Emergence of connectivity motifs in networks of model neurons with short- and long-term plastic synapses

PLoS One. 2014 Jan 15;9(1):e84626. doi: 10.1371/journal.pone.0084626. eCollection 2014.


Recent experimental data from the rodent cerebral cortex and olfactory bulb indicate that specific connectivity motifs are correlated with short-term dynamics of excitatory synaptic transmission. It was observed that neurons with short-term facilitating synapses form predominantly reciprocal pairwise connections, while neurons with short-term depressing synapses form predominantly unidirectional pairwise connections. The cause of these structural differences in excitatory synaptic microcircuits is unknown. We show that these connectivity motifs emerge in networks of model neurons, from the interactions between short-term synaptic dynamics (SD) and long-term spike-timing dependent plasticity (STDP). While the impact of STDP on SD was shown in simultaneous neuronal pair recordings in vitro, the mutual interactions between STDP and SD in large networks are still the subject of intense research. Our approach combines an SD phenomenological model with an STDP model that faithfully captures long-term plasticity dependence on both spike times and frequency. As a proof of concept, we first simulate and analyze recurrent networks of spiking neurons with random initial connection efficacies and where synapses are either all short-term facilitating or all depressing. For identical external inputs to the network, and as a direct consequence of internally generated activity, we find that networks with depressing synapses evolve unidirectional connectivity motifs, while networks with facilitating synapses evolve reciprocal connectivity motifs. We then show that the same results hold for heterogeneous networks, including both facilitating and depressing synapses. This does not contradict a recent theory that proposes that motifs are shaped by external inputs, but rather complements it by examining the role of both the external inputs and the internally generated network activity. Our study highlights the conditions under which SD-STDP might explain the correlation between facilitation and reciprocal connectivity motifs, as well as between depression and unidirectional motifs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Humans
  • Nerve Net
  • Neuronal Plasticity*
  • Neurons / physiology*
  • Synapses / physiology*

Grants and funding

This work was partly supported by the European Commission (FP7 Marie Curie Initial Training Network “NAMASEN,” grant n. 264872, http://cordis.europa.eu/fp7; the Future Emerging Technology programme project “BRAINLEAP” grant n. 306502, http://cordis.europa.eu/fp7/ict/fet-open) and by the Royal Society (travel grant JP091330-2009/R4, http://royalsociety.org). MG also acknowledges additional support from the Flemish agency for Innovation by Science and Technology (grant n. 90455/1955, http://www.iwt.be) and from the Interuniversity Attraction Poles Program (IUAP), initiated by the Belgian Science Policy Office (http://www.belspo.be); EV acknowledges additional support from the Engineering and Physical Sciences Research Council (grant n. EP/J019534/1 and e-futures award EFXD12003/EFXD12004, http://efutures.ac.uk/xd). Access to the supercomputer facilities CalcUA (University of Antwerp) and Tier 1 (Flemish Supercomputer Center - VSC) is warmly acknowledged. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.