Goldberg J I, Lukowiak K
J Neurobiol. 1984 Nov;15(6):395-411. doi: 10.1002/neu.480150602.
Habituation of the Aplysia gill-withdrawal reflex (and siphon-withdrawal reflex) has been attributed to low-frequency homosynaptic depression at central sensory-motor synapses. The recent demonstration that transfer of habituation between stimulation sites occurs in this model system has prompted the hypothesis that heterosynaptic inhibitory pathways also play a role in the mediation of habituation behavior. To test this hypothesis, the sites and mechanisms of neural plasticity which underlie transfer of habituation in Aplysia were examined. Transfer of habituation is a reduction in the reflex evoked at one stimulation site (siphon) due to repeated presentation of a stimulus to a second site (gill). Centrally mediated transfer of habituation, measured in a preparation lacking the siphon-gill peripheral nervous system (PNS), was associated with a reduced excitatory response in central motor neurons. Repeated tactile stimulation of the gill did not attenuate the gill response evoked by electrical stimulation of the branchial nerve nor the mechanoreceptor response recorded in LE sensory neurons. In contrast, repeated stimulation of siphon or gill at a site which was "off" the sensory field of a specific mechanoreceptor led to a diminution in synaptic transmission between that sensory neuron and its followers (motor neurons and inter-neurons). These data demonstrate that centrally mediated transfer of habituation results from heterosynaptic modulation of synaptic transmission at the sensory-motor (and sensory-interneuron) synapses. Therefore, habituation behavior in Aplysia is mediated through the conjoint action of homosynaptic and heterosynaptic inhibitory processes.
海兔鳃收缩反射（以及虹吸管收缩反射）的习惯化被认为是由于中枢感觉运动突触处的低频同突触抑制。最近在这个模型系统中发现习惯化可以在刺激位点之间转移，这促使人们提出假说，即异突触抑制通路在习惯化行为的介导中也起作用。为了验证这一假说，研究了海兔中习惯化转移所基于的神经可塑性位点和机制。习惯化转移是指由于对第二个位点（鳃）重复施加刺激，导致在一个刺激位点（虹吸管）诱发的反射减弱。在缺乏虹吸管 - 鳃外周神经系统（PNS）的标本中测量的中枢介导的习惯化转移，与中枢运动神经元兴奋性反应的降低有关。对鳃进行反复触觉刺激，并不会减弱由鳃神经电刺激诱发的鳃反应，也不会减弱在LE感觉神经元中记录到的机械感受器反应。相反，在特定机械感受器的感觉场“之外”的位点对虹吸管或鳃进行反复刺激，会导致该感觉神经元与其后续神经元（运动神经元和中间神经元）之间的突触传递减弱。这些数据表明，中枢介导的习惯化转移是由感觉运动（以及感觉 - 中间神经元）突触处突触传递的异突触调制引起的。因此，海兔的习惯化行为是通过同突触和异突触抑制过程的联合作用介导的。
