Serotonin mediates learning-induced potentiation of excitability

Journal of Neurophysiology

Volumn 94, Issue 6, 2005, Pages 4002-4010

  Burrell, Brian D ^a   Sahley, Christie L ^b  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE INHIBITOR; GUANINE NUCLEOTIDE BINDING PROTEIN; METABOTROPIC RECEPTOR; METHYSERGIDE; SEROTONIN; SEROTONIN ANTAGONIST; SEROTONIN RECEPTOR;

ANIMAL CELL; ARTICLE; ENZYME ACTIVATION; HIPPOCAMPUS; INTERNEURON; LEARNING; LEECH; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; PYRAMIDAL NERVE CELL; SENSITIZATION; SEROTONIN RELEASE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CYCLIC AMP; CYCLIC CMP; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; GANGLIA, INVERTEBRATE; GUANOSINE DIPHOSPHATE; INTERNEURONS; LEARNING; LEECHES; METHYSERGIDE; NEURAL NETWORKS (COMPUTER); NEURONAL PLASTICITY; REFLEX; SEROTONIN; SEROTONIN ANTAGONISTS; THIONUCLEOTIDES; TIME FACTORS;

EID: 28044439820     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00432.2005     Document Type: Article

References (62)

1. Abraham WC and Bear MF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19: 126-130, 1996.
2. + currents mediates retention of a learned association. Behav Neural Biol 44: 278-300, 1985.
3. Andersen P, Sundberg SH, Sveen O, Swann JW, and Wigstrom H. Possible mechanisms for long-lasting potentiation of synaptic transmission in hippocampal slices from guinea pigs. J Physiol 302: 463-482, 1980.
4. Antonov I, Antonova I, Kandel ER, and Hawkins RD. The contribution of activity-dependent synaptic plasticity to classical conditioning in Aplysia. J Neurosci 21: 6413-6422, 2001.
5. Baccus SA, Burrell BD, Sahley CL, and Muller KJ. Action potential reflection and failure at axon branch points cause stepwise changes in EPSPs in a neuron essential for learning. J Neurophysiol 83: 1693-1700, 2000.
6. Baccus SA, Sahley CL, and Muller KJ. Multiple sites of action potential initiation increase neuronal firing rate. J Neurophysiol 86: 1226-1236, 2001.
7. Bekkers JM and Delaney AJ. Modulation of excitability by alpha-dendrotoxin-sensitive potassium channels in neocortical pyramidal neurons. J Neurosci 21: 6553-6560, 2001.
8. Belardetti F, Biondi C, Colombaioni L, Brunelli M, and Trevisani A. Role of serotonin and cyclic AMP on facilitation of the fast conducting system activity in the leech Hirudo medicinalis. Brain Res 246: 89-103, 1982.
9. Bliss TV and Lomo T. 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, 1973.
10. Burrell BD and Sahley CL. Multiple forms of long-term potentiation and long-term depression converge on a single interneuron in the leech CNS. J Neurosci 24: 4011-4019, 2004.
11. Burrell BD, Sahley CL, and Muller KJ. Non-associative learning and serotonin induce similar bi-directional changes in excitability of a neuron critical for learning in the medicinal leech. J Neurosci 21: 1401-1412, 2001.
12. Burrell BD, Sahley CL, and Muller KJ. Differential effects of serotonin enhance activity of an electrically coupled neural network. J Neurophysiol 87: 2889-2895, 2002.
13. Burrell BD, Sahley CL, and Muller KJ. Progressive recovery of learning during regeneration of a single synapse in the medicinal leech. J Comp Neurol 457: 67-74, 2003.
14. + electrogenic pump in T sensory neurones of the leech. J Exp Biol 155: 261-273, 1991.
15. Catarsi S, Scuri R, and Brunelli M. Octopamine and Leydig cell stimulation depress the afterhyperpolarization in touch sensory neurons of the leech. Neuroscience 66: 751-759, 1995.
16. Cleary LJ, Lee WL, and Byrne JH. Cellular correlates of long-term sensitization in Aplysia. J Neurosci 18: 5988-5998, 1998.
