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PART 4: BEHAVIORAL PLASTICITY #21: LEARNING & MEMORY of a SIMPLE REFLEX in APLYSIA II. model system: sea hare ( Aplysia californica ) behavior: the gill & siphon withdrawal reflex even more cell biology: learning & memory summary. PART 4: BEHAVIORAL PLASTICITY

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Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

PART 4: BEHAVIORAL PLASTICITY

#21: LEARNING & MEMORY of a SIMPLE REFLEX in APLYSIA II

  • model system: sea hare (Aplysia californica)

  • behavior: the gill & siphon withdrawal reflex

  • even more cell biology: learning & memory

  • summary


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

PART 4: BEHAVIORAL PLASTICITY

#21: LEARNING & MEMORY of a SIMPLE REFLEX in APLYSIA II

  • model system: sea hare (Aplysia californica)

  • behavior: the gill & siphon withdrawal reflex

  • even more cell biology: learning & memory

  • summary


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

    • convergence of CS & US in sensory neuron

    • adenylyl cyclase (AC) = coincidence detector?

    • sensitization:

      • Ca++ channels closed

      • Ca++not bound to calmodulin

      • calmodulin not bound to AC

      • some cAMP ...


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

    • convergence of CS & US in sensory neuron

    • adenylyl cyclase (AC) = coincidence detector?

    • associative learning:

      • Ca++ channels open

      • Ca++ bound to calmodulin

      • calmodulin bound to AC

      • lots of cAMP ...


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • glutamate, excitatory transmitter

    • activates N-methyl-D-aspartate (NMDA) receptor


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • glutamate, excitatory transmitter

    • activates N-methyl-D-aspartate (NMDA) receptor

    • no signal...

      • NMDA channel closed

      • no Ca++ enters cell


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • glutamate, excitatory transmitter

    • activates N-methyl-D-aspartate (NMDA) receptor

    • signal...

      • glutamate binds to receptor

      • postsynaptic membrane

        depolarizes

      • postsynaptic neuron fires

      • test this model?


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • differential conditioning


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • differential conditioning

    • aminophosphonovalerate

      (APV) block of NMDA receptor…


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • differential conditioning

    • block NMDA receptor with APV during training


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • differential conditioning

    • block NMDA receptor with APV during training

    • associative synaptic facilitation 


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • differential conditioning

    • block NMDA receptor with APV during training

    • associative synaptic facilitation 

    • NMDA receptor necessary


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • differential conditioning

    • same result during training if

      • postsynaptic neuron:

        • hyperpolarized

        • Ca++ blocked

      • presynaptic neuron:

        • PKA blocked

        • Ca++ 


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • postsynaptic factors

    • implication that the postsynaptic neuron communicates with the presynaptic neuron

    • retrograde (backward) signaling

    • evidence (not shown) – associative facilitation mechanism in postsynaptic neuron changes signaling properties in the presynaptic neuron

    • neurons communicate in both directions

    • but... what is the signal?


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • revised model

    • 2 sites of CS-US coincidence

      • presynaptic AC


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • revised model

    • 2 sites of CS-US coincidence

      • presynaptic AC

      • postsynaptic

        NMDA receptor

        gated channels


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of classical conditioning

  • revised model

    • 2 sites of CS-US coincidence

      • presynaptic AC

      • postsynaptic

        NMDA receptor

        gated channels

    • retrograde signal

      (hypothetical)


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

  • terminology:

    • long-term memory (LTM) behavioral measure

    • long-term facilitation (LTF) physiological measure


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • distributed sensitization training


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • distributed sensitization training:

      • siphon withdrawal 


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • distributed sensitization training

      • siphon withdrawal 

      • sensory EPSPs 


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • distributed sensitization training

      • siphon withdrawal 

      • sensory EPSPs 

      • S-current 

        (data not given)


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • distributed sensitization training

      • siphon withdrawal 

      • sensory EPSPs 

      • S-current 

      • serotonin-induced

        presynaptic transmitter release 

        (data not given)


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • distributed sensitization training

      • siphon withdrawal 

      • sensory EPSPs 

      • S-current 

      • serotonin-induced

        presynaptic transmitter release 

        (data not given)

      • presynaptic neuronal plasticity


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • distributed sensitization training

      • serotonin substitutes for tail shock @ sensory

        • cell body  LTF

        • terminal  STF


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • distributed sensitization training

      • serotonin substitutes for tail shock @ sensory

        • cell body  LTF

        • terminal  STF


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • serotonin induces

      • LTF

        • intracellular signal

        • protein synthesis (?)

        • neural plasticity (?)

