Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia

Shiv K. Sharma, Carolyn M. Sherff, Justin Shobe, Martha W. Bagnall, Michael A. Sutton, Thomas Carew

Research output: Contribution to journalArticle

Abstract

The mitogen-activated protein kinase (MAPK) pathway has been implicated recently in synaptic plasticity and memory. Here we used tail shock-induced sensitization of the tail-elicited siphon withdrawal reflex in Aplysia to examine the role of MAPK in three different phases of memory. We show that a specific pattern of serotonin (5-HT) application that produces intermediate-term and long-term synaptic facilitation (ITF and LTF, respectively) of the sensory-motor (SN-MN) synapses in Aplysia leads to sustained activation of extracellular signal-regulated kinase in the ventrocaudal cluster sensory neurons (SNs), which include the tail SNs. Furthermore, repeated tail shocks that induce intermediate-term and long-term memory (ITM and LTM, respectively) for sensitization also lead to sustained MAPK activation in the SNs. Given these results, we next examined the requirement of MAPK activity in (1) SN-MN synaptic facilitation and (2) memory for sensitization in Aplysia, by inhibiting MEK, the upstream kinase that phosphorylates and activates MAPK. In cellular experiments, we show that MAPK activity is required for ITF of tail SN-tail MN synapses, and, in parallel behavioral experiments, we show that ITM requires MAPK activity for its induction but not its expression. In contrast, short-term memory for sensitization does not require MAPK activity. Finally, 5-HT-induced LTF has been shown previously to require MAPK activity. Here we show that LTM for sensitization also requires MAPK activity. These results provide evidence that MAPK plays important roles specifically in long-lasting phases of synaptic plasticity and memory.

Original languageEnglish (US)
Pages (from-to)3899-3907
Number of pages9
JournalJournal of Neuroscience
Volume23
Issue number9
StatePublished - May 1 2003

Fingerprint

Aplysia
Mitogen-Activated Protein Kinases
Sensory Receptor Cells
Tail
Serotonin
Neuronal Plasticity
Synapses
Shock
MAP Kinase Kinase Kinases
Long-Term Memory
Extracellular Signal-Regulated MAP Kinases
Motor Neurons
Short-Term Memory
Reflex

Keywords

  • ERK
  • Learning
  • MAP kinase
  • Memory
  • Sensitization
  • Synaptic facilitation

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. / Sharma, Shiv K.; Sherff, Carolyn M.; Shobe, Justin; Bagnall, Martha W.; Sutton, Michael A.; Carew, Thomas.

In: Journal of Neuroscience, Vol. 23, No. 9, 01.05.2003, p. 3899-3907.

Research output: Contribution to journalArticle

Sharma, Shiv K. ; Sherff, Carolyn M. ; Shobe, Justin ; Bagnall, Martha W. ; Sutton, Michael A. ; Carew, Thomas. / Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia. In: Journal of Neuroscience. 2003 ; Vol. 23, No. 9. pp. 3899-3907.
@article{c60284a9cb9d4725ac32a3864f0c7362,
title = "Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia",
abstract = "The mitogen-activated protein kinase (MAPK) pathway has been implicated recently in synaptic plasticity and memory. Here we used tail shock-induced sensitization of the tail-elicited siphon withdrawal reflex in Aplysia to examine the role of MAPK in three different phases of memory. We show that a specific pattern of serotonin (5-HT) application that produces intermediate-term and long-term synaptic facilitation (ITF and LTF, respectively) of the sensory-motor (SN-MN) synapses in Aplysia leads to sustained activation of extracellular signal-regulated kinase in the ventrocaudal cluster sensory neurons (SNs), which include the tail SNs. Furthermore, repeated tail shocks that induce intermediate-term and long-term memory (ITM and LTM, respectively) for sensitization also lead to sustained MAPK activation in the SNs. Given these results, we next examined the requirement of MAPK activity in (1) SN-MN synaptic facilitation and (2) memory for sensitization in Aplysia, by inhibiting MEK, the upstream kinase that phosphorylates and activates MAPK. In cellular experiments, we show that MAPK activity is required for ITF of tail SN-tail MN synapses, and, in parallel behavioral experiments, we show that ITM requires MAPK activity for its induction but not its expression. In contrast, short-term memory for sensitization does not require MAPK activity. Finally, 5-HT-induced LTF has been shown previously to require MAPK activity. Here we show that LTM for sensitization also requires MAPK activity. These results provide evidence that MAPK plays important roles specifically in long-lasting phases of synaptic plasticity and memory.",
keywords = "ERK, Learning, MAP kinase, Memory, Sensitization, Synaptic facilitation",
author = "Sharma, {Shiv K.} and Sherff, {Carolyn M.} and Justin Shobe and Bagnall, {Martha W.} and Sutton, {Michael A.} and Thomas Carew",
year = "2003",
month = "5",
day = "1",
language = "English (US)",
volume = "23",
pages = "3899--3907",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "9",

