Insights from the Study of Simple Animals
Progress in analyzing the mechanisms of learning and memory in the vertebrate nervous system has been hindered by the enormous complexity of the brain. Consequently, many neuroscientists have turned to the study of selected invertebrates in order to exploit their relatively simple nervous systems and large, identifiable neurons that are accessible for detailed anatomical, biophysical, biochemical, and molecular studies.
One animal that is well suited for the examination of the molecular, cellular, morphologic, and network mechanisms underlying neuronal plasticity and learning and memory is the marine mollusk Aplysia. Neurons and neural circuits that mediate many behaviors in Aplysia have been identified. In several cases, these behaviors have been shown to be modified by learning. Moreover, specific loci within neural circuits at which modifications occur during learning have been identified, and aspects of the cellular mechanisms underlying these modifications have been analyzed and modeled (for reviews, see Byrne et al., 1993; Byrne and Kandel, 1996; Hawkins et al., 1993). Defensive reflexes in Aplysia (Fig. 4A) exhibit three forms of nonassociative learning: habituation, dishabituation, and sensitization. A single sensitizing stimulus can produce an enhancement that lasts minutes (short-term sensitization), whereas more prolonged
61. Learning and Memory training (e.g., multiple stimuli) produces an enhancement that lasts days to weeks (long-term sensitization). Aplysia also exhibits classical conditioning and operant conditioning.
A prerequisite for the analysis of the neural and molecular basis of these different forms of learning is an understanding of the neural circuit that controls the behavior. The afferent limb of the withdrawal reflex in Fig. 4A consists of sensory neurons with somata in the central nervous system. The sensory neurons (SNs) monosynap-tically excite motor neurons (MNs) that are also located in the central nervous system (Fig. 4B). Activation of the motor neurons leads to contraction of the peripheral muscle and the subsequent withdrawal response. Excitatory and inhibitory interneurons in the withdrawal circuit have also been identified, although these inter-neurons are not illustrated in Fig. 4B. The sensory neurons appear to be important plastic elements in the neural circuits. Changes in their membrane properties and the strength of their synaptic connections (synaptic efficacy) are associated with sensitization.
Cellular Mechanisms in Sensory Neurons Contributing to Short- and Long-Term Sensitization in Aplysia
Short-term sensitization is induced when a single brief train of shocks to the body wall results in the release of modulatory transmitters, such as serotonin (5-HT), from a separate class of interneurons (INs) referred to as facilitatory neurons (Fig. 4B). These facilitatory neurons regulate the properties of the sensory neurons and the strength of their connections with postsynaptic inter-neurons and motor neurons, a process called hetero-synaptic facilitation (Fig. 4C). The molecular mechanisms contributing to heterosynaptic facilitation are illustrated in Fig. 5. Serotonin binds to at least two types of receptors on the outer surface of the membrane of the sensory neurons. The binding of 5-HT to one class of receptors leads to the activation of adenylyl cyclase, which in turn, leads to an elevation of the intracellular level of the second-messenger adenosine-3' ,5'-monophosphate (cyclic adenosine monophosphate, or cAMP) in sensory
A2. Withdrawn xTail
Skin (sensory input)
Skin (sensory input)
Muscle (reflex response)
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