Long-Term Modulation of A-Type K+ Conductances in Hippocampal CA1 Interneurons in Rats After Chronic Intermittent Ethanol Exposure During Adolescence or Adulthood

Alcoholism: Clinical and Experimental Research

Volumn 37, Issue 12, 2013, Pages 2074-2085

  Li, Qiang ^a   Fleming, Rebekah L ^a   Acheson, Shawn K ^a   Madison, Roger D ^a   Moore, Scott D ^a   Risher, Mary Louise ^a   Wilson, Wilkie A ^a,b   Swartzwelder, H Scott ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

Adolescent; Chronic Intermittent Ethanol Exposure; Hippocampus; Interneurons

Indexed keywords

ALCOHOL; VOLTAGE GATED POTASSIUM CHANNEL;

ADOLESCENT; ADULT; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DENSITY; CELL DISRUPTION; CELL FUNCTION; DEPOLARIZATION; ELECTROPHYSIOLOGICAL PROCEDURES; HIPPOCAMPAL CA1 REGION; HYPERPOLARIZATION; INTERNEURON; LONG TERM EXPOSURE; MALE; NEUROMODULATION; NONHUMAN; POTASSIUM CONDUCTANCE; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; STEADY STATE;

RATTUS;

ADOLESCENT; CHRONIC INTERMITTENT ETHANOL EXPOSURE; HIPPOCAMPUS; INTERNEURONS;

AGE FACTORS; ANIMALS; CA1 REGION, HIPPOCAMPAL; ELECTRIC CONDUCTIVITY; ELECTROPHYSIOLOGICAL PHENOMENA; ETHANOL; INTERNEURONS; MALE; POTASSIUM CHANNELS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 84897039491     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/acer.12204     Document Type: Article

References (55)

