Synaptic potentials and transfer functions of lamprey spinal neurons

Abstract

1. Electrotonic and chemical synaptic potentials were measured as a function of frequency of presynaptic action potentials. Over the frequency range from 0.02 to 10 Hz, the electrotonic synaptic potential was constant, while the chemical synaptic potential decreased in magnitude. Above 10 Hz, both synaptic events decreased in magnitude consistent with filtering by the dendritic structures. 2. Electrotonic synaptic transfer functions from 0.5 to 100 Hz were measured for the I ₁ reticulospinal Müller axon to spinal neuron electrotonic synaptic junction of the lamprey spinal cord using paired recordings from the pre-synaptic terminals and the post-synaptic neurons. In addition to this two-point synaptic transfer function, individual single point impedance functions of both the postsynaptic soma and the pre-synaptic axon terminal were measured. 3. The measured functions were interpreted with a computational model based on a three dimensional reconstruction of a Lucifer yellow filled motoneuron. Simulations of the model for a synaptic location of the I ₁, synapse were consistent with the measured synaptic transfer functions. 4. Synaptic potentials were simulated for inputs on dendrites near the I ₁ axon as well as distal dendritic regions. The high frequency filtering increased as the synaptic location was moved from the soma to the periphery, but the potential response on distal dendrites was larger than would have been predicted from the end of the equivalent cylinder of a Rall model that was used to fit soma impedance functions. 5. Electrotonic post-synaptic potentials were enhanced by the activation of a TTX-sensitive negative conductance. The algebraic addition of the increased negative conductance and all of the positive conductances led to a decreased net conductance, i.e. an increased impedance. Thus, the same synaptic current caused a larger potential response proportional to the neuronal impedance. Post-synaptic potentials computed from the transfer function data showed an enhancement with depolarization similar to that observed by direct measurement. 6. Thus, measurements of point and transfer impedances of central neurons, coupled with simulations allow a quantitative description of the cable properties of dendritic processes including both passive filtering and active voltagedependent properties that may enhance synaptic potentials.