Alterations in intrinsic neuronal excitability during normal aging

Aging Cell

Volumn 6, Issue 3, 2007, Pages 327-336

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

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Afterhyperpolarization; Aging; Alzheimer's disease; Hippocampus; Learning

Indexed keywords

3 [3 (3 METHOXYPHENYL) 2 PROPYNYLOXYIMINO] 1 AZABICYCLO[2.2.1]HEPTANE; CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM CHANNEL L TYPE; GALANTAMINE; METRIFONATE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTRANSMITTER; NIMODIPINE;

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; AGING; ALZHEIMER DISEASE; COGNITIVE DEFECT; DRUG EFFICACY; DRUG MECHANISM; EYELID REFLEX; HIPPOCAMPUS; HUMAN; LEARNING; LEARNING DISORDER; LONG TERM POTENTIATION; MOLECULAR DYNAMICS; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; SYNAPTIC TRANSMISSION; TASK PERFORMANCE; TRANSGENICS; WORKING MEMORY;

AGED; AGING; ALZHEIMER DISEASE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; HIPPOCAMPUS; HUMANS; LEARNING; MODELS, BIOLOGICAL; MODELS, NEUROLOGICAL; NEURONS; PYRAMIDAL CELLS; RABBITS; SYNAPTIC TRANSMISSION;

ORYCTOLAGUS CUNICULUS; RATTUS;

EID: 34249075140     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/j.1474-9726.2007.00297.x     Document Type: Review

References (99)

