Input Summation by Cultured Pyramidal Neurons Is Linear and Position-Independent

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Abstract
The role of dendritic morphology in integration and processing of neuronal inputs is still unknown. Models based on passive cable theory suggest that dendrites serve to isolate synapses from one another. Because of decreases in driving force or resistance, two inputs onto the same dendrite would diminish their joint effect, resulting in sublinear summation. When on different dendrites, however, inputs would not interact and therefore would sum linearly. These predictions have not been rigorously tested experimentally. In addition, recent results indicate that dendrites have voltage-sensitive conductances and are not passive cables. To investigate input integration, we characterized the effects of dendritic morphology on the summation of subthreshold excitatory inputs on cultured hippocampal neurons with pyramidal morphologies. We used microiontophoresis of glutamate to systematically position inputs throughout the dendritic tree and tested the summation of two inputs by measuring their individual and joint effects. We find that summation was surprisingly linear regardless of input position. For small inputs, this linearity arose because no significant shunts or changes in driving force occurred and no voltage-dependent channels were opened. Larger inputs also added linearly, but this linearity was caused by balanced action of NMDA and IApotassium conductances. Therefore, active conductances can maintain, paradoxically, a linear input arithmetic. Furthermore, dendritic morphology does not interfere with this linearity, which may be essential for particular neuronal computations.