Sensory adaptation as an optimal redistribution of neural resources
Sergei Gepshtein
Category:
Biology of Perception
Introduction. It has been proposed that sensory
adaptation optimizes visual sensitivity to properties of the variable
environment (Sakitt and Barlow, 1982; Wainwright, 1999). On this view, motion
adaptation is expected to improve the ability to perceive motion at the
adapting conditions. Yet experimental evidence of motion adaptation has been
controversial. In speed adaptation, for example, sensitivity to adapting speeds
can either increase or decrease; it can also change for speeds very different
from the adapting speed (Krekelberg, van Wezel, and Albright, 2006). We
presently test a normative theory of motion adaptation which implements the
premise that motion adaptation improves the ability to perceive motion in a new
environment but which also predicts that (a) sensitivity to motion must
deteriorate at some adapting conditions, and (b) adaptation-induced changes are
global so increments and decrements of sensitivity are expected also away from
the adapting conditions.
Theory. According to a new normative-economic
theory of motion perception (Gepshtein, Tyukin, and Kubovy, 2007),
spatiotemporal sensitivity manifests an optimal allocation of limited resources
(such as motion-sensitive cells) to conditions of visual stimulation. The
allocation is optimal in two respects. First, it balances the errors of
estimating stimulus location and stimulus content, satisfying the uncertainty
principle of measurement (Gabor, 1946). Second, it places more resources at the
conditions where the resources are more likely to be used, by taking into
account the statistics of visual stimulation. The theory predicts that motion
adaptation should induce a characteristic pattern of changes in the
spatiotemporal contrast sensitivity function (Kelly, 1979), forming
well-defined foci of increased and decreased sensitivity across a map of
sensitivity to spatial and temporal frequencies of stimulation.
Experiments. We tested the predictions by measuring
human contrast sensitivity over a large range of spatial and temporal
frequencies (0.25-8 c/deg and 0.5-32 Hz). The observers viewed drifting
luminance gratings of variable contrast and discriminated the direction of
motion. We varied the statistics of motion speed: In some blocks of trials low
speeds were more common than high speeds, and in other blocks high speeds were
more common than low speeds. To rapidly measure the entire contrast sensitivity
function in both statistical contexts, we used a novel adaptive procedure that
combined Bayesian adaptive inference with a trial-to-trial information-gain
strategy (Lesmes, Lu, Baek, and Albright, 2008). We compared the spatiotemporal sensitivity
functions obtained in the different statistical contexts and found that
sensitivity changed similar to our predictions. The changes were global and
they formed foci of increased and decreased sensitivity, so the map of observed
changes was similar to the map of predicted changes.
Conclusions. These findings support the normative-economic theory and the view that motion adaptation amounts to reallocation of neural computational resources in the visual system: The allocation of sensitivity takes into account both the uncertainty principle of measurement and the statistics of stimulation. Since computational resources of the visual system are limited, improvement of sensitivity to some stimuli is accompanied by deterioration of sensitivity to other stimuli.