Are photoreceptors in the attention spotlight? Efferent neuromodulators accelerate and/or retard the time course of photoreceptor responses evoked by light

Abstract

Change blindness can be modified by selective attention so that stimuli that are otherwise too fast or too slow become visible. This fact has always been consistent with the idea that attention might operate on the timing of photoreceptor responses. But, to our knowledge, this idea was not explored even though photoreceptors clearly limit the temporal bandwidth of vision.

We now report that neuromodulators released by efferents from the brain modify the temporal properties of photoreceptor responses. This discovery leads to a further development of the spotlight theory of attention; it implicates efferents to photoreceptors as candidate neural components of the spotlight.

We reached this conclusion by executing two types of experiments on the influence of neuromodulation on the timing of photoreceptor potentials (RPs). In one type, intracellular microelectrodes were used to record from single receptor cells residing in eye slices perfused in vitro with neuromodulators. In the other type, electroretinograms (ERGs) with a clear photoreceptor component were obtained in vivo from intact animals while efferent neuromodulation was manipulated. The logic of this approach is that the in vitro RP data directly demonstrate the effects of modulation at the cellular level in a highly reduced preparation while the in vivo ERG data determine whether these effects are physiological and natural.

Converging evidence from virtually intact living animals indicated that various methods of mobilizing efference all affect the timing of receptor responses. No matter whether efference is produced by electrical stimulation of efferent fibers or whether the activity of these fibers is modified by variation in the time of day or whether an efferent neuromodulator is infiltrated into the eye, the result patterns are always the same: ERG indicators of photoreceptor timing clearly change in ways that are linked to both efference and to the RP timing changes that occur under perfusion of eye slices in vitro.