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

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 o...

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Bibliographic Details
Published in:Current biology 2011-11, Vol.21 (21), p.1773-1782
Main Authors: Shomrat, Tal, Graindorge, Nicolas, Bellanger, Cécile, Fiorito, Graziano, Loewenstein, Yonatan, Hochner, Binyamin
Format: Article
Language:English
Subjects:
Animals
brain
Brain - anatomy & histology
Brain - physiology
Cognitive science
correlation
Female
Ganglionic Blockers - pharmacology
Hexamethonium - pharmacology
Learning
Long-Term Potentiation
Male
Memory
molluscs
neurons
Neurons - drug effects
Neurons - physiology
Neuroscience
Octopodiformes - anatomy & histology
Octopodiformes - physiology
Octopus vulgaris
phylogeny
physiology
Sepia - anatomy & histology
Sepia - physiology
Sepia officinalis
Species Specificity
Synaptic Transmission
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Summary: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. 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. 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. ► Memory networks in octopus and cuttlefish have the same fan-out fan-in connectivity ► Surprisingly, the locus of synaptic plasticity in the two species is different ► In both species, the input-output relationship of the networks is linear ► Because of this linearity, the computation is indifferent to the locus of plasticity
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2011.09.011