1. + currents in Lymnaea neurons. J Pharmacol Exp Ther 281:84-92.
2. An WF, Bowlby MR, Betty M, Cao J, Ling HP, Mendoza G, Hinson JW, Mattsson KI, Strassle BW, Trimmer JS, Rhodes KJ (2000) Modulation of A-type potassium channels by a family of calcium sensors. Nature 403:553-556.
3. Andrásfalvy K, Makara JK, Johnston D, Magee JC (2008) Altered synaptic and non-synaptic properties of CA1 pyramidal neurons in Kv4.2 knockout mice. J Physiol 586:3881-3892.
4. Binbaum SG, Varga AW, Yuan LL, Anderson AE, Sweatt JD, Schrader LA (2004) Structure and function of Kv4-family transient potassium channels. Physiol Rev 84:803-833.
5. + currents and repetitive firing in hippocampal interneurons. Neuroscience 176:173-187.
6. Bourdeau ML, Morin F, Laurent CE, Azzi M, Lacaille JC (2007) Kv43-mediated A-type K+ currents underlie rhythmic activity in hippocampal interneurons. J Neurosci 27:1942-1953.
7. Cai SQ, Li WC, Sesti F (2007) Multiple modes of A-type potassium current regulation. Curr Pharm Des 13:3178-3184.
8. Carrasquillo Y, Burkhalter A, Nerbonne JM (2012) A-type K+ channels encoded by Kv4.2, Kv4.3 and Kv1.4 differentially regulate intrinsic excitability of cortical pyramidal neurons. J Physiol 590:3877-3890.
9. Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, Moreno H, Nadal MS, Ozaita A, Pountney D, Saganich M, Vega-Saenz de Miera E, Rudy B (1999) Molecular diversity of K channels. Ann N Y Acad Sci 868:233-285.
10. Cooper EC, Milroy A, Jan YN, Jan LY, Lowenstein DH (1998) Presynaptic localization of Kv1.4-containing A-type potassium channels near excitatory synapses in the hippocampus. J Neurosci 18:965-997.
11. Dahl RE (2004) Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann N Y Acad Sci 1021:1-22.
12. Elfant D, Zoltan B, Emptage N, Capogna N (2008) Specific inhibitory synapses shift the balance from feedforward to feedback inhibition of hippocampal CA1 pyramidal cells. Eur J Pharmacol 27:104-113.
13. Empson RM, Heinemann U (1995) The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J Physiol (Lond) 484:707-729.
14. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
15. Freund TF, Gulyas AI (1997) Inhibitory control of GABAergic interneurons in the hippocampus. Can J Physiol Pharmacol 75:479-487.
16. Gonzalez LP (1998) Electrophysiological changes after repeated alcohol withdrawal. Alcohol Health Res World 22:34-37.
17. Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869-875.
18. Jerng HH, Pfaffinger PJ, Covarrubias M (2004) Molecular physiology and modulation of somatodendritic A-type potassium channels. Mol Cell Neurosci 27:343-369.
19. Johnston J, Forsythe ID, Kopp-Scheinpflug C (2010) Going native: voltage-gated potassium channels controlling neuronal excitability. J Physiol 588:3187-3200.
20. + channel downregulation mediates intrinsic plasticity in hippocampal CA1 pyramidal neurons. PLoS ONE 4:e6549.
21. Jung SC, Kim J, Hoffman DA (2008) Rapid, bidirectional remodeling of synaptic NMDA receptor subunit composition by A-type K+ channel activity in hippocampal CA1 pyramidal neurons. Neuron 60:657-671.
22. Kang J, Huguenard JR, Prince DA (2000) Voltage-gated potassium channels activated during action potentials in layer V neocortical pyramidal neurons. J Neurophysiol 83:70-80.
23. Khaliq ZM, Bean BP (2008) Dynamic, nonlinear feedback regulation of slow pacemaking by A-type potassium current in ventral tegmental area neurons. J Neurosci 28:10905-10917.
24. Kim J, Hoffman DA (2008) Potassium channels: newly found players in synaptic plasticity. Neuroscientist 14:276-286.
25. Kim J, Wei DS, Hoffman DA (2005) Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurons. J Physiol (Lond) 569:41-57.
26. Kole MHP, Letzkus JJ, Stuart GJ (2007) Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55:633-647.
27. Lacaille JC, Schwartzkroin PA (1988) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intracellular response characteristics, synaptic responses, and morphology. J Neurosci 8:1400-1410.
28. Lefebvre T, Gonzalez BJ, Vaudry D, Desrues L, Falluel-Morel A, Aubert N, Fournier A, Tonon M-C, Vaudry H, Castel H (2009) Paradoxical effect of ethanol on potassium channel currents and cell survival in cerebellar granule neurons. J Neurochem 110:976-989.
29. Lei Z, Deng P, Li J, Xu ZC (2012) Alterations of A-type potassium channels in hippocampal neurons after traumatic brain injury. J Neurotrauma 20:235-245.
30. Lien CC, Jonas P (2003) Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J Neurosci 23:2058-2068.
31. + channels in dendritic inhibitory interneurons of rat hippocampus. J Physiol (Lond) 538:405-419.
32. Liss B, Franz O, Sewing S, Bruns R, Neuhoff H, Roeper J (2001) Tuning pacemaker frequency of individual dopaminergic neurons by Kv4.3L and KChip3.1 transcription. EMBO J 20:5715-5724.
33. Littleton J (1998) Neurochemical mechanisms underlying alcohol withdrawal. Alcohol Health Res World 22:13-24.
34. Lugo JN, Brewster AL, Spencer CM, Anderson AE (2012) Kv4.2 knockout mice have hippocampal-dependent learning and memory deficits. Learn Mem 19:182-189.
35. + currents in neurons. J Physiol (Lond) 586:5609-5623.
36. Markwiese BJ, Acheson SK, Levin ED, Wilson WA, Swartzwelder HS (1998) Differential effects of ethanol on memory in adolescent and adult rats. Alcohol Clin Exp Res 22:416-421.
37. Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18:8111-8125.
38. Marty VN, Spigelman I (2012) Long-lasting alterations in membrane properties, k(+) currents, and glutamatergic synaptic currents of nucleus accumbens medium spiny neurons in a rat model of alcohol dependence. Front Neurosci 6:3-15.
39. Menegola M, Hisonou H, Vacher H, Trimmer JS (2008) Dendritic A-type potassium channels subunit expression in CA1 hippocampal interneurons. Neuroscience 154:953-964.
40. Migliore M, Hoffman DA, Magee JC, Johnston D (1999) Role of an A-type K+ conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J Comput Neurosci 7:5-15.
41. Monti PM, Miranda R Jr, Nixon K, Sher KJ, Swartzwelder HS, Tapert SF, White A, Crews FT (2005) Adolescence: booze, brains, and behavior. Alcohol Clin Exp Res 29:207-220.
42. + currents contributing to subthreshold membrane potential oscillations in hippocampal CA1 interneurons. J Neurophysiol 103:3472-3489.
43. NIAAA (2000) 10th Special Report to the U.S. Congress on Alcohol and Health. US Deparment of Health and Human Services, Bethesda, MD.
44. + channels supports activity-dependent enhancement of back-propagating action potentials in hippocampal CA1. J Neurophysiol 85:1013-1016.
45. Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159-1163.
46. Pouille F, Scanziani M (2004) Routing of spike series by dynamic circuits in the hippocampus. Nature 429:717-723.
47. Sircar R, Sircar D (2005) Adolescent rats exposed to repeated ethanol treatment show lingering behavioral impairments. Alcohol Clin Exp Res 29:1402-1410.
48. Swartzwelder HS, Wilson WA, Tayyeb MI (1995) Age-dependent inhibition of long-term potentiation by ethanol in immature versus mature hippocampus. Alcohol Clin Exp Res 19:1480-1485.
49. Tavian D, De Giorgio A, Granato A (2011) Selective underexpression of Kv3.2 and Kv3.4 channels in the cortex of rats exposed to ethanol during early postnatal life. Neurol Sci 32:571-577.
50. + currents amplitude are linearly related in basal ganglia and basal forebrain neurons. J Neurosci 20:579-588.
51. Treistman SN, Wilson AH (1987) Effects of ethanol on early potassium currents in Aplysia: cell-specificity and influence of channel state. J Neurosci 7:3207-3214.
52. Tukker J, Fuentealba P, Hartwich K, Somoguyi P, Klausberger T (2007) Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo. J Neurosci 27:8184-8189.
53. Vida I, Halasy K, Szinyei C, Somogyi P, Buhl EH (1998) Unitary IPSPs evoked by interneurons at the stratum radiatum-stratum lacunosum-moleculare border in the CA1 area of the rat hippocampus in vitro. J Physiol (Lond) 506:755-773.
54. White AM, Ghia AJ, Levin ED, Swartzwelder HS (2000) Binge pattern ethanol exposure: differential impact on subsequent responsiveness to ethanol. Alcohol Clin Exp Res 24:1251-1256.
55. Yan HD, Li Q, Fleming R, Madison R, Wilson W, Swartzwelder HS (2009) Developmental sensitivity of hippocampal interneurons to ethanol: involvement of the hyperpolarization-activated current, Ih. J Neurophysiol 101:67-83.