehl G.W., Sparks F.T., Leutgeb S., Leutgeb J.K. Hippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts. Neuron 2015, 85:190-201.
33. Millan M.J., Bales K.L. Towards improved animal models for evaluating social cognition and its disruption in schizophrenia: the CNTRICS initiative. Neurosci. Biobehav. Rev. 2013, 37(9 Pt B):2166-2180.
34. Narr K.L., Thompson P.M., Szeszko P., Robinson D., Jang S., Woods R.P., Kim S., Hayashi K.M., Asunction D., Toga A.W., Bilder R.M. Regional specificity of hippocampal volume reductions in first-episode schizophrenia. Neuroimage 2004, 21:1563-1575.
35. Nasrallah K., Piskorowski R.A., Chevaleyre V. Inhibitory plasticity permits the recruitment of CA2 pyramidal neurons by CA3(1,2,3). eNeuro 2015, 2. ENEURO.0049-15.2015.
36. O'Donnell P. Adolescent onset of cortical disinhibition in schizophrenia: insights from animal models. Schizophr. Bull. 2011, 37:484-492.
37. Olney J.W., deGubareff T., Sloviter R.S. "Epileptic" brain damage in rats induced by sustained electrical stimulation of the perforant path. II. Ultrastructural analysis of acute hippocampal pathology. Brain Res. Bull. 1983, 10:699-712.
38. Pagani J.H., Zhao M., Cui Z., Avram S.K., Caruana D.A., Dudek S.M., Young W.S. Role of the vasopressin 1b receptor in rodent aggressive behavior and synaptic plasticity in hippocampal area CA2. Mol. Psychiatry 2015, 20:490-499.
39. Penn D.L., Sanna L.J., Roberts D.L. Social cognition in schizophrenia: an overview. Schizophr. Bull. 2008, 34:408-411.
40. Pikkarainen M., Rönkkö S., Savander V., Insausti R., Pitkänen A. Projections from the lateral, basal, and accessory basal nuclei of the amygdala to the hippocampal formation in rat. J. Comp. Neurol. 1999, 403:229-260.
41. Piskorowski R.A., Chevaleyre V. Delta-opioid receptors mediate unique plasticity onto parvalbumin-expressing interneurons in area CA2 of the hippocampus. J. Neurosci. 2013, 33:14567-14578.
42. Pouille F., Scanziani M. Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 2001, 293:1159-1163.
43. Rowland D.C., Weible A.P., Wickersham I.R., Wu H., Mayford M., Witter M.P., Kentros C.G. Transgenically targeted rabies virus demonstrates a major monosynaptic projection from hippocampal area CA2 to medial entorhinal layer II neurons. J. Neurosci. 2013, 33:14889-14898.
44. Sigurdsson T., Stark K.L., Karayiorgou M., Gogos J.A., Gordon J.A. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 2010, 464:763-767.
45. Simons S.B., Caruana D.A., Zhao M., Dudek S.M. Caffeine-induced synaptic potentiation in hippocampal CA2 neurons. Nat. Neurosci. 2012, 15:23-25.
46. Small S.A., Schobel S.A., Buxton R.B., Witter M.P., Barnes C.A. A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat. Rev. Neurosci. 2011, 12:585-601.
47. Stark K.L., Xu B., Bagchi A., Lai W.-S., Liu H., Hsu R., Wan X., Pavlidis P., Mills A.A., Karayiorgou M., Gogos J.A. Altered brain microRNA biogenesis contributes to phenotypic deficits in a 22q11-deletion mouse model. Nat. Genet. 2008, 40:751-760.
48. Stevenson E.L., Caldwell H.K. The vasopressin 1b receptor and the neural regulation of social behavior. Horm. Behav. 2012, 61:277-282.
49. Stevenson E.L., Caldwell H.K. Lesions to the CA2 region of the hippocampus impair social memory in mice. Eur. J. Neurosci. 2014, 40:3294-3301.
50. Talley E.M., Solorzano G., Lei Q., Kim D., Bayliss D.A. Cns distribution of members of the two-pore-domain (KCNK) potassium channel family. J. Neurosci. 2001, 21:7491-7505.
51. Wintzer M.E., Boehringer R., Polygalov D., McHugh T.J. The hippocampal CA2 ensemble is sensitive to contextual change. J. Neurosci. 2014, 34:3056-3066.
52. Wittner L., Huberfeld G., Clémenceau S., Eross L., Dezamis E., Entz L., Ulbert I., Baulac M., Freund T.F., Maglóczky Z., Miles R. The epileptic human hippocampal cornu ammonis 2 region generates spontaneous interictal-like activity in vitro. Brain 2009, 132:3032-3046.
53. Xu B., Roos J.L., Levy S., van Rensburg E.J., Gogos J.A., Karayiorgou M. Strong association of de novo copy number mutations with sporadic schizophrenia. Nat. Genet. 2008, 40:880-885.
54. Young W.S., Li J., Wersinger S.R., Palkovits M. The vasopressin 1b receptor is prominent in the hippocampal area CA2 where it is unaffected by restraint stress or adrenalectomy. Neuroscience 2006, 143:1031-1039.
55. Zhang Z.J., Reynolds G.P. A selective decrease in the relative density of parvalbumin-immunoreactive neurons in the hippocampus in schizophrenia. Schizophr. Res. 2002, 55:1-10.
56. Zhao M., Choi Y.-S., Obrietan K., Dudek S.M. Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons. J. Neurosci. 2007, 27:12025-12032.