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Aging in Sensory and Motor Neurons Results in Learning Failure in Aplysia californica.

Kempsell AT, Fieber LA - PLoS ONE (2015)

Bottom Line: The physiological and molecular mechanisms of age-related memory loss are complicated by the complexity of vertebrate nervous systems.This implied that the neuronal machinery governing nonassociative learning was compromised during aging.Synaptic plasticity in the form of short-term facilitation between tail sensory and motor neurons decreased during aging whether the sensitizing stimulus was tail shock or the heterosynaptic modulator serotonin (5-HT).

View Article: PubMed Central - PubMed

Affiliation: University of Miami, Rosenstiel School of Marine and Atmospheric Science, Department of Marine Biology and Ecology, Miami, Florida, United States of America.

ABSTRACT
The physiological and molecular mechanisms of age-related memory loss are complicated by the complexity of vertebrate nervous systems. This study takes advantage of a simple neural model to investigate nervous system aging, focusing on changes in learning and memory in the form of behavioral sensitization in vivo and synaptic facilitation in vitro. The effect of aging on the tail withdrawal reflex (TWR) was studied in Aplysia californica at maturity and late in the annual lifecycle. We found that short-term sensitization in TWR was absent in aged Aplysia. This implied that the neuronal machinery governing nonassociative learning was compromised during aging. Synaptic plasticity in the form of short-term facilitation between tail sensory and motor neurons decreased during aging whether the sensitizing stimulus was tail shock or the heterosynaptic modulator serotonin (5-HT). Together, these results suggest that the cellular mechanisms governing behavioral sensitization are compromised during aging, thereby nearly eliminating sensitization in aged Aplysia.

No MeSH data available.


Related in: MedlinePlus

Schematic diagram of Aplysia illustrating regions of the tail subject to mechanical test stimulation and sensitizing electrical shocks.A) Behavioral experiments were performed in the intact animal. TWR amplitude and TWR duration were monitored in response to tail tap (75 g/mm2). After 3 baseline pretest taps, each animal received sensitization training consisting of five 1.5 sec, 100 mA shocks delivered to a site immediately posterior to the parapodial convergence. TWR amplitude and TWR duration in response to test tail tap were recorded 15, 30, 45, and 60 min after training and compared to baseline. B) Electrophysiological experiments consisted of a reduced preparation that involved the pleural-pedal ganglia, nerve P9, and attached tail. Tail SN and MN responses to mechanical tail tap were assessed before and after sensitization training as described in A.
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pone.0127056.g001: Schematic diagram of Aplysia illustrating regions of the tail subject to mechanical test stimulation and sensitizing electrical shocks.A) Behavioral experiments were performed in the intact animal. TWR amplitude and TWR duration were monitored in response to tail tap (75 g/mm2). After 3 baseline pretest taps, each animal received sensitization training consisting of five 1.5 sec, 100 mA shocks delivered to a site immediately posterior to the parapodial convergence. TWR amplitude and TWR duration in response to test tail tap were recorded 15, 30, 45, and 60 min after training and compared to baseline. B) Electrophysiological experiments consisted of a reduced preparation that involved the pleural-pedal ganglia, nerve P9, and attached tail. Tail SN and MN responses to mechanical tail tap were assessed before and after sensitization training as described in A.

Mentions: The same 18 animals were measured for sensitization in TWR at mature and aged II time points following previously defined protocols [16, 27]. An animal was placed on its foot in the center of the cage and allowed to acclimate for 5 min. The animal’s resting body length was measured with a ruler. A 500 ms tap to the tip of the tail at a stimulus pressure of 75 grams/mm2 caused tail withdrawal towards the center of the body and signified the start of the reflex. The retracted body length was then measured. The time to relax the tail to ~30% of original tail length was recorded, and signified the end of the reflex and the reflex duration. TWR amplitude was calculated as the fraction of starting body length withdrawn following tail touch. TWR amplitude and TWR duration were measured at 15, 10 and 5 min before sensitizing electrical shocks to the tail (-15, -10, -5 min) and the average of these 3 measurements was designated as baseline. Five minutes after the last baseline tail tap, sensitizing tail shocks were then delivered, consisting of five 1.5 sec, 100 mA electrical shocks, with an interstimulus interval of 1 sec, delivered to the tail immediately posterior to the parapodial convergence at a different site than that used to measure baseline TWR (Fig 1A). This site was ~2–3 cm anterior to the tip of the tail. Next, TWR was again elicited by tail tap 5, 15, 30, and 60 min following sensitizing shocks, and amplitude and duration were measured.