17. Cohen AS, Coussens CM, Raymond CR, and Abraham WC. Long-lasting increase in cellular excitability associated with the priming of LTP induction in rat hippocampus. J Neurophysiol 82: 3139-3148, 1999.
18. Cruz GE, Sahley CL, and Muller KJ. A neuronal network with multiple initiation sites in a behaving leech. Soc Neurosci Abstr 520: 9, 2003.
19. Cudmore RH and Turrigiano GG. Long-term potentiation of intrinsic excitability in LV visual cortical neurons. J Neurophysiol 92: 341-348, 2004.
20. Daly KC, Christensen TA, Lei H, Smith BH, and Hildebrand JG. Learning modulates the ensemble representations for odors in primary olfactory networks. Proc Natl Acad Sci USA 101: 10476-10481, 2004.
21. Daoudal G and Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem 10: 456-465, 2003.
22. Daoudal G, Hanada Y, and Debanne D. Bidirectional plasticity of excitatory postsynaptic potential (EPSP)-spike coupling in CA1 hippocampal pyramidal neurons. Proc Natl Acad Sci USA 99: 14512-14517, 2002.
23. Debski EA and Friesen WO. Role of central interneurons in habituation of swimming activity in the medicinal leech. J Neurophysiol 55: 977-994, 1986.
24. Ehrlich JS, Boulis NM, Karrer T, and Sahley CL. Differential effects of serotonin depletion on sensitization and dishabituation in the leech, Hirudo medicinalis. J Neurobiol 23: 270-279, 1992.
25. Frank E, Jansen JK, and Rinvik E. A multisomatic axon in the central nervous system of the leech. J Comp Neurol 159: 1-13, 1975.
26. Frick A and Johnston D. Plasticity of dendritic excitability. J Neurobiol 64: 100-115, 2005.
27. Frick A, Magee J, and Johnston D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci 7: 126-135, 2004.
28. Gainutdinov KL, Chekmarev LJ, and Gainutdinova TH. Excitability increase in withdrawal interneurons after conditioning in snail. Neuroreport 9: 517-520, 1998.
29. Gardner-Medwin AR, Jansen JK, and Taxt T. The "giant" axon of the leech. Acta Physiol Scand 87: 30-31, 1973.
30. Hoyer D, Hannon JP, and Martin GR. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71: 533-554, 2002.
31. Le Ray D, Fernandez DS, Belen PA, Fuenzalida M, and Buno W. Heterosynaptic metaplastic regulation of synaptic efficacy in CA1 pyramidal neurons of rat hippocampus. Hippocampus 14: 1011-1025, 2004.
32. Lisman JE. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20: 38-43, 1997.
33. Mar A and Drapeau P. Modulation of conduction block in leech mechanosensory neurons. J Neurosci 16: 4335-4343, 1996.
34. Modney BK, Sahley CL, and Muller KJ. Regeneration of a central synapse restores nonassociative learning. J Neurosci 17: 6478-6482, 1997.
35. Moita MA, Rosis S, Zhou Y, LeDoux JE, and Blair HT. Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37: 485-497, 2003.
36. Morozov A, Muzzio IA, Bourtchouladze R, Van Strien N, Lapidus K, Yin D, Winder DG, Adams JP, Sweatt JD, and Kandel ER. Rap1 couples cAMP signaling to a distinct pool of p42/44MAPK regulating excitability, synaptic plasticity, learning, and memory. Neuron 39: 309-325, 2003.
37. Moss BL, Fuller AD, Sahley CL, and Burrell BD. Serotonin modulates axo-axonal coupling between neurons critical for learning in the leech. J Neurophysiol 94: 2575-2589, 2005.
38. Moyer JR Jr, Power JM, Thompson LT, and Disterhoft JF. Increased excitability of aged rabbit CA1 neurons after trace eyeblink conditioning. J Neurosci 20: 5476-5482, 2000.
39. Moyer JR Jr, Thompson LT, and Disterhoft JF. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J Neurosci 16: 5536-5546, 1996.
40. Muller KJ and Scott SA. Transmission at a "direct" electrical connexion mediated by an interneuron in the leech. J Physiol 311: 565-583, 1981.
41. Nicholls JG and Purves D. Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. J Physiol 209: 647-667, 1970.
