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The Journal of Neuroscience, April 21, 2004, 24(16):4011-4019; doi:10.1523/JNEUROSCI.0178-04.2004

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Behavioral/Systems/Cognitive
Multiple Forms of Long-Term Potentiation and Long-Term Depression Converge on a Single Interneuron in the Leech CNS

Brian D. Burrell and Christie L. Sahley

Department of Biological Sciences, Purdue University, West Lafayette, Indiana 47907

Long-term potentiation (LTP) of synaptic transmission was observed in two types of synapses that converge on the same postsynaptic neuron in the leech CNS. These synapses were made by identifiable sensory neurons, the mechanosensory touch (T-) and pressure (P-) cells, onto the S-cell, an interneuron critical for certain forms of learning. Changes in both the T-S and P-S synapses appear to be activity dependent because LTP was restricted to inputs that had undergone tetanization; however, properties of synaptic plasticity at the T-S and P-S connections differ considerably. At the P-S synapse, LTP was induced in the tetanized synapse but not in the nontetanized synapse tested in parallel. P-S LTP was blocked by the NMDA receptor antagonist DL-2-amino-5-phosphono-valeric acid (AP-5) or by lowering the extracellular concentration of glycine, an NMDA receptor (NMDAR) co-agonist. P-S LTP was strongly affected by the initial amplitude of the synaptic potential at the time LTP was induced. Smaller amplitude synapses (<3.5 mV) underwent robust potentiation, whereas the less common, larger amplitude synapse (>3.5 mV) depressed after tetanization. At the T-S synapse, tetanization simultaneously induced homosynaptic LTP in the tetanized input and heterosynaptic long-term depression (LTD) in the input made by a nontetanized T-cell onto the same S-cell. Interestingly, AP-5 failed to block homosynaptic LTP at the T-S synapse but did prevent heterosynaptic LTD. T-S LTP was not affected by the initial EPSP amplitude. Thus, leech neurons exhibit synaptic plasticity with properties similar to LTP and LTD found in the vertebrate nervous system.

View larger version (35K): [in this window] [in a new window]   Figure 2. Experimental setup and recordings from presynaptic and postsynaptic neurons during the delivery of a single tetanus. A, A suction electrode was applied to the DP nerve to co-tetanize the dorsal P- and T-cells (highlighted) selectively without activating the other T- and P-cells in the ganglion (shaded) that do not have processes in the DP nerve. The subscripts represent lateral (L), ventral (V), and dorsal (D) and indicate receptive fields in the skin that each sensory neuron innervates. B, Sample recordings from the dorsal P- and T-cells, from the postsynaptic S-cell, and from an N-cell and a Retzius cell (which also have processes in the DP nerve) during delivery of a single tetanus.

 

Key words: long-term potentiation; long-term depression; leech; synaptic plasticity; learning; NMDA

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Received Aug 4, 2003; revised March 18, 2004; accepted March 18, 2004.

This article has been cited by other articles:

				K. B. Grey and B. D. Burrell Forskolin Induces NMDA Receptor-Dependent Potentiation at a Central Synapse in the Leech J Neurophysiol, May 1, 2008; 99(5): 2719 - 2724. [Abstract] [Full Text] [PDF]

				D. L. Glanzman The Cellular Mechanisms of Learning in Aplysia: Of Blind Men and Elephants Biol. Bull., June 1, 2006; 210(3): 271 - 279. [Abstract] [Full Text] [PDF]

				K. M. Crisp and K. J. Muller A 3-synapse positive feedback loop regulates the excitability of an interneuron critical for sensitization in the leech. J. Neurosci., March 29, 2006; 26(13): 3524 - 3531. [Abstract] [Full Text] [PDF]

				B. D. Burrell and C. L. Sahley Serotonin Mediates Learning-Induced Potentiation of Excitability J Neurophysiol, December 1, 2005; 94(6): 4002 - 4010. [Abstract] [Full Text] [PDF]

				B. L. Moss, A. D. Fuller, C. L. Sahley, and B. D. Burrell Serotonin Modulates Axo-Axonal Coupling Between Neurons Critical for Learning in the Leech J Neurophysiol, October 1, 2005; 94(4): 2575 - 2589. [Abstract] [Full Text] [PDF]

				L. Blackburn LEARNING WITH LEECHES J. Exp. Biol., September 1, 2004; 207(17): iv - iv. [Full Text] [PDF]

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