Habituation in the Tail Withdrawal Reflex Circuit is Impaired During Aging in Aplysia californica

Kempsell, Andrew T.; Fieber, Lynne A.

doi:10.3389/fnagi.2016.00024

Cited by 9 publications

(4 citation statements)

References 47 publications

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“…LFI, as an operant paradigm ( Michel et al, 2011 ), is consistent with this pattern. In contrast, and more commonly reported, there are many other studies that assert cognition declines with age, including spatial learning in rats ( Adams et al, 2008 ); spatial, visual, and temporal learning in fish ( Yu et al, 2006 ; Terzibasi et al, 2008 ); sensitization and habituation in Aplysia ( Kempsell and Fieber, 2015 , 2016 ); electric shock avoidance, locomotion, geotaxis, and phototaxis in Drosophila ( Simon et al, 2006 ); and isothermal tracking in C. elegans ( Murakami and Murakami, 2005 ).…”

Section: Discussionmentioning

confidence: 99%

Improvements in operant memory of Aplysia are correlated with age and specific gene expression

Randolph,

Fieber

2023

Front. Behav. Neurosci.

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The transcription factor Aplysia CCAAT/enhancer binding protein (ApC/EBP) is expressed as an immediate early gene in the cAMP responsive element binding protein (CREB) mediated gene cascade, and it has essential functions in the synaptic consolidation of memory following a learning event. Synaptic consolidation primarily involves morphological changes at neuronal synapses, which are facilitated through the reorganization of the actin and microtubular cytoarchitecture of the cell. During early nervous system development, the transmembrane synaptic protein teneurin acts directly upon neuronal presynaptic microtubules and postsynaptic spectrin-based cytoskeletons to facilitate the creation of new synapses. It is reasonable to hypothesize that teneurin may also be linked to learning-induced synaptic changes and is a potential candidate to be a later gene expressed in the CREB-mediated gene cascade downstream of ApC/EBP. To assess the role of ApC/EBP and teneurin in learning and memory in the marine snail Aplysia californica, young (age 7–8 months) and aged (age 13–15 months; aging stage AII) siblings of Aplysia were trained in an operant conditioning paradigm—learning food is inedible (LFI)—over 2 days, during which they learned to modify the feeding reflex. Aged Aplysia had enhanced performance of the LFI task on the second day than younger siblings although far more aged animals were excluded from the analysis because of the initial failure in learning to recognize the inedible probe. After 2 days of training, ApC/EBP isoform X1 mRNA and teneurin mRNA were quantified in selected neurons of the buccal ganglia, the locus of neural circuits in LFI. Teneurin expression was elevated in aged Aplysia compared to young siblings regardless of training. ApC/EBP isoform X1 expression was significantly higher in untrained aged animals than in untrained young siblings but decreased in trained aged animals compared to untrained aged animals. Elevated levels of ApC/EBP isoform X1 and teneurin mRNA before training may have contributed to the enhancement of LFI performance in the aged animals that successfully learned.

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Section: Discussionmentioning

confidence: 99%

Improvements in operant memory of Aplysia are correlated with age and specific gene expression

Randolph,

Fieber

2023

Front. Behav. Neurosci.

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“…The post-training TWR response was assessed 20, 25 and 30 min after training in the same way as pre-training. This protocol is the same as that of another previous study investigating habituation of the TWR [ 57 ].…”

Section: Methodsmentioning

confidence: 99%

Neuromolecular mechanisms related to reflex behaviour in Aplysia are affected by ocean acidification

Sourisse,

Schunter

2024

R. Soc. Open Sci.

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While ocean acidification (OA) impacts the behaviour of marine organisms, the complexity of neurosystems makes linking behavioural impairments to environmental change difficult. Using a simple model, we exposed Aplysia to ambient or elevated CO 2 conditions (approx. 1500 µatm) and tested how OA affected the neuromolecular response of the pleural–pedal ganglia and caused tail withdrawal reflex (TWR) impairment. Under OA, Aplysia relax their tails faster with increased sensorin-A expression, an inhibitor of mechanosensory neurons. We further investigate how OA affects habituation training output, which produced a ‘sensitization-like’ behaviour and affected vesicle transport and stress response gene expression, revealing an influence of OA on learning. Finally, gabazine did not restore normal behaviour and elicited little molecular response with OA, instead, vesicular transport and cellular signalling link other neurotransmitter processes with TWR impairment. Our study shows the effects of OA on neurological tissue parts that control for behaviour.

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Section: Methodsmentioning

confidence: 99%

“…The posttraining TWR response was assessed 20, 25 and 30 min after training in the same way as pretraining. This protocol is the same as that of another previous study investigating habituation of the tail withdrawal reflex (46). To test if GABA-ergic neurotransmission is involved in observed behavioural impairments, Aplysia reared under near-future CO2 conditions (pCO2 ~ 1200 µatm) for seven days were either administered the GABAA receptor antagonist gabazine (4 mg/L of SR-95531, Sigma; n = 14), or control water solution (n = 16; Fig.…”

Section: Behavioural Assaysmentioning

confidence: 99%

Ocean acidification alters the transcriptomic response in the nervous system ofAplysia californicaduring reflex behaviour

Sourisse,

Schunter

2023

Preprint

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Ocean acidification (OA) has numerous impacts on marine organisms including behaviour. While behaviours are controlled in the neuro system, its complexity makes linking behavioural impairments to environmental change difficult. Here we use a neurological modelAplysia californicawith well-studied simple neuro system and behaviours. By exposingAplysiato current day (∼500 µatm) or near-future CO2conditions (∼1100 µatm), we test the effect of OA on their tail withdrawal reflex (TWR) and the underlying neuromolecular response of the pleural-pedal ganglia, responsible for the behaviour. Under OA,Aplysiarelax tails faster due to increased sensorin-A expression, an inhibitor of mechanosensory neurons. We further investigate how OA affects habituation, which produced a “sensitization-like” behaviour and affected vesicle transport and stress response, revealing an influence of OA on neuronal and behavioural outputs associated with learning. Finally, we test whether GABA-mediated neurotransmission is involved in impaired TWR, but exposure to gabazine did not restore normal behaviour and provoked little molecular response, rejecting the involvement in TWR impairment. Instead, vesicular transport and cellular signalling link other neurotransmitter processes directly with TWR impairment. Our study shows effects of OA on neurological tissue parts that control for behaviour revealing the neurological mechanisms when faced with OA.

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Habituation in the Tail Withdrawal Reflex Circuit is Impaired During Aging in Aplysia californica

Cited by 9 publications

References 47 publications

Improvements in operant memory of Aplysia are correlated with age and specific gene expression

Improvements in operant memory of Aplysia are correlated with age and specific gene expression

Neuromolecular mechanisms related to reflex behaviour in Aplysia are affected by ocean acidification

Ocean acidification alters the transcriptomic response in the nervous system ofAplysia californicaduring reflex behaviour

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