Brain-derived neurotrophic factor differentially modulates excitability of two classes of hippocampal output neurons

Journal of Neurophysiology

Volumn 116, Issue 2, 2016, Pages 466-471

  Graves, A R ^a,b   Moore, S J ^a,c   Spruston, N ^a,b   Tryba, A K ^d,e   Kaczorowski, C C ^d,f  

^a NORTHWESTERN UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

^d MEDICAL COLLEGE OF WISCONSIN   (United States)

^e UNIVERSITY OF CHICAGO   (United States)

^f UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Burst firing; Hippocampus; Intrinsic plasticity; Long term potentiation; Metabotropic glutamate receptors

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; AMINO ACID RECEPTOR BLOCKING AGENT;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION; ANIMAL; CLASSIFICATION; CYTOLOGY; DRUG EFFECTS; EXCITATORY POSTSYNAPTIC POTENTIAL; NERVE CELL; PATCH CLAMP TECHNIQUE;

ACTION POTENTIALS; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; MALE; MICE; NEURONS; PATCH-CLAMP TECHNIQUES;

EID: 84984618857     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00186.2016     Document Type: Article

References (35)

1. Aicardi G, Argilli E, Cappello S, Santi S, Riccio M, Thoenen H, Canossa M. Induction of long-term potentiation and depression is reflected by corresponding changes in secretion of endogenous brain-derived neurotrophic factor. Proc Natl Acad Sci USA 101: 15788-15792, 2004.
2. Behr J, Wozny C, Fidzinski P, Schmitz D. Synaptic plasticity in the subiculum. Prog Neurobiol 89: 334-342, 2009.
3. Bindu B, Rekha J, Kutty BM. Post insult enriched housing improves the 8-arm radial maze performance but not the Morris water maze task in ventral subicular lesioned rats. Brain Res 1063: 121-131, 2005.
4. Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39, 1993.
5. Cunha C, Brambilla R, Thomas KL. A simple role for BDNF in learning and memory? Front Mol Neurosci 3: 1, 2010.
6. Figurov A, Pozzo-Miller LD, Olafsson P, Wang T, Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 381: 706-709, 1996.
7. Graves AR, Moore SJ, Bloss EB, Mensh BD, Kath WL, Spruston N. Hippocampal pyramidal neurons comprise two distinct cell types that are countermodulated by metabotropic receptors. Neuron 76: 776-789, 2012.
8. Griffin EW, Bechara RG, Birch AM, Kelly AM. Exercise enhances hippocampal-dependent learning in the rat: evidence for a BDNF-related mechanism. Hippocampus 19: 973-980, 2009.
9. Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24: 677-736, 2001.
10. Huang EJ, Reichardt LF. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 72: 609-642, 2003.
11. Jarsky T, Mady R, Kennedy B, Spruston N. Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus. J Comp Neurol 506: 535-547, 2008.
12. Kang H, Schuman EM. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267: 1658-1662, 1995.
13. Kang H, Welcher AA, Shelton D, Schuman EM. Neurotrophins and time: different roles for TrkB signaling in hippocampal long-term potentiation. Neuron 19: 653-664, 1997.
14. Kim Y, Spruston N. Target-specific output patterns are predicted by the distribution of regular-spiking and bursting pyramidal neurons in the subiculum. Hippocampus 22: 693-706, 2012.
15. Knierim JJ, Neunuebel JP, Deshmukh SS. Functional correlates of the lateral and medial entorhinal cortex: objects, path integration and localglobal reference frames. Philos Trans R Soc Lond B Biol Sci 369: 20130369, 2014.
16. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T. Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor. Proc Natl Acad Sci USA 92: 8856-8860, 1995.
17. Levine ES, Dreyfus CF, Black IB, Plummer MR. Brain-derived neurotrophic factor rapidly enhances synaptic transmission in hippocampal neurons via postsynaptic tyrosine kinase receptors. Proc Natl Acad Sci USA 92: 8074-8077, 1995.
18. Lisman JE. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20: 38-43, 1997.
19. Lu VB, Ballanyi K, Colmers WF, Smith PA. Neuron type-specific effects of brain-derived neurotrophic factor in rat superficial dorsal horn and their relevance to "central sensitization." J Physiol 584: 543-563, 2007.
20. Lu Y, Christian K, Lu B. BDNF: a key regulator for protein synthesisdependent LTP and long-term memory? Neurobiol Learn Mem 89: 312-323, 2008.
21. Menendez de la Prida L, Gal B. Synaptic contributions to focal and widespread spatiotemporal dynamics in the isolated rat subiculum in vitro. J Neurosci 24: 5525-5536, 2004.
22. Menendez de la Prida L, Suarez F, Pozo MA. Electrophysiological and morphological diversity of neurons from the rat subicular complex in vitro. Hippocampus 13: 728-744, 2003.
23. Moore SJ, Cooper DC, Spruston N. Plasticity of burst firing induced by synergistic activation of metabotropic glutamate and acetylcholine receptors. Neuron 61: 287-300, 2009.
24. Neuner SM, Wilmott LA, Hope KA, Hoffmann B, Chong JA, Abramowitz J, Birnbaumer L, O’Connell KM, Tryba AK, Greene AS, Savio Chan C, Kaczorowski CC. TRPC3 channels critically regulate hippocampal excitability and contextual fear memory. Behav Brain Res 281: 69-77, 2015.
25. Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, Kandel ER. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16: 1137-1145, 1996.
26. Patterson SL, Grover LM, Schwartzkroin PA, Bothwell M. Neurotrophin expression in rat hippocampal slices: a stimulus paradigm inducing LTP in CA1 evokes increases in BDNF and NT-3 mRNAs. Neuron 9: 1081-1088, 1992.
27. Pike FG, Meredith RM, Olding AW, Paulsen O. Rapid report: postsynaptic bursting is essential for "Hebbian" induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J Physiol 518: 571-576, 1999.
28. Rex CS, Lin CY, Kramar EA, Chen LY, Gall CM, Lynch G. Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J Neurosci 27: 3017-3029, 2007.
29. Sakata K, Martinowich K, Woo NH, Schloesser RJ, Jimenez DV, Ji Y, Shen L, Lu B. Role of activity-dependent BDNF expression in hippocampal-prefrontal cortical regulation of behavioral perseverance. Proc Natl Acad Sci USA 110: 15103-15108, 2013.
30. Sanchez MM, Das D, Taylor JL, Noda A, Yesavage JA, Salehi A. BDNF polymorphism predicts the rate of decline in skilled task performance and hippocampal volume in healthy individuals. Transl Psychiatry 1: e51, 2011.
31. Segal RA. Selectivity in neurotrophin signaling: theme and variations. Annu Rev Neurosci 26: 299-330, 2003.
32. Segal RA, Greenberg ME. Intracellular signaling pathways activated by neurotrophic factors. Annu Rev Neurosci 19: 463-489, 1996.
33. Stewart M, Wong RK. Intrinsic properties and evoked responses of guinea pig subicular neurons in vitro. J Neurophysiol 70: 232-245, 1993.
34. Tapia-Arancibia L, Aliaga E, Silhol M, Arancibia S. New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res Rev 59: 201-220, 2008.
35. Wozny C, Maier N, Schmitz D, Behr J. Two different forms of long-term potentiation at CA1-subiculum synapses. J Physiol 586: 2725-2734, 2008.