Cellular correlates of long-term sensitization in Aplysia - PubMed (original) (raw)
Cellular correlates of long-term sensitization in Aplysia
L J Cleary et al. J Neurosci. 1998.
Abstract
Although in vitro analyses of long-term changes in the sensorimotor connection of Aplysia have been used extensively to understand long-term sensitization, relatively little is known about the ways in which the connection is modified by learning in vivo. Moreover, sites other than the sensory neurons might be modified as well. In this paper, several different biophysical properties of sensory neurons, motor neurons, and LPl17, an identified interneuron, were examined. Membrane properties of sensory neurons, which were expressed as increased excitability and increased spike afterdepolarization, were affected by the training. The biophysical properties of motor neurons also were affected by training, resulting in hyperpolarization of the resting membrane potential and a decrease in spike threshold. These results suggest that motor neurons are potential loci for storage of the memory in sensitization. The strength of the connection between sensory and motor neurons was affected by the training, although the connection between LPl17 and the motor neuron was unaffected. Biophysical properties of LPl17 were unaffected by training. The results emphasize the importance of plasticity at sensory-motor synapses and are consistent with the idea that there are multiple sites of plasticity distributed throughout the nervous system.
Figures
Fig. 1.
Behavioral training protocol. A dorsal view of the animal is illustrated in A. Thin silver electrodes were implanted bilaterally under the skin of the tail for delivery of weak test stimuli. Strong sensitizing stimuli were delivered to one side of the body wall (hatched area) through a hand-held spanning electrode. Baseline responsiveness of the siphon withdrawal component of the reflex was determined during a pretraining test period (B). Test stimuli consisted of a single weak AC shock of 20 msec duration. These were delivered alternately to the left and right sides of the animal at 5 min intervals, totaling five tests per side. During the subsequent training session, sensitizing stimuli were delivered as four trains of strong AC shocks separated by 30 min. Each train consisted of 10 pulses of 500 msec duration delivered at 1 Hz. At 24 hr after the training session the testing protocol was repeated.
Fig. 2.
Schematic representation of the neural circuits underlying the tail-elicited tail–siphon withdrawal reflex. Stimulation of the tail of the animal activates sensory neurons (SN) located in the pleural ganglion. These neurons activate motor neurons (MN) in the pedal ganglion that produce tail withdrawal. In addition, sensory neurons activate a polysynaptic pathway that projects to the abdominal ganglion, resulting in siphon withdrawal. The interneuron (IN) LPl17 is an element of this pathway.
Fig. 3.
Long-term sensitization training increased the duration of the tail-induced siphon withdrawal reflex. The duration of siphon withdrawal observed during the post-training tests was expressed as a percentage of the pretest duration. Learning was assessed by comparing the normalized duration on the trained side of the animal (Sensitized) with that on the contralateral untrained side (Control).
Fig. 4.
Long-term sensitization produced changes in three biophysical properties of tail sensory neurons: excitability (A), the amplitude of the afterdepolarization that follows a 1 sec, 2 nA depolarization (B), and the amplitude of the afterdepolarization that follows a 50 msec, 0.5 nA depolarization (C). In Panels 1 (top), recordings from both control and sensitized animals are shown. In Panels 2(bottom), the group data are shown. In _B_and C, the examples were chosen to emphasize the differences.
Fig. 5.
Long-term sensitization produced changes in two biophysical properties of tail motor neurons: resting membrane potential (A) and threshold for spike initiation (B). In Panels 1(top), recordings from both control and sensitized animals are shown. In Panels 2 (bottom), the group data are shown. In B1, the threshold for each neuron is illustrated by a solid line. The solid line in the Control trace was extended by a_dashed line_ to facilitate comparison. Note that threshold was defined as the largest depolarization that did not initiate a spike. Therefore, threshold was not determined from these traces.
Fig. 6.
Long-term sensitization training increased synaptic strength between sensory and motor neurons. Recordings of EPSPs evoked in motor neurons by sensory neurons are shown in_A_. In this experiment the motor neurons were held at −80 mV. For the purposes of comparing group data, the EPSC was calculated by normalizing the EPSP by the input resistance of the motor neuron.
Fig. 7.
The amplitude of the EPSC from ganglia from the sensitized side was correlated with the duration of withdrawal after sensitization training (r = 0.59). Duration was expressed as a percentage of the pretest duration. Values <100% indicate that the animal was not sensitized.
Fig. 8.
Training had no effect on the amplitude of the slow EPSP evoked in the motor neuron by LPl17. Recording of slow EPSPs evoked in ganglia from control (top) and sensitized (bottom) sides of the animal are illustrated in_A_. Because it was difficult to control the number of spikes generated in LPl17 by a given current pulse, several slow EPSPs were evoked by depolarizations of different amplitudes. The amplitude of the slow EPSP was plotted against the number of spikes elicited in LPl17. The slope of the regression line (mV/spike) over the linear range was used to compare ganglia from control and sensitized sides. The relationships for the two preparations shown in A_are illustrated in B. The slopes of the regression lines are 0.112 mV/spike (Control) and 0.123 mV/spike (Sensitized). Group data are illustrated in_C.
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References
- Baxter DA, Byrne JH. Serotonergic modulation of two potassium currents in the pleural sensory neurons of Aplysia. J Neurophysiol. 1989;62:665–679. - PubMed
- Buonomano DV, Cleary LJ, Byrne JH. Inhibitory neuron produces heterosynaptic inhibition of the sensory-to-motor neuron synapse in Aplysia. Brain Res. 1992;577:147–150. - PubMed
- Byrne JH, Shapiro E, Dieringer N, Koester J. Biophysical mechanisms contributing to inking behavior in Aplysia. J Neurophysiol. 1979;42:1233–1250. - PubMed
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