Reward sharpens orientation coding independently on attention

Rewarding improves performance. Is it due to modulations of the output modules of the neural systems or are there mechanisms favoring more generous inputs? Some recent study included V1 in the the circuitry of reward-based modulations, but the effects of reward can easily be confused with effects of attention. Here we address this issue with a psychophysical dual task to control attention while orientation sensitivity on targets associated to different levels of reward is measured. We found that different reward rates improve orientation discrimination and sharpen the internal response distributions. Data are unaffected by changing attentional load nor by dissociating the feature of the reward cue from the feature relevant for the task. This suggests that reward may act independently on attention by modulating the activity of early sensory stages, perhaps V1, through a SNR improvement of task-relevant channels. Reward acts like attention, but using separate channels. “Gold? Yellow, glittering, precious gold? No, Gods, I am no idle votarist! ... Thus much of this will make black white, foul fair, Wrong right, base noble, old young, coward valiant. ... Why, this” (Shakespeare in Timon of Athens, 1623) The activity of the visual channels, both at the neuronal and at the overall behavioral level, can be modulated by virtue of several sources of influence. Many such modulatory activities depend on the global behavioral state of the organism, driven by cognitive, emotional or motivational factors. Since these states have a profound impact on the behavioral performance of the individuals, determining successes or failures of goal-directed behavior, their mechanisms of action have attracted the interests of psychologists, cognitive neuroscientists and neurophysiologists for long time. Attention and reward are among the most studied modulating factors of behavior and have traditionally been investigated independently from one another. In general, as we refer to modulations of the sensory systems and of perceptual performance, the idea of attention is more often reflecting fast, short-term modulation based on exogenous or endogenous cues to bias the processing power toward specific spatial location or stimulus features. Reward of specific actions or classes of stimuli is instead investigated assuming that it exerts long-term effects on sensory channels; these effects would alter the learning process toward specific stimuli or classes of stimuli and/or responses. Moreover, selective attention has been often studied in its relations to changes of the early stages of the input-output flow of information processing, with an active effort of finding neural correlates of attention in the Visual Area V41-3, V23, 4, V15, 6 and as early as in the LGN7, 8. On the other hand, reward has been widely studied as a variable affecting the later stages, closer to mechanisms related to visual-motor transformations9, to the decision-making modules10, 11 and to the overt behavior12. More recently a number of studies have shifted the focus backward in the attempt of seeking the effect of reward to purely sensory areas, opening new doors for re-framing the functional properties of the early visual modules13-15. However, since reward is a built-in feature of the neurophysiological paradigms of attention, focusing on the early effects of reward has the implicit risks of confusing the effects of reward with those of attention16. Moreover, recent proposals have raised the idea that perceptual performance can be modulated by reward through its action on the attentional system17, implying that attention has a monopoly over the modulation of perception. Here we specifically address the functional liaison between attention and reward by investigating whether the probability of reward may become associated to a change of perceptual performance when attention is engaged in a concurrent task and learning is prevented by making the reward value associated to specific stimuli contingent on a trial-to-trial base. We have used a recently introduced psychophysical paradigm18 to measure orientation discrimination acuity for a simple peripheral target (a task assumed to summon early mechanisms19, 20) and to obtain at once a quantitative estimate of the observer s noisy internal response distributions for any physical value of the target. Attention was controlled through the use of a concurrent task of varying difficulty, that has the key potential of showing independence of resources21, while learning could be excluded based on the fact that the same stimulus and the same response could be associated to one of two probabilities of obtaining reward (0.9 present/0.1 absent Vs 0.1 present/0.9 absent) unpredictably at each trial based on a precue (see Fig. 1). We found that a higher likelihood of earning credit to obtain a Scratch & Win ticket, a highly efficient and effective reward even in non-gamblers, improved performance. In particular, higher reward rates produced finer orientation acuity, as revealed by lower thresholds (about 50% decrease), and this was possibly due to a significant change of the channel s Signal-to-Noise Ratio (SNR), as revealed by sharper response distributions when the reward was more likely to be achieved. The reward-based modulation was unaffected by whether the orientation task was performed in isolation or it was competing with a central task of varying difficulty. Moreover, the effect was dissociated from the nature of the cue, as it remained stable when the cue was modulated in the colour domain and the task in the orientation domain. Our results are coherent with the possibility that attention and reward may act independently to modulate perceptual performance and offer novel insights for studying reward and attention measuring their effect independently in the context of the same experimental paradigm.