Action Potential Reflection and Failure at Axon Branch Points Cause Stepwise Changes in EPSPs in a Neuron Essential for Learning

Abstract

In leech mechanosensory neurons, action potentials reverse direction, or reflect, at central branch points. This process enhances synaptic transmission from individual axon branches by rapidly activating synapses twice, thereby producing facilitation. At the same branch points action potentials may fail to propagate, which can reduce transmission. It is now shown that presynaptic action potential reflection and failure under physiological conditions influence transmission to the same postsynaptic neuron, the S cell. The S cell is an interneuron essential for a form of nonassociative learning, sensitization of the whole body shortening reflex. The P to S synapse has components that appear monosynaptic (termed "direct") and polysynaptic, both with glutamatergic pharmacology. Reflection at P cell branch points on average doubled transmission to the S cell, whereas action potential failure, or conduction block, at the same branch points decreased it by one-half. Each of two different branch points affected transmission, indicating that the P to S connection is spatially distributed around these branch points. This was confirmed by examining the locations of individual contacts made by the P cell with the S cell and its electrically coupled partner C cells. These results show that presynaptic neuronal morphology produces a range of transmission states at a set of synapses onto a neuron necessary for a form of learning. Reflection and conduction block are activity-dependent and are basic properties of action potential propagation that have been seen in other systems, including axons and dendrites in the mammalian brain. Individual branch points and the distribution of synapses around those branch points can substantially influence neuronal transmission and plasticity.

Information processing in the axon

“…Reflection (or reverse propagation) occurs when an action potential is near failure 105 . This form of axonal computation has been well described in leech mechanosensory neurons 75,76 (FIG. 8) in which an unexpected event occurs when conduction nearly becomes blocked -the action potential that has nearly failed to invade the thick branch of the principal axon sets up a local potential that propagates backwards.…”

“…Axonal propagation might also 'bounce back' at a branch point or at the cell body. However, at present, only a handful of examples of reflected propagation have been observed 75,76,87,108,121 . Reflected impulses might limit the spread of the neuronal message and enhance synaptic transmission.…”

“…When the action potential fails to propagate along the axon, no signal can reach the output of the cell. Conduction failure filters communication with postsynaptic neurons, and has been observed experimentally in various axons including vertebrate spinal axons 68,69 , spiny lobster or crayfish motor neurons 33,64,70,71 , leech mechanosensory neurons [72][73][74][75][76] , thalamocortical axons 77 , rabbit nodose ganglion neurons 78 , rat dorsal root ganglion neurons 63,79 , neurohypophysial axons 17,80 and hippocampal pyramidal cells 39,66,81 . Several factors determine whether propagation along axons fails or succeeds.…”

“…Reflection also occurs in T cells 75 . Interestingly, the facilitation of synaptic transmission also affects the chemical synapse between the P cell and the S neuron, a neuron that has an essential role in sensitization, a non-associative form of learning 76 . Reflected propagation is not restricted to mechanosensory neurons of the leech but has also been observed in the axon of an identified snail neuron 87 .…”

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

“…The S-and C-cells are electrically coupled and EPSPs elicited in the C-cell are carried to the S-cell with little attenuation, essentially acting as monosynaptic EPSPs (Muller and Scott, 1981) and will referred to as such. The P-cells elicit a glutamatergic EPSP onto the S-cell of 1-5 mV in amplitude that has both monosynaptic and polysynaptic components (Baccus et al, 2000). Most of the monosynaptic contacts by the P-cell are on the coupling interneuron, but a few synapses terminate directly onto the S-cell (Baccus et al, 2000).…”