"Self" versus "non-self" connectivity dictates properties of synaptic transmission and plasticity

• Published in: PloS one 2013-04, Vol.8 (4), p.e62414-e62414
• Main Authors: Liu, Huisheng, Chapman, Edwin R, Dean, Camin
• Format: Article
• Language: English
• Subjects: Animals; Biology; Brain research; Cell Communication; Cell culture; Cells, Cultured; Embryo, Mammalian; Excitatory postsynaptic potentials; Excitatory Postsynaptic Potentials - physiology; Hippocampus - cytology; Hippocampus - embryology; Hippocampus - physiology; Innervation; Interneurons - cytology; Interneurons - physiology; Islands; Medicine; Neural networks; Neuronal Plasticity; Neurons; Neurosciences; Patch-Clamp Techniques; Plasticity; Protein synthesis; Rats; Rats, Wistar; Rodents; Short-term potentiation; Synapses; Synapses - physiology; Synaptic plasticity; Synaptic Transmission
• ISSN: 1932-6203; 1932-6203
• DOI: 10.1371/journal.pone.0062414

Autapses are connections between a neuron and itself. These connections are morphologically similar to "normal" synapses between two different neurons, and thus were long thought to have similar properties of synaptic transmission. However, this has not been directly tested. Here, using a micro-island culture assay in which we can define the number of interconnected cells, we directly compared synaptic transmission in excitatory autapses and in two-neuron micronetworks consisting of two excitatory neurons, in which a neuron is connected to one other neuron and to itself. We discovered that autaptic synapses are optimized for maximal transmission, and exhibited enhanced EPSC amplitude, charge, and RRP size compared to interneuronal synapses. However, autapses are deficient in several aspects of synaptic plasticity. Short-term potentiation only became apparent when a neuron was connected to another neuron. This acquisition of plasticity only required reciprocal innervation with one other neuron; micronetworks consisting of just two interconnected neurons exhibited enhanced short-term plasticity in terms of paired pulse ratio (PPR) and release probability (Pr), compared to autapses. Interestingly, when a neuron was connected to another neuron, not only interneuronal synapses, but also the autaptic synapses on itself exhibited a trend toward enhanced short-term plasticity in terms of PPR and Pr. Thus neurons can distinguish whether they are connected via "self" or "non-self" synapses and have the ability to adjust their plasticity parameters when connected to other neurons.