Hilar GABAergic interneuron activity controls spatial learning and memory retrieval

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Andrews Zwilling, Yaisa ^a,d   Gillespie, Anna K ^a,c   Kravitz, Alexxai V ^a   Nelson, Alexandra B ^a,d   Devidze, Nino ^a   Lo, Iris ^a   Yoon, Seo Yeon ^a   Bien Ly, Nga ^a,c   Ring, Karen ^a,c   Zwilling, Daniel ^a,d   Potter, Gregory B ^c   Rubenstein, John L R ^c   Kreitzer, Anatol C ^a,c,d   Huang, Yadong ^a,b,c,d  

^a GLADSTONE INSTITUTE OF NEUROLOGICAL DISEASE   (United States)

^b GLADSTONE INSTITUTE OF CARDIOVASCULAR DISEASE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CRE RECOMBINASE; HALORHODOPSIN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CONTROLLED STUDY; DENTATE GYRUS; EXPLORATORY BEHAVIOR; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IN VITRO STUDY; IN VIVO STUDY; LEARNING; MEMORY CONSOLIDATION; MOTOR COORDINATION; MOUSE; NONHUMAN; OPEN READING FRAME; OPTOGENETIC INHIBITION; PROTEINASE INHIBITION; PYRAMIDAL NERVE CELL; SHORT TERM MEMORY; SPATIAL LEARNING; SPATIAL MEMORY; SPATIAL MEMORY RETRIEVAL; TASK PERFORMANCE; VIRUS EXPRESSION; WORKING MEMORY;

ANIMALS; DENTATE GYRUS; DEPENDOVIRUS; GABAERGIC NEURONS; GENES, REPORTER; GENETIC VECTORS; INTERNEURONS; LEARNING; MEMORY; MEMORY, SHORT-TERM; MICE; MICE, TRANSGENIC; PSYCHOMOTOR PERFORMANCE;

ADENO-ASSOCIATED VIRUS; MUS;

EID: 84863611022     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0040555     Document Type: Article

References (49)