Aging in Sensory and Motor Neurons Results in Learning Failure in Aplysia californica.

Kempsell AT, Fieber LA - PLoS ONE (2015)

Schematic diagram of Aplysia illustrating regions of the tail subject to mechanical test stimulation and sensitizing electrical shocks.A) Behavioral experiments were performed in the intact animal. TWR amplitude and TWR duration were monitored in response to tail tap (75 g/mm2). After 3 baseline pretest taps, each animal received sensitization training consisting of five 1.5 sec, 100 mA shocks delivered to a site immediately posterior to the parapodial convergence. TWR amplitude and TWR duration in response to test tail tap were recorded 15, 30, 45, and 60 min after training and compared to baseline. B) Electrophysiological experiments consisted of a reduced preparation that involved the pleural-pedal ganglia, nerve P9, and attached tail. Tail SN and MN responses to mechanical tail tap were assessed before and after sensitization training as described in A.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4430239&req=5

pone.0127056.g001: Schematic diagram of Aplysia illustrating regions of the tail subject to mechanical test stimulation and sensitizing electrical shocks.A) Behavioral experiments were performed in the intact animal. TWR amplitude and TWR duration were monitored in response to tail tap (75 g/mm2). After 3 baseline pretest taps, each animal received sensitization training consisting of five 1.5 sec, 100 mA shocks delivered to a site immediately posterior to the parapodial convergence. TWR amplitude and TWR duration in response to test tail tap were recorded 15, 30, 45, and 60 min after training and compared to baseline. B) Electrophysiological experiments consisted of a reduced preparation that involved the pleural-pedal ganglia, nerve P9, and attached tail. Tail SN and MN responses to mechanical tail tap were assessed before and after sensitization training as described in A.
Mentions: The same 18 animals were measured for sensitization in TWR at mature and aged II time points following previously defined protocols [16, 27]. An animal was placed on its foot in the center of the cage and allowed to acclimate for 5 min. The animal’s resting body length was measured with a ruler. A 500 ms tap to the tip of the tail at a stimulus pressure of 75 grams/mm2 caused tail withdrawal towards the center of the body and signified the start of the reflex. The retracted body length was then measured. The time to relax the tail to ~30% of original tail length was recorded, and signified the end of the reflex and the reflex duration. TWR amplitude was calculated as the fraction of starting body length withdrawn following tail touch. TWR amplitude and TWR duration were measured at 15, 10 and 5 min before sensitizing electrical shocks to the tail (-15, -10, -5 min) and the average of these 3 measurements was designated as baseline. Five minutes after the last baseline tail tap, sensitizing tail shocks were then delivered, consisting of five 1.5 sec, 100 mA electrical shocks, with an interstimulus interval of 1 sec, delivered to the tail immediately posterior to the parapodial convergence at a different site than that used to measure baseline TWR (Fig 1A). This site was ~2–3 cm anterior to the tip of the tail. Next, TWR was again elicited by tail tap 5, 15, 30, and 60 min following sensitizing shocks, and amplitude and duration were measured.

Bottom Line: The physiological and molecular mechanisms of age-related memory loss are complicated by the complexity of vertebrate nervous systems.This implied that the neuronal machinery governing nonassociative learning was compromised during aging.Synaptic plasticity in the form of short-term facilitation between tail sensory and motor neurons decreased during aging whether the sensitizing stimulus was tail shock or the heterosynaptic modulator serotonin (5-HT).

View Article: PubMed Central - PubMed

Affiliation: University of Miami, Rosenstiel School of Marine and Atmospheric Science, Department of Marine Biology and Ecology, Miami, Florida, United States of America.

ABSTRACT
The physiological and molecular mechanisms of age-related memory loss are complicated by the complexity of vertebrate nervous systems. This study takes advantage of a simple neural model to investigate nervous system aging, focusing on changes in learning and memory in the form of behavioral sensitization in vivo and synaptic facilitation in vitro. The effect of aging on the tail withdrawal reflex (TWR) was studied in Aplysia californica at maturity and late in the annual lifecycle. We found that short-term sensitization in TWR was absent in aged Aplysia. This implied that the neuronal machinery governing nonassociative learning was compromised during aging. Synaptic plasticity in the form of short-term facilitation between tail sensory and motor neurons decreased during aging whether the sensitizing stimulus was tail shock or the heterosynaptic modulator serotonin (5-HT). Together, these results suggest that the cellular mechanisms governing behavioral sensitization are compromised during aging, thereby nearly eliminating sensitization in aged Aplysia.

No MeSH data available.


Related in: MedlinePlus