Learning increases intrinsic excitability of hippocampal interneurons

Journal of Neuroscience

Volumn 33, Issue 13, 2013, Pages 5499-5506

  Mckay, Bridget M ^a   Oh, M Matthew ^a   Disterhoft, John F ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; SOMATOSTATIN;

AFTERHYPERPOLARIZATION; ANIMAL BEHAVIOR; ANIMAL CELL; ARTICLE; CONDITIONING; CONTROLLED STUDY; ELECTROMYOGRAPHY; ELECTROPHYSIOLOGY; EYELID REFLEX; FLUORESCENCE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; INTERNEURON; LEARNING; MALE; MEMBRANE STEADY POTENTIAL; MODULATION; MOUSE; NERVE CELL NETWORK; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; CONDITIONING, EYELID; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA ANTAGONISTS; GREEN FLUORESCENT PROTEINS; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MALE; MICE; MICE, TRANSGENIC; MORPHOLINES; PYRIDAZINES; RATS; SODIUM CHANNEL BLOCKERS; SOMATOSTATIN; TETRODOTOXIN;

EID: 84875426315     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4068-12.2013     Document Type: Article

References (36)

1. Berger TW, Alger B, Thompson RF (1976) Neuronal substrate of classical conditioning in the hippocampus. Science 192:483-485.CrossRef Medline
2. Brosh I, Barkai E (2009) Learning-induced enhancement of feedback inhibitory synaptic transmission. Learn Mem 16:413-416.CrossRef Medline
3. Buzsáki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.CrossRef Medline
4. Christian KM, Thompson RF (2003) Neural substrates of eyeblink conditioning: acquisition and retention. Learn Mem 10:427-455.CrossRef Medline
5. Cui Y, Costa RM, Murphy GG, Elgersma Y, Zhu Y, Gutmann DH, Parada LF, Mody I, Silva AJ (2008) Neurofibromin regulation of ERK signaling modulates GABA release and learning. Cell 135:549-560.CrossRef Medline
6. Disterhoft JF, Oh MM (2006) Learning, aging and intrinsic neuronal plasticity. Trends Neurosci 29:587-599.CrossRef Medline
7. Disterhoft JF, Coulter DA, Alkon DL (1986) Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci U S A 83:2733-2737.CrossRef Medline
8. Farley SJ, McKay BM, Disterhoft JF, Weiss C (2011) Reevaluating hippocampus-dependent learning in FVB/N mice. Behav Neurosci 125: 871-878.CrossRef Medline
9. Freund TF, Buzsáki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.Medline
10. Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, Lebeau FE, Bannerman DM, Rozov A, Whittington MA, Traub RD, Rawlins JN, Monyer H (2007) Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53:591-604.CrossRef Medline
11. Han JH, Kushner SA, Yiu AP, Cole CJ, Matynia A, Brown RA, Neve RL, Guzowski JF, Silva AJ, Josselyn SA (2007) Neuronal competition and selection during memory formation. Science 316:457-460.CrossRef Medline
12. Han JH, Kushner SA, Yiu AP, Hsiang HL, Buch T, Waisman A, Bontempi B, Neve RL, Frankland PW, Josselyn SA (2009) Selective erasure of a fear memory. Science 323:1492-1496.CrossRef Medline
13. Kaczorowski CC, Sametsky E, Shah S, Vassar R, Disterhoft JF (2011) Mechanisms underlying basal and learning-related intrinsic excitability in a mouse model of Alzheimer's disease. Neurobiol Aging 32:1452-1465.CrossRef Medline
14. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53-57.CrossRef Medline
15. Knott GW, Quairiaux C, Genoud C, Welker E (2002) Formation of dendritic spines with GABAergic synapses induced by whisker stimulation in adult mice. Neuron 34:265-273.CrossRef Medline
16. Leão RN, Mikulovic S, Leão KE, Munguba H, Gezelius H, Enjin A, Patra K, Eriksson A, Loew LM, Tort AB, Kullander K (2012) OLM interneurons differentially modulate CA3 and entorhinal inputs to hippocampal CA1 neurons. Nat Neurosci 15:1524-1530.CrossRef Medline