}

TY - JOUR

T1 - Differential role of mitogen-activated protein kinase in three distinct phases of memory for sensitization in Aplysia

AU - Sharma, Shiv K.

AU - Sherff, Carolyn M.

AU - Shobe, Justin

AU - Bagnall, Martha W.

AU - Sutton, Michael A.

AU - Carew, Thomas

PY - 2003/5/1

Y1 - 2003/5/1

N2 - The mitogen-activated protein kinase (MAPK) pathway has been implicated recently in synaptic plasticity and memory. Here we used tail shock-induced sensitization of the tail-elicited siphon withdrawal reflex in Aplysia to examine the role of MAPK in three different phases of memory. We show that a specific pattern of serotonin (5-HT) application that produces intermediate-term and long-term synaptic facilitation (ITF and LTF, respectively) of the sensory-motor (SN-MN) synapses in Aplysia leads to sustained activation of extracellular signal-regulated kinase in the ventrocaudal cluster sensory neurons (SNs), which include the tail SNs. Furthermore, repeated tail shocks that induce intermediate-term and long-term memory (ITM and LTM, respectively) for sensitization also lead to sustained MAPK activation in the SNs. Given these results, we next examined the requirement of MAPK activity in (1) SN-MN synaptic facilitation and (2) memory for sensitization in Aplysia, by inhibiting MEK, the upstream kinase that phosphorylates and activates MAPK. In cellular experiments, we show that MAPK activity is required for ITF of tail SN-tail MN synapses, and, in parallel behavioral experiments, we show that ITM requires MAPK activity for its induction but not its expression. In contrast, short-term memory for sensitization does not require MAPK activity. Finally, 5-HT-induced LTF has been shown previously to require MAPK activity. Here we show that LTM for sensitization also requires MAPK activity. These results provide evidence that MAPK plays important roles specifically in long-lasting phases of synaptic plasticity and memory.

AB - The mitogen-activated protein kinase (MAPK) pathway has been implicated recently in synaptic plasticity and memory. Here we used tail shock-induced sensitization of the tail-elicited siphon withdrawal reflex in Aplysia to examine the role of MAPK in three different phases of memory. We show that a specific pattern of serotonin (5-HT) application that produces intermediate-term and long-term synaptic facilitation (ITF and LTF, respectively) of the sensory-motor (SN-MN) synapses in Aplysia leads to sustained activation of extracellular signal-regulated kinase in the ventrocaudal cluster sensory neurons (SNs), which include the tail SNs. Furthermore, repeated tail shocks that induce intermediate-term and long-term memory (ITM and LTM, respectively) for sensitization also lead to sustained MAPK activation in the SNs. Given these results, we next examined the requirement of MAPK activity in (1) SN-MN synaptic facilitation and (2) memory for sensitization in Aplysia, by inhibiting MEK, the upstream kinase that phosphorylates and activates MAPK. In cellular experiments, we show that MAPK activity is required for ITF of tail SN-tail MN synapses, and, in parallel behavioral experiments, we show that ITM requires MAPK activity for its induction but not its expression. In contrast, short-term memory for sensitization does not require MAPK activity. Finally, 5-HT-induced LTF has been shown previously to require MAPK activity. Here we show that LTM for sensitization also requires MAPK activity. These results provide evidence that MAPK plays important roles specifically in long-lasting phases of synaptic plasticity and memory.

KW - ERK

KW - Learning

KW - MAP kinase

KW - Memory

KW - Sensitization

KW - Synaptic facilitation

UR - http://www.scopus.com/inward/record.url?scp=0038206549&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0038206549&partnerID=8YFLogxK

M3 - Article

C2 - 12736359

AN - SCOPUS:0038206549

VL - 23

SP - 3899

EP - 3907

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 9

ER -