DIFFERENTIAL SIGNALING VIA THE SAME AXON OF NEOCORTICAL PYRAMIDAL NEURONS

The nature of information stemming from a single neuron and conveyed s imultaneously to several hundred target neurons is not known. Triple a nd quadruple neuron recordings revealed that each synaptic connection established by neocortical pyramidal neurons is potentially unique. Sp ecifically, synaptic connections onto the same morphological class dif fered in the numbers and dendritic locations of synaptic contacts, the ir absolute synaptic strengths, as well as their rates of synaptic dep ression and recovery from depression. The same axon of a pyramidal neu ron innervating another pyramidal neuron and an interneuron mediated f requency-dependent depression and facilitation, respectively, during h igh frequency discharges of presynaptic action potentials, suggesting that the different natures of the target neurons underlie qualitative differences in synaptic properties. Facilitating-type synaptic connect ions established by three pyramidal neurons of the same class onto a s ingle interneuron, were all qualitatively similar with a combination o f facilitation and depression mechanisms. The time courses of facilita tion and depression, however, differed for these convergent connection s, suggesting that different pre-postsynaptic interactions underlie qu antitative differences in synaptic properties. Mathematical analysis o f the transfer functions of frequency-dependent synapses revealed supr alinear, linear, and sub-linear signaling regimes in which mixtures of presynaptic rates, integrals of rates, rind derivatives of rates are transferred to targets depending on the precise values of the synaptic parameters and the history of presynaptic action potential activity. Heterogeneity of synaptic transfer functions therefore allows multiple synaptic representations of the same presynaptic action potential tra in and suggests that these synaptic representations are regulated in a complex manner. It is therefore proposed that differential signaling is a key mechanism in neocortical information processing, which can be regulated by selective synaptic modifications.