Short-Term Attractive Tilt Aftereffects Predicted by a Recurrent Network Model of Primary Visual Cortex.

Maria Del Mar Quiroga,Bart Krekelberg,Adam P Morris

doi:10.3389/fnsys.2019.00067

Abstract

Adaptation is a multi-faceted phenomenon that is of interest in terms of both its function and its potential to reveal underlying neural processing. Many behavioral studies have shown that after exposure to an oriented adapter the perceived orientation of a subsequent test is repulsed away from the orientation of the adapter. This is the well-known Tilt Aftereffect (TAE). Recently, we showed that the dynamics of recurrently connected networks may contribute substantially to the neural changes induced by adaptation, especially on short time scales. Here we extended the network model and made the novel behavioral prediction that the TAE should be attractive, not repulsive, on a time scale of a few 100 ms. Our experiments, using a novel adaptation protocol that specifically targeted adaptation on a short time scale, confirmed this prediction. These results support our hypothesis that recurrent network dynamics may contribute to short-term adaptation. More broadly, they show that understanding the neural processing of visual inputs that change on the time scale of a typical fixation requires a detailed analysis of not only the intrinsic properties of neurons, but also the slow and complex dynamics that emerge from their recurrent connectivity. We argue that this is but one example of how even simple recurrent networks can underlie surprisingly complex information processing, and are involved in rudimentary forms of memory, spatio-temporal integration, and signal amplification.

Highlights

In a broad sense, sensory adaptation is the phenomenon that perception depends on the current stimulus, and what was presented before
We studied the dynamics of orientation-tuned units in a recurrently connected network model without any form of plasticity and showed that this model quantitatively captured the tuning shifts observed in monkey and cat V1 (Quiroga et al, 2016)
We first present model simulations based on macaque V1 responses that lead to the prediction of a short-term attractive Tilt Aftereffect (TAE), and the results of a set of psychophysical experiments that test and confirm the prediction in human observers

Summary

Introduction

Sensory adaptation is the phenomenon that perception depends on the current stimulus, and what was presented before. Adaptation is found across a wide range of time scales, from contrast adaptation occurring within a few hundreds of milliseconds (Shapley and Victor, 1978; Heinrich and Bach, 2001) to slow serial dependence spanning beyond seconds (Chopin and Mamassian, 2012; Fischer and Whitney, 2014) These behavioral phenomena are of interest in terms of their function, and as a tool to gain insight into the underlying neural mechanisms. We focus on visual adaptation on the timescale of a few 100 ms This has high ecological relevance as it corresponds to the typical duration of a single fixation in the primate. In behavioral experiments with such an adaptation protocol, subjects typically report that the test orientation is more different from the adapter than

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