1. Aiba A, Kano M, Chen C, Stanton ME, Fox GD, Herrup K, Zwingman TA, Tonegawa S (1994) Deficient cerebellar long-term depression and impaired motor learning in mGluR1 mutant mice. Cell 79, 377-388.
2. +-conductance. Brain Res. 698, 193-203.
3. Barnes CA (1979) Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 93, 74-104.
4. Berger TW, Alger B, Thompson RF (1976) Neuronal substrate of classical conditioning in the hippocampus. Science 192, 483-485.
5. Berridge MJ (1998) Neuronal calcium signaling. Neuron 21, 13-26.
6. 2+. Trends Neurosci. 28, 422-428.
7. Bliss TV, Collingridge GL, Morris RG (2003) Long-term potentiation: enhancing neuroscience for 30 years. Philos. Trans. R. Soc. Lond. B, Biol. Sci. 358, 607-842.
8. Bliss TV, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J. Physiol. 232, 357-374.
9. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 331-356.
10. + channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J. Neurosci. 24, 5301-5306.
11. Campbell LW, Hao SY, Thibault O, Blalock EM, Landfield PW (1996) Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J. Neurosci. 16, 6286-6295.
12. Cason H (1922) The conditioned eyelid reaction. J. Exp. Psychol. 3, 153-196.
13. 2+ channel activity in single neurons of hippocampal 'zipper' slices. Proc. Natl Acad. Sci. USA 97, 4357-4362.
14. Christian KM, Thompson RF (2003) Neural substrates of eyeblink conditioning: Acquisition and retention. Learn. Mem. 10, 427-455.
15. Clark RE, Squire LR (1998) Classical conditioning and brain systems: The role of awareness. Science 280, 77-81.
16. Cohen AS, Coussens CM, Raymond CR, Abraham WC (1999) Long-lasting increase in cellular excitability associated with the priming of LTP induction in rat hippocampus. J. Neurophysiol. 82, 3139-3148.
17. Coulter DA, Lo Turco JJ, Kubota M, Disterhoft JF, Moore JW, Alkon DL (1989) Classical conditioning reduces amplitude and duration of calcium-dependent afterhyperpolarization in rabbit hippocampal pyramidal cells. J. Neurophysiol. 61, 971-981.
18. Disterhoft JF, Coulter DA, Alkon DL (1986) Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc. Natl Acad. Sci. USA 83, 2733-2737.
19. Disterhoft JF, Golden DT, Read HL, Coulter DA, Alkon DL (1988) AHP reductions in rabbit hippocampal neurons during conditioning correlate with acquisition of the learned response. Brain Res. 462, 118-125.
20. Disterhoft JF, Oh MM (2006a) Learning, aging and intrinsic neuronal plasticity. Trends Neurosci. 29, 587-599.
21. Disterhoft JF, Oh MM (2006b) Pharmacological and molecular enhancement of learning in aging and Alzheimer's disease. J. Physiol. Paris 99, 180-192.
22. Foster TC (1999) Involvement of hippocampal synaptic plasticity in age-related memory decline. Brain Res. Brain Res. Rev. 30, 236-249.
23. Foster TC, Kumar A (2002) Calcium dysregulation in the aging brain. Neuroscientist 8, 297-301.
24. 2+-release. J. Neuroscience 26, 3482-3490.
25. Geinisman Y (2000) Structural synaptic modifications associated with hippocampal LTP and behavioral learning. Cereb. Cortex 10, 952-962.
26. + channel inactivation, spike broadening, and after-hyperpolarization in Kvβ1.1 deficient mice with impaired learning. Learn. Mem. 5, 257-273.
27. Gormezano I, Prokasy WF, Thompson RF (1987) Classical Conditioning. Hillsdale, NJ: L. Erlbaum Associates.
28. Graves CA, Solomon PR (1985) Age-related disruption of trace but not delay classical conditioning of the rabbit's nictitating membrane response. Behav. Neurosci. 99, 88-96.
29. Gu N, Vervaeke K, Hu H, Storm JF (2005) Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells. J. Physiol. 566, 689-715.
30. Harrison J, Buchwald J (1983) Eyeblink conditioning deficits in the old cat. Neurobiol. Aging 4, 45-51.
31. Hebert LE, Scherr PA, Bienias JL, Bennett DA, Evans DA (2003) Alzheimer disease in the US population: Prevalence estimates using the 2000 census. Arch. Neurol. 60, 1119-1122.
32. 2+ accumulation and the slow afterhyperpolarization in hippocampal CA1 pyramidal neurons. Neuroscience 135, 413-420.
33. Hughes B, Schlosberg H (1938) Conditioning in the white rat. IV. The conditioned lid reflex. J. Exp. Psychol. 23, 641-650.
34. de Jong GI, Naber PA, Van der Zee EA, Thompson LT, Disterhoft JF, Luiten PG (1996) Age-related loss of calcium binding proteins in rabbit hippocampus. Neurobiol. Aging 17, 459-465.
35. Kim JJ, Clark RE, Thompson RF (1995) Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav. Neurosci. 109, 195-203.
36. Kim JJ, Thompson RF (1997) Cerebellar circuits and synaptic mechanisms involved in classical eyeblink conditioning. Trends Neurosci. 20, 177-181.
37. Kishimoto Y, Suzuki M, Kawahara S, Kirino Y (2001) Age-dependent impairment of delay and trace eyeblink conditioning in mice. Neuroreport 12, 3349-3352.
