Analysis of Development of Direction Selectivity in Retinotectum by a Neural Circuit Model with Spike Timing-Dependent Plasticity

Abstract

The development of direction selectivity in the visual system depends on visual experience. In the developing Xenopus retinotectal system, tectal neurons (TNs) become direction selective through spike timing-dependent plasticity (STDP) after repetitive retinal exposure to a moving bar in a specific direction. We investigated the mechanism responsible for the development of direction selectivity in the Xenopus retinotectal system using a neural circuit model with STDP. In this retinotectal circuit model, a moving bar stimulated the retinal ganglion cells (RGCs), which provided feedforward excitation to the TNs and interneurons (INs). The INs provided delayed feedforward inhibition to the TNs. The TNs also received feedback excitation from neighboring TNs. As a synaptic learning rule, a molecular STDP model was used for synapses between the RGCs and TNs. The retinotectal circuit model reproduced experimentally observed features of the development of direction selectivity, such as increase in input to the TN. The peak of feedforward excitation from RGCs to TNs shifted earlier as a result of STDP. Together with the delayed feedforward inhibition, a stronger earlier transient feedforward signal was generated, which exceeded the threshold of the feedback excitation from the neighboring TNs and resulted in amplification of input to the TN. The suppression of the delayed feedforward inhibition resulted in the development of orientation selectivity rather than direction selectivity, indicating the pivotal role of the delayed feedforward inhibition in direction selectivity. We propose a mechanism for the development of direction selectivity involving a delayed feedforward inhibition with STDP and the amplification of feedback excitation.

The Spike-Timing Dependence of Plasticity

“…This asymmetrically expands the receptive field toward earlier-activated spatial locations (Engert et al, 2002). In a computational model, STDP at retinotectal synapses explained these findings (Honda et al, 2011). These results strongly suggest that natural motion stimuli drive emergence of motion direction tuning via STDP.…”

Refinement and Pattern Formation in Neural Circuits by the Interaction of Traveling Waves with Spike-Timing Dependent Plasticity

“…Here, the imaginary component gives rise to a spatial phase shift in w ( x ), a feature that has been exploited to drive a spatial redistribution of synaptic strengths by asymmetric STDP rules in several models of sequence learning [ 26 , 32 ], asymmetric shifts in hippocampal place fields [ 33 , 34 ], and the formation of direction selective cells [ 24 , 27 , 28 ].…”

“…However, the spatiotemporal correlations induced by traveling waves are space-time inseparable, providing additional information that may be utilized during circuit building. Space-time inseparable activity patterns map the temporal profile of the STDP rule into a spatial profile of synaptic strength changes [ 24 ], which can be used to build circuits that mimic neuronal sensitivity to visual motion during repeated exposure to moving visual stimuli [ 25 – 28 ]. But despite the demonstrated applicability of STDP to specific cases of neural circuit development, a more general, formal analysis of the interaction of STDP and wave-like activity patterns is still lacking.…”

Spike Timing-Dependent Plasticity

“…First, retinotectal synapses exhibit robust Hebbian STDP in vivo, by pairing either electrically or visually evoked presynaptic spikes with postsynaptic spikes (Zhang et al, 1998(Zhang et al, , 2000. In a recent computational model, STDP at retinotectal synapses was shown to explain all these findings (Honda et al, 2011). This is the hallmark of Hebbian STDP (Engert et al, 2002;Mu and Poo, 2006).…”