17. Lopez de Armentia M, Jancic D, Olivares R, Alarcon JM, Kandel ER, Barco A (2007) cAMP response element-binding protein-mediated gene expression increases the intrinsic excitability of CA1 pyramidal neurons. J Neurosci 27:13909-13918.CrossRef Medline
18. Maccaferri G, McBain CJ (1996) The hyperpolarization-activated current (Ih) and its contribution to pacemaker activity in rat CA1 hippocampal stratum oriens-alveus interneurones. J Physiol 497:119-130.Medline
19. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.CrossRef Medline
20. Maviel T, Durkin TP, Menzaghi F, Bontempi B (2004) Sites of neocortical reorganization critical for remote spatial memory. Science 305:96-99.CrossRef Medline
21. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11-23.CrossRef Medline
22. McEchron MD, Disterhoft JF (1997) Sequence of single neuron changes in CA1 hippocampus of rabbits during acquisition of trace eyeblink conditioned responses. J Neurophysiol 78:1030-1044.Medline
23. McEchron MD, Disterhoft JF (1999) Hippocampal encoding of non-spatial trace conditioning. Hippocampus 9:385-396.CrossRef Medline
24. McKay BM, Oh MM, Galvez R, Burgdorf J, Kroes RA, Weiss C, Adelman JP, Moskal JR, Disterhoft JF (2012) Increasing SK2 channel activity impairs associative learning. J Neurophysiol 108:863-870.CrossRef Medline
25. Minneci F, Janahmadi M, Migliore M, Dragicevic N, Avossa D, Cherubini E (2007) Signaling properties of stratum oriens interneurons in the hippocampus of transgenic mice expressing EGFP in a subset of somatostatin-containing cells. Hippocampus 17:538-553.CrossRef Medline
26. Oh MM, Power JM, Thompson LT, Disterhoft JF (2000) Apamin increases excitability of CA1 hippocampal pyramidal neurons. Neurosci Res Comm 27:135-142.
27. Oh MM, McKay BM, Power JM, Disterhoft JF (2009) Learning-related postburst afterhyperpolarization reduction in CA1 pyramidal neurons is mediated by protein kinase A. Proc Natl Acad Sci U S A 106:1620-1625.CrossRef Medline
28. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20: 3354-3368.Medline
29. Poolos NP, Migliore M, Johnston D (2002) Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites. Nat Neurosci 5:767-774.Medline
30. Power JM, Thompson LT, Moyer JR Jr, Disterhoft JF (1997) Enhanced synaptic transmission in CA1 hippocampus after eyeblink conditioning. J Neurophysiol 78:1184-1187.Medline
31. Ruediger S, Vittori C, Bednarek E, Genoud C, Strata P, Sacchetti B, Caroni P (2011) Learning-related feedforward inhibitory connectivity growth required for memory precision. Nature 473:514-518.CrossRef Medline
32. Stocker M, Krause M, Pedarzani P (1999) An apamin-sensitive Ca 2- activated K current in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 96:4662-4667.CrossRef Medline
33. Urban-Ciecko J, Kossut M, Mozrzymas JW (2010) Sensory learning differentially affects GABAergic tonic currents in excitatory neurons and fast spiking interneurons in layer 4 of mouse barrel cortex. J Neurophysiol 104:746-754.CrossRef Medline
34. Wu WW, Chan CS, Disterhoft JF (2004) Slow afterhyperpolarization governs the development of NMDA receptor-dependent afterdepolarization in CA1 pyramidal neurons during synaptic stimulation. J Neurophysiol 92:2346-2356.CrossRef Medline
35. Zhang L, McBain CJ (1995) Potassium conductances underlying repolarization and after-hyperpolarization in rat CA1 hippocampal interneurones. J Physiol 488 (Pt 3):661-672.
36. Zhou Y, Won J, Karlsson MG, Zhou M, Rogerson T, Balaji J, Neve R, Poirazi P, Silva AJ (2009) CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala. Nat Neurosci 12:1438-1443.CrossRef Medline