1. Squire LR, Wixted JT, (2011) The cognitive neuroscience of human memory since H.M. Annu Rev Neurosci 34: 259-288.
2. Wang SH, Morris RGM, (2010) Hippocampal-neocortical interactions in memory formation, consolidation, and reconsolidation. Annu Rev Psychol 61: 49-79.
3. Myers CE, Scharfman HE, (2009) A role for hilar cells in pattern separation in the dentate gyrus: a computational approach. Hippocampus 19: 321-337.
4. Kullmann D, (2011) Interneuron networks in the hippocampus. Curr Opin Neurobiol 21: 709-716.
5. Klausberger T, Somogyi P, (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321: 53-57.
6. Cui Y, Costa RM, Murphy GG, Elgersma Y, Zhu Y, et al. (2008) Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 135: 549-560.
7. Andrews-Zwilling Y, Bien-Ly N, Xu Q, Li G, Bernardo A, et al. (2010) Apolipoprotein E4 causes age- and Tau-dependent impairment of GABAergic interneurons, leading to learning and memory deficits in mice. J Neurosci 30: 13707-13717.
8. Palop JJ, Mucke L, (2010) Amyloid-β-induced neuronal dysfunction in Alzheimer's disease: from synapses toward neural networks. Nat Neurosci 13: 812-818.
9. Uhlhaas PJ, Singer W, (2010) Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11: 100-113.
10. Bast T, (2011) The hippocampal learning-behavior translation and the functional significance of hippocampal dysfunction in schizophrenia. Curr Opin Neurobiol 21: 492-501.
11. Potter GB, Petryniak MA, Shevchenko E, McKinsey GL, Ekker M, et al. (2009) Generation of Cre-transgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol Cell Neurosci 40: 167-186.
12. Cobos I, Long JE, Thwin MT, Rubenstein JL, (2006) Cellular patterns of transcription factor expression in developing cortical interneurons. Cereb Cortex pp. i82-i88.
13. Fenno L, Yizhar O, Deisseroth K, (2011) The development and application of optogenetics. Annu Rev Neurosci 34: 389-412.
14. Roberson ED, Scearce-Levie K, Palop JJ, Yan F, Cheng IH, et al. (2007) Reducing endogenous tau ameliorates amyloid ®-induced deficits in an Alzheimer's disease mouse model. Science 316: 750-754.
15. Kravitz AV, Freeze BS, Parker PRL, Kay K, Thwin MT, et al. (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466: 622-626.
16. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, et al. (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446: 633-639.
17. Henze DA, Wittner L, Buzsáki G, (2002) Single granule cells reliably discharge targets in the hippocampal CA3 network in vivo. Nat Neurosci 5: 790-795.
18. Sachidhanandam S, Blanchet C, Jeantet Y, Cho YH, Mulle C, (2009) Kainate receptors act as conditional amplifiers of spike transmission at hippocampal mossy fiber synapses. J Neurosci 29: 5000-5008.
19. Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, et al. (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471: 358-362.
20. Jasinska M, Siucinska E, Cybulska-Klosowicz A, Pyza E, Furness DN, et al. (2010) Rapid, learning-induced inhibitory synaptogenesis in murine barrel field. J Neurosci 30: 1176-1184.
21. Brosh I, Barkai E, (2009) Learning-induced enhancement of feedback inhibitory synaptic transmission. Learn Mem 16: 413-416.
22. Nitz D, McNaughton B, (2004) Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. Amer Physiol Soc 91: 863-872.
23. Ruediger S, Vittori C, Bednarek E, Genoud C, Strata P, et al. (2011) Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 473: 514-518.
24. Hu JH, Ma YH, Jiang J, Yang N, Duan SH, et al. (2004) Cognitive impairment in mice over-expressing gamma-aminobutyric acid transporter 1 (GAT1). Neuroreport 15: 9-12.
25. Murray AJ, Sauer JF, Riedel G, McClure C, Ansel L, et al. (2011) Parvalbumin-positive CA1 interneurons are required for spatial working but not reference memory. Nat Neurosci 14: 297-299.
26. Winocur G, (1985) The hippocampus and thalamus: their roles in short- and long-term memory and the effects of interference. Behav Brain Res 16: 135-152.
27. Kim JJ, Fanselow MS, (1992) Modality-specific retrograde amnesia of fear. Science 256: 675-677.
28. Squire LR, Alvarez P, (1995) Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr Opin Neurobiol 5: 169-177.
29. Bontempi B, Laurent-Demir C, Destrade C, Jaffard R, (1999) Time-dependent reorganization of brain circuitry underlying long-term memory storage. Nature 400: 671-675.
30. Dudai Y, (2004) The neurobiology of consolidations, or, how stable is the engram? Annu Rev Psychol 55: 51-86.
31. Winocur G, Frankland PW, Sekeres M, Fogel S, Moscovitch M, (2009) Changes in context-specificity during memory reconsolidation: selective effects of hippocampal lesions. Learn Mem 16: 722-729.
32. Squire LR, Bayley PJ, (2007) The neuroscience of remote memory. Curr Opin Neurobiol 17: 185-196.
33. Nadel L, Moscovitch M, (1997) Memory consolidation, retrograde amnesia and the hippocampal complex. Curr Opin Neurobiol 7: 217-227.
34. Noulhiane M, Piolino P, Hasboun D, Clemenceau S, Baulac M, et al. (2007) Autobiographical memory after temporal lobe resection: neuropsychological and MRI volumetric findings. Brain 130: 3184-3199.
35. Cipolotti L, Bird CM, (2006) Amnesia and the hippocampus. Curr Opin Neurobiol 19: 593-598.
36. Moscovitch M, Nadel L, Winocur G, Gilboa A, Rosenbaum RS, (2006) The cognitive neuroscience of remote episodic, semantic and spatial memory. Curr Opin Neurobiol 16: 179-190.
37. Winocur G, Moscovitch M, Bontempi B, (2010) Memory formation and long-term retention in humans and animals: convergence towards a transformation account of hippocampal-neocortical interactions. Neuropsychologia 48: 2339-2356.
38. Goshen I, Brodsky M, Prakash R, Wallace J, Gradinaru V, et al. (2011) Dynamics of retrieval strategies for remote memories. Cell 147: 678-689.
39. Lopez J, Herbeaux K, Cosquer B, Engeln M, Muller C, et al. (2011) Context-dependent modulation of hippocampal and cortical recruitment during remote spatial memory retrieval. Hippocampus 22: 827-841.
40. Davies P, Katzman R, Terry RD, (1980) Reduced somatostatin-like immunoreactivity in cerebral cortex from cases of Alzheimer disease and Alzheimer senile dementia. Nature 288: 279-280.
41. Bareggi SR, Franceschi M, Bonini L, Zecca L, Smirne S, (1982) Decreased CSF concentrations of homovanillic acid and γ-aminobutyric acid in Alzheimer's disease. Age- or disease-related modifications? Arch Neurol 39: 709-712.
42. Zimmer R, Teelken AW, Trieling WB, Weber W, Weihmayr T, et al. (1984) γ-Aminobutyric acid and homovanillic acid concentration in the CSF of patients with senile dementia of Alzheimer's type. Arch Neurol 41: 602-604.
43. Hardy J, Cowburn R, Barton A, Reynolds G, Dodd P, et al. (1987) A disorder of cortical GABAergic innervation in Alzheimer's disease. Neurosci Lett 73: 192-196.
44. Seidl R, Cairns N, Singewald N, Kaehler ST, Lubec G, (2001) Differences between GABA levels in Alzheimer's disase and Down syndrome with Alzheimer-like neuropathology. Naunyn Schmiedeberg Arch Pharmacol 363: 139-145.
45. Grouselle D, Winsky-Sommerer R, David JP, Delacourte A, Dournaud P, et al. (1998) Loss of somatostatin-like immunoreactivity in the frontal cortex of Alzheimer patients carrying the apolipoprotein epsilon 4 allele. Neurosci Lett 255: 21-24.
46. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, et al. (2007) Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55: 697-711.
47. Roberson ED, Halabisky B, Yoo JW, Yao J, Chin J, et al. (2011) Amyloid-β/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. J Neurosci 31: 700-711.
48. Corder EH, Saunders AM, Strittmatter WJ, Schmechel DE, Gaskell PC, et al. (1993) Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer's disease in late onset families. Science 261: 921-923.
49. Huang Y, (2010) Aβ-independent roles of apolipoprotein E4 in the pathogenesis of Alzheimer's disease. Trends Mol Med 16: 287-294.