38. Knuttinen MG, Gamelli AE, Weiss C, Power JM, Disterhoft JF (2001a) Age-related effects on eyeblink conditioning in the F344 × BN F1 hybrid rat. Neurobiol. Aging 22, 1-8.
39. Knuttinen MG, Power JM, Preston AR, Disterhoft JF (2001b) Awareness in classical differential eyeblink conditioning in young and aging humans. Behav. Neurosci. 115, 747-757.
40. Kramar EA, Lin B, Lin CY, Arai AC, Gall CM, Lynch G (2004) A novel mechanism for the facilitation of θ-induced long-term potentiation by brain-derived neurotrophic factor. J. Neurosci. 24, 5151-5161.
41. Kumar A, Foster TC (2002) 17β-estradiol benzoate decreases the AHP amplitude in CA1 pyramidal neurons. J. Neurophysiol. 88, 621-626.
42. Kumar A, Foster TC (2004) Enhanced long-term potentiation during aging is masked by processes involving intracellular calcium stores. J. Neurophysiol. 91, 2437-2444.
43. Kumar A, Foster TC (2007) Environmental enrichment decreases the afterhyperpolarization in senescent rats. Brain Res. 1130, 103-107.
44. Kuo AG, Lee G, Disterhoft JF (2004) Alteration of sI AHP underlies reduction of AHP in rat CA1 pyramidal neurons after trace eyeblink conditioning. Program No. 741. 13. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Online.
45. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226, 1089-1092.
46. Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J. Physiol. 354, 319-331.
47. 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.
48. McEchron MD, Weible AP, Disterhoft JF (2001) Aging and learning-specific changes in single-neuron activity in CA1 hippocampus during rabbit trace eyeblink conditioning. J. Neurophysiol. 86, 1839-1857.
49. McGlinchey-Berroth R, Carrillo MC, Gabrieli JD, Brawn CM, Disterhoft JF (1997) Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behav. Neurosci. 111, 873-882.
50. Moyer JR Jr, Deyo RA, Disterhoft JF (1990) Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav. Neurosci. 104, 243-252.
51. Moyer JR, Power JM, Thompson LT, Disterhoft JF (2000) Increased excitability of aged rabbit CA1 neurons after trace eyeblink conditioning. J. Neurosci. 20, 5476-5482.
52. Moyer JR, Thompson LT, Black JP, Disterhoft JF (1992) Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. J. Neurophysiol. 68, 2100-2109.
53. Moyer JR, Thompson LT, Disterhoft JF (1996) Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J. Neurosci. 16, 5536-5546.
54. Murphy GG, Fedorov NB, Giese KP, Ohno M, Friedman E, Chen R, Silva AJ (2004) Increased neuronal excitability, synaptic plasticity, and learning in aged Kvβ1.1 knockout mice. Curr. Biol. 14, 1907-1915.
55. Need AC, Irvine EE, Giese KP (2003) Learning and memory impairments in Kvβ1.1-null mutants are rescued by environmental enrichment or ageing. Eur. J. Neurosci. 18, 1640-1644.
56. 2+-mediated feedback loop in dendritic spines. Nat. Neurosci. 8, 642-649.
57. Nicoll RA (1988) The coupling of neurotransmitter receptors to ion channels in the brain. Science 241, 545-551.
58. 2+ channels. J. Neurosci. 18, 3171-3179.
59. Oakley H, Cole SL, Logan S, Maus E, Shao P, Craft J, Guillozet-Bongaarts A, Ohno M, Disterhoft J, Van Eldik L, Berry R, Vassar R (2006) Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: Potential factors in amyloid plaque formation. J. Neurosci. 26, 10129-10140.
60. Oh MM, Kuo AG, Wu WW, Sametsky EA, Disterhoft JF (2003) Watermaze learning enhances excitability of CA1 pyramidal neurons. J. Neurophysiol. 90, 2171-2179.
61. Oh MM, Power JM, Thompson LT, Moriearty PL, Disterhoft JF (1999) Metrifonate increases neuronal excitability in CA1 pyramidal neurons from both young and aging rabbit hippocampus. J. Neurosci. 19, 1814-1823.
62. Oh MM, Weible AP, Azzarello J, Galvez R, Maccaferri G, Disterhoft JF (2004) Decreased excitability in stratum oriens interneurons of hippocampal slices from aging animals. Program No. 565.10. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience. Online.
63. Ohno M, Chang L, Tseng W, Oakley H, Citron M, Klein WL, Vassar R, Disterhoft JF (2006a) Temporal memory deficits in Alzheimer's mouse models: Rescue by genetic deletion of BACE1. Eur. J. Neurosci. 23, 251-260.
64. Ohno M, Sametsky EA, Silva AJ, Disterhoft JF (2006b) Differential effects of αCaMKII mutation on hippocampal learning and changes in intrinsic neuronal excitability. Eur. J. Neurosci. 23, 2235-2240.
65. Ohno M, Sametsky EA, Younkin LH, Oakley H, Younkin SG, Citron M, Vassar R, Disterhoft JF (2004) BACE1 deficiency rescues memory deficits and cholinergic dysfunction in a mouse model of Alzheimer's disease. Neuron 41, 27-33.
66. Potier B, Krzywkowski P, Lamour Y, Dutar P (1994) Loss of calbindin-immunoreactivity in CA1 hippocampal stratum radiatum and stratum lacunosum-moleculare interneurons in the aged rat. Brain Res. 661, 181-188.