      • STF

        • locally @ synapse


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • protein synthesis (?)

      • transcription

      • translation

      • transport  synapses


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • protein synthesis inhibited by blockers

    • also block LTF

      • during serotonin application only

      • not before or after...

      • narrow temporal window


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • protein synthesis inhibited by blockers

    • also block LTF

      • during serotonin application only

      • not before or after...

      • narrow temporal window

    • no block of STF


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term synaptic facilitation in sensory neurons

    • protein synthesis inhibited by blockers

    • also block LTF

      • during serotonin application only

      • not before or after...

      • narrow temporal window

    • no block of STF

    • ... and does block LTM (behavior)

    • protein synthesis necessary for LTM


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term sensitization / serotonin treatments  molecular changes in sensory neurons:

    • persistent phosphorylation of existing proteins

    • synthesis of new proteins

    • growth of sensory neurons... neural plasticity


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term sensitization / serotonin treatments  molecular changes in sensory neurons:

    • growth of sensory neurons... neural plasticity

      • visual examination

      •  axonal processes,

        branching, varicosities


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term sensitization / serotonin treatments  molecular changes in sensory neurons:

    • growth of sensory neurons... neural plasticity

      • visual examination

      •  axonal processes,

        branching, varicosities


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term sensitization / serotonin treatments  molecular changes in sensory neurons:

    • growth of sensory neurons... neural plasticity

      • model for synaptic restructuring / plasticity

      •  varicosities

      •  terminal active zones

      • opposite for habituation


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • long-term sensitization / serotonin treatments  molecular changes in sensory neurons:

    • growth of sensory neurons... neural plasticity

      • model for synaptic restructuring / plasticity

      •  varicosities

      •  terminal active zones

    •  long-term increase in synaptic transmission

    • what are the molecular mechanisms?


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • molecular induction of LTF in sensory neurons

    • cAMP pathway implicated:

      • cAMP injection ... S-current 

      • PKA inhibitors ... block serotonin-induced LTF

      • serotonin application ... PKA catalytic subunit cytoplasmic  nuclear

      • activity of genes:

        • immediate early (IEG), transcription factors

        • late-responsive, leave nucleus


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • molecular induction of LTF in sensory neurons

    • cAMP pathway implicated:

    • cAMP response elements (CREs) on DNA

    • CRE binding protein (CREB)

    • phosphorylated by PKA...

      CREBs  IEGs

    • IEGs  late-responsive genes


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • molecular induction of LTF in sensory neurons

    • single training event  some PKA, STF

    • distributed training  more PKA... nucleus, LTF


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • molecular induction of LTF in sensory neurons

    • competition studies using injected CRE sequences  block CREB binding & LTF 


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • molecular induction of LTF in sensory neurons

    • competition studies using injected CRE sequences  block CREB binding & LTF 


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • molecular induction of LTF in sensory neurons

    • competition studies using injected CRE sequences  block CREB binding & LTF 

    • enhanced CREB + 1 serotonin application 

      • LTF

      • structural enhancement

    • CREB essential for LTF & LTM

    • similar findings in Drosophila (next chapter)


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • mechanistic analysis of long-term memory

  • LTF molecular model

    • what proteins?

    • how do they work?

    • other 2nd messenger

      cascades?

    • homology (flies, mice)


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

CELL BIOLOGY OF LEARNING & MEMORY

  • middle-term memory... read the section on your own


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

SUMMARY

  • defensive withdrawal reflex after stimulation (CS) of

    • siphon, mantle, gill

  • shows non-associative learning properties

    • habituation, dishabituation, sensitization

  • sensitization: reflex with preceding tail shock

  • associative learning

    • reflex (CS) + paired shock (US)

    • differential conditioning = CS1+ + US, CS2–

  • distributed training  long-term memory


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

SUMMARY

  • tail shock sensitization

    • interneuron serotonin release  sensory neuron

    •  K current flow (out of cell)

    • spike broadening

    • synaptic facilitation

    • cAMP cascade mediated

    • sensory neuron transmitter release


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

SUMMARY

  • classical conditioning

    • interneuron serotonin release  sensory neuron

    • tail shock US responses augmented by concurrent CS signal...

    • activity-dependent presynaptic facilitation

    • postsynaptic process, NMDA receptor in motor neuron


Model system sea hare aplysia californica behavior the gill siphon withdrawal reflex

SUMMARY

  • long-term memory

    • dispersed training

    • protein synthesis-dependent

    • cAMP & CREB  IEGs

    • IEGs  late-response genes

    • proteins  neuron terminals

    • neuronal plasticity