42. Nolan MF, Malleret G, Dudman JT, Buhl DL, Santoro B, Gibbs E, Vronskaya S, Buzsaki G, Siegelbaum SA, Kandel ER, and Morozov A. A behavioral role for dendritic integration: HCN1 channels constrain spatial memory and plasticity at inputs to distal dendrites of CA1 pyramidal neurons. Cell 119: 719-732, 2004.
43. Oh MM, Kuo AG, Wu WW, Sametsky EA, and Disterhoft JF. Watermaze learning enhances excitability of CA1 pyramidal neurons. J Neurophysiol 90: 2171-2179, 2003.
44. Peterson EL. Photoreceptors and visual interneurons in the medicinal leech. J Neurobiol 15: 413-428, 1984.
45. Saar D, Grossman Y, and Barkai E. Reduced after-hyperpolarization in rat piriform cortex pyramidal neurons is associated with increased learning capability during operant conditioning. Eur J Neurosci 10: 1518-1523, 1998.
46. Sah P and Faber ES. Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 66: 345-353, 2002.
47. Sahley CL. Serotonin depletion impairs but does not eliminate classical conditioning in the leech Hirudo medicinalis. Behav Neurosci 108: 1043-1052, 1994.
48. Sahley CL, Modney BK, Boulis NM, and Muller KJ. The S cell: an interneuron essential for sensitization and full dishabituation of leech shortening. J Neurosci 14: 6715-6721, 1994.
49. Schreurs BG, Tomsic D, Gusev PA, and Alkon DL. Dendritic excitability microzones and occluded long-term depression after classical conditioning of the rabbit's nictitating membrane response. J Neurophysiol 77: 86-92, 1997.
50. Schreurs BG, Gusev PA, Tomsic D, Alkon DL, and Shi T. Intracellular correlates of acquisition and long-term memory of classical conditioning in Purkinje cell dendrites in slices of rabbit cerebellar lobule HVI. J Neurosci 18: 5498-5507, 1998.
51. Shaw BK and Kristan WB Jr. The whole-body shortening reflex of the medicinal leech: motor pattern, sensory basis, and interneuronal pathways. J Comp Physiol [A] 177: 667-681, 1995.
52. Shaw BK and Kristan WB Jr. Relative roles of the S cell network and parallel interneuronal pathways in the whole-body shortening reflex of the medicinal leech. J Neurophysiol 82: 1114-1123, 1999.
53. + channels modulate synaptic plasticity and memory encoding. J Neurosci 22: 10163-10171, 2002.
54. Straub VA and Benjamin PR. Extrinsic modulation and motor pattern generation in a feeding network: a cellular study. J Neurosci 21: 1767-1778, 2001.
55. Thompson LT, Moyer JR Jr, and Disterhoft JF. Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J Neurophysiol 76: 1836-1849, 1996.
56. Tierney AJ. Structure and function of invertebrate 5-HT receptors: a review. Comp Biochem Physiol A Mol Integr Physiol 128: 791-804, 2001.
57. Wang Y. Myomodulin modulation of the Retzius cell and its role in the leech associative learning (PhD thesis). West Lafayette, IN: Purdue University, 1998.
58. Wang Y, Strong JA, and Sahley CL. Modulatory effects of myomodulin on the excitability and membrane currents in Retzius cells of the leech. J Neurophysiol 82: 216-225, 1999.
59. Wu N, Enomoto A, Tanaka S, Hsiao CF, Nykamp DQ, Izhikevich E, and Chandler SH. Persistent sodium currents in mesencephalic V neurons participate in burst generation and control of membrane excitability. J Neurophysiol 2004.
60. Wu WW, Oh MM, and Disterhoft JF. Age-related biophysical alterations of hippocampal pyramidal neurons: implications for learning and memory. Ageing Res Rev 1: 181-207, 2002.
61. Zaccardi ML, Traîna G, Cataldo E, and Brunelli M. Sensitization and dishabituation of swim induction in the leech Hirudo medicinalis. role of serotonin and cyclic AMP. Behav Brain Res 153: 317-326, 2004.
62. Zhang W and Linden DJ. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4: 885-900, 2003.