Abstract
We studied how a neuronal circuit composed of two neuron types connected by chemical and electrical synapses maintains constant its integrative capacities as neurons grow. For this we combined electrophysiological experiments with mathematical modeling in pairs of electrically-coupled Retzius neurons from postnatal to adult leeches. The electrically-coupled dendrites of both Retzius neurons receive a common chemical input, which produces excitatory postsynaptic potentials (EPSPs) with varying amplitudes. Each EPSP spreads to the soma, but also crosses the electrical synapse to arrive at the soma of the coupled neuron. The leak of synaptic current across the electrical synapse reduces the amplitude of the EPSPs in proportion to the coupling ratio. In addition, summation of EPSPs generated in both neurons generates the baseline action potentials of these serotonergic neurons. To study how integration is adjusted as neurons grow, we first studied the characteristics of the chemical and electrical connections onto the coupled dendrites of neuron pairs with soma diameters ranging from 21 to 75 μm. Then by feeding a mathematical model with the neuronal voltage responses to pseudorandom noise currents we obtained the values of the coupling ratio, the membrane resistance of the soma (rm) and dendrites (rdend), the space constant (λ) and the characteristic dendritic length (L = l/λ). We found that the EPSPs recorded from the somata were similar regardless on the neuron size. However, the amplitude of the EPSPs and the firing frequency of the neurons were inversely proportional to the coupling ratio of the neuron pair, which also was independent from the neuronal size. This data indicated that the integrative constancy relied on the passive membrane properties. We show that the growth of Retzius neurons was compensated by increasing the membrane resistance of the dendrites and therefore the λ value. By solely increasing the dendrite resistance this circuit maintains constant its integrative capacities as its neurons grow.
Highlights
Many neuronal circuits are fully functional at birth, long before the brain reaches its final dimensions
The overall electrical activity recorded from nine pairs of these Retzius neurons with average soma diameters between 21 and 75 μm was similar to that already described in adult neurons (Hagiwara and Morita, 1962), consisting of a resting potential between −55 and −60 mV, on top of which pairs of excitatory postsynaptic potentials (EPSPs) appeared simultaneously in both somata with amplitudes that varied randomly between neurons and from one pair to the (Figures 3A–C), suggesting presynaptic stepwise variations in transmitter release (DeMiguel et al, 2001)
The microcircuit established by electrically-coupled Retzius neurons and their chemical input maintains its integrative properties as the neuronal soma of neurons triples its diameter during growth
Summary
Many neuronal circuits are fully functional at birth, long before the brain reaches its final dimensions. Growth and Electrical Properties in Electrically-Coupled Neurons other hand, circuits that are well-preserved from one species to another display wide size differences in adult specimens, for example, certain neurons performing the same function in mice or elephants have radically different dimensions In all these cases the electrical properties of neurons and their connectivity must compensate the progressive expansion of the soma, dendrites and axons. Before birth Retzius neurons already formed their known chemical and electrical synapses (Reese and Drapeau, 1988; Todd et al, 2010; Baker and Macagno, 2014) and at the time of birth their arborization pattern is already remarkably similar to that in the adult nervous system (Jellies et al, 1987) Using this neuronal circuit we measured the different variables contributing to synaptic integration of Retzius neurons with soma sizes ranging from 21 to 75 μm.
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