67. Power JM, Wu WW, Sametsky E, Oh MM, Disterhoft JF (2002) Age-related enhancement of the slow outward calcium-activated potassium current in hippocampal CA1 pyramidal neurons in vitro. J. Neurosci. 22, 7234-7243.
68. Saar D, Grossman Y, Barkai E (1998) Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur. J. Neurosci. 10, 1518-1523.
69. Sah P, Bekkers JM (1996) Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of long-term potentiation. J. Neurosci. 16, 4537-4542.
70. Sah P, Faber ES (2002) Channels underlying neuronal calcium-activated potassium currents. Prog. Neurobiol. 66, 345-353.
71. + channels in rat brain. J. Neurosci. 22, 9698-9707.
72. Sametsky EA, Wu WW, Oh MM, Moskal JR, Disterhoft JF (2001) Dorso-ventral gradient of excitability in hippocampal pyramidal neurons. Soc. Neurosci. Abstr. 27, 382.7.
73. Schneiderman N, Fuentes I, Gormezano I (1962) Acquisition and extinction of the classically conditioned eyelid response in the albino rabbit. Science 136, 650-652.
74. + currents generated by NMDA receptor activation in rat hippocampal pyramidal neurons. J. Neurophysiol. 87, 2983-2989.
75. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav. Neurosci. 100, 729-744.
76. Squire LR, Alvarez P (1995) Retrograde amnesia and memory consolidation: a neurobiological perspective. Curr. Opin. Neurobiol. 5, 169-177.
77. Squire LR, Kandel ER (1999) Memory: From Mind to Molecules. New York: Scientific American Library: Distributed by W. H. Freeman and Co.
78. Stanley DP, Shetty AK (2004) Aging in the rat hippocampus is associated with widespread reductions in the number of glutamate decarboxylase-67 positive interneurons but not interneuron degeneration. J. Neurochem. 89, 204-216.
79. + channels: molecular determinants and function of the SK family. Nat. Rev. Neurosci. 5, 758-770.
80. Storm JF (1990) Potassium currents in hippocampal pyramidal cells. Prog. Brain Res. 83, 161-187.
81. 2+] i and L-type calcium channel activity in aged hippocampal neurons: Relationship to impaired synaptic plasticity. J. Neurosci. 21, 9744-9756.
82. Thibault O, Landfield PW (1996) Increase in single L-type calcium channels in hippocampal neurons during aging. Science 272, 1017-1020.
83. Thompson RF (2005) In search of memory traces. Annu. Rev. Psychol. 56, 1-23.
84. Thompson LT, Deyo RA, Disterhoft JF (1990) Nimodipine enhances spontaneous activity of hippocampal pyramidal neurons in aging rabbits at a dose that facilitates associative learning. Brain Res. 535, 119-130.
85. Thompson LT, Moyer JR, Disterhoft JF (1996a) Trace eyeblink conditioning in rabbits demonstrates heterogeneity of learning ability both between and within age groups. Neurobiol. Aging 17, 619-629.
86. Thompson LT, Moyer JR, Disterhoft JF (1996b) Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J. Neurophysiol. 76, 1836-1849.
87. Tombaugh GC, Rowe WB, Rose GM (2005) The slow afterhyperpolarization in hippocampal CA1 neurons covaries with spatial learning ability in aged Fisher 344 rats. J. Neurosci. 25, 2609-2616.
88. Torres GE, Arfken CL, Andrade R (1996) 5-Hydroxytryptamine4 receptors reduce afterhyperpolarization in hippocampus by inhibiting calcium-induced calcium release. Mol. Pharmacol. 50, 1316-1322.
89. Tseng W, Guan R, Disterhoft JF, Weiss C (2004) Trace eyeblink conditioning is hippocampally dependent in mice. Hippocampus 14, 58-65.
90. Vela J, Gutierrez A, Vitorica J, Ruano D (2003) Rat hippocampal GABAergic molecular markers are differentially affected by ageing. J. Neurochem. 85, 368-377.
91. Weible AP, O'Reilly J, Weiss C, Disterhoft JF (2006) Comparisons of dorsal and ventral hippocampal CA1 pyramidal neuron activity during trace eye-blink conditioning in the rabbit. Neuroscience 141, 1123-1137.
92. Weiss C, Bouwmeester H, Power JM, Disterhoft JF (1999) Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behav. Brain Res. 99, 123-132.
93. Weiss C, Thompson RF (1991) The effects of age on eyeblink conditioning in the freely moving Fischer-344 rat. Neurobiol. Aging 12, 249-254.
94. Woodruff-Pak DS, Thompson RF (1988) Classical conditioning of the eyeblink response in the delay paradigm in adults aged 18-83 years. Psychol. Aging 3, 219-229.
95. Woodruff-Pak DS, Trojanowski JQ (1996) The older rabbit as an animal model: Implications for Alzheimer's disease. Neurobiol. Aging 17, 283-290.
96. Woody CD, Brozek G (1969) Conditioned eye blink in the cat: Evoked responses of short latency. Brain Res. 12, 257-260.
97. 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.
98. Wu WW, Oh MM, Disterhoft JF (2002) Age-related biophysical alterations of hippocampal pyramidal neurons: Implications for learning and memory. Ageing Res. Rev. 1, 181-207.
99. Zelcer I, Cohen H, Richter-Levin G, Lebiosn T, Grossberger T, Barkai E (2006) A cellular correlate of learning-induced metaplasticity in the hippocampus. Cereb. Cortex 16, 460-468.