Push-Pull Receptive Field Organization and Synaptic Depression: Mechanisms for Reliably Encoding Naturalistic Stimuli in V1

Figure 3

Figure 3. Spiking model of the early visual system. (A) The stimulus was modeled as a sequence of frames presented at 150 Hz (grating stimulus shown here). (B) Model of the visual thalamus (lateral geniculate nucleus “LGN”). ON and OFF center cell populations were modeled by linear spatiotemporal receptive fields followed by a non-linear spike generation mechanism. Thalamo-cortical synapses implemented short-term depression (feedforward depression). (C) Prototypic recurrent network model of layer 4 in the cat primary visual cortex “V1” with correlation-based connectivity implementing the push-pull receptive field organization. Inputs from the LGN provide direct excitatory (push). In cat V1, inhibitory neurons project preferentially to neurons having a receptive field phase difference of around 180°, effectively implementing the push-pull inhibition. Note also the intracortical reciprocal inhibition between inhibitory I1 and I2 neurons (Kayser and Miller, 2002) and the intracortical excitatory amplification for E1 and E2 neurons. Neurons were modeled as conductance based leaky-integrate-and-fire neurons. (D) Level of contrast invariant orientation tuning of the model in the complete parameter space of feedforward depression (τrec) and push-pull inhibition (inhibitory gain). Orientation tuning curves of example parameter combinations (S1–S4) at different contrast values (gray = low contrast, black = high contrast). S1 = model without push-pull inhibition and feedforward depression; S2 = model with feedforward depression; S3 = model with push-pull inhibition; S4 = model with push-pull inhibition and feedforward depression.

Neurons in the primary visual cortex are known for responding vigorously but with high variability to classical stimuli such as drifting bars or gratings. By contrast, natural scenes are encoded more efficiently by sparse and temporal precise spiking responses. We used a conductance-based model of the visual system in higher mammals to investigate how two specific features of the thalamo-cortical pathway, namely push-pull receptive field organization and fast synaptic depression, can contribute to this contextual reshaping of V1 responses. By comparing cortical dynamics evoked respectively by natural vs. artificial stimuli in a comprehensive parametric space analysis, we demonstrate that the reliability and sparseness of the spiking responses during natural vision is not a mere consequence of the increased bandwidth in the sensory input spectrum. Rather, it results from the combined impacts of fast synaptic depression and push-pull inhibition, the later acting for natural scenes as a form of "effective" feed-forward inhibition as demonstrated in other sensory systems. Thus, the combination of feedforward-like inhibition with fast thalamo-cortical synaptic depression by simple cells receiving a direct structured input from thalamus composes a generic computational mechanism for generating a sparse and reliable encoding of natural sensory events.


All material (c) L. Perrinet. Please check the copyright notice.

This work was supported by European integrated project FP6-015879, "FACETS".

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