Alternative Sites of Synaptic Plasticity in Two Homologous “Fan-out Fan-in” Learning and Memory Networks

BACKGROUND To what extent are the properties of neuronal networks constrained by computational considerations? Comparative analysis of the vertical lobe (VL) system, a brain structure involved in learning and memory, in two phylogenetically close cephalopod mollusks, Octopus vulgaris and the cuttlefish Sepia officinalis, provides a surprising answer to this question. RESULTS We show that in both the octopus and the cuttlefish the VL is characterized by the same simple fan-out fan-in connectivity architecture, composed of the same three neuron types. Yet, the sites of short- and long-term synaptic plasticity and neuromodulation are different. In the octopus, synaptic plasticity occurs at the fan-out glutamatergic synaptic layer, whereas in the cuttlefish plasticity is found at the fan-in cholinergic synaptic layer. CONCLUSIONS Does this dramatic difference in physiology imply a difference in function? Not necessarily. We show that the physiological properties of the VL neurons, particularly the linear input-output relations of the intermediate layer neurons, allow the two different networks to perform the same computation. The convergence of different networks to the same computational capacity indicates that it is the computation, not the specific properties of the network, that is self-organized or selected for by evolutionary pressure.