Novelty Enhances Visual Salience Independently of Reward in the Parietal Lobe

Abstract

Novelty modulates sensory and reward processes, but it remains unknown how these effects interact, i.e., how the visual effects of novelty are related to its motivational effects. A widespread hypothesis, based on findings that novelty activates reward-related structures, is that all the effects of novelty are explained in terms of reward. According to this idea, a novel stimulus is by default assigned high reward value and hence high salience, but this salience rapidly decreases if the stimulus signals a negative outcome. Here we show that, contrary to this idea, novelty affects visual salience in the monkey lateral intraparietal area (LIP) in ways that are independent of expected reward. Monkeys viewed peripheral visual cues that were novel or familiar (received few or many exposures) and predicted whether the trial will have a positive or a negative outcome-i.e., end in a reward or a lack of reward. We used a saccade-based assay to detect whether the cues automatically attracted or repelled attention from their visual field location. We show that salience-measured in saccades and LIP responses-was enhanced by both novelty and positive reward associations, but these factors were dissociable and habituated on different timescales. The monkeys rapidly recognized that a novel stimulus signaled a negative outcome (and withheld anticipatory licking within the first few presentations), but the salience of that stimulus remained high for multiple subsequent presentations. Therefore, novelty can provide an intrinsic bonus for attention that extends beyond the first presentation and is independent of physical rewards.Key words: intrinsic motivation; monkey; novelty; parietal; reward; salience IntroductionOne of the most remarkable abilities of the mammalian brain is its vast capacity to learn and acquire new information. An important ingredient of this ability is a novelty bias, whereby animals show preference over novel rather than familiar items (Brockmole and Henderson, 2005; Wittmann et al., 2008;Yang et al., 2009; Park et al., 2010;Liao et al., 2011). In humans, monkeys, and rats, novelty has widespread effects on sensory processing and motivation (Rainer and Miller, 2002;Düzel et al., 2010; Roozendaal and McGaugh, 2011), showing that understanding its neural coding is essential for understanding the control of learning and exploration.A central question in novelty research is how animals become motivated to explore novel items given that, by definition, they do not yet know the value of these items. One explanation, proposed in studies of reinforcement learning, is that the effects of novelty are explained in terms of reward. According to this idea, a novel stimulus is by default afforded high reward value but this salience is modified through learning, declining rapidly if the stimulus signals a negative outcome (Kakade and Dayan, 2002; Laurent, 2008). Consistent with this hypothesis, novelty activates the reward circuitry, including midbrain dopamine (DA) neurons in animals (Ljungberg et al., 1992; Horvitz, 2...

Parietal neurons encode expected gains in instrumental information

“…A second common interpretation of the LIP target selection response is in terms of a "priority" map that ranks competing visual cues for saccades or attention (14,33,(46)(47)(48)(49)(50)(51)(52). Similar to the value interpretation, the priority hypothesis describes LIP as encoding a common currency for visual selection.…”

Prediction suppression in monkey inferotemporal cortex depends on the conditional probability between images

“…Damped responding to predicted events is frequently observed at the level of perceptual, cognitive, and motivational systems (den Ouden et al 2012). Filtering out could be adaptive both in preventing the capture of attention by things that require no processing (Foley et al 2014) and in allowing the refinement of the very brain mechanisms that mediate prediction making. The idea that surprising events (prediction errors) fine tune the predictive apparatus lies at the heart of animal learning theory ( If prediction suppression indeed arises from the tendency of the visual system to filter out the representation of a predicted event, then it should be possible to reduce the strength of prediction suppression by reducing the predictability of the trailing image during training.…”

Organization and evolution of parieto-frontal processing streams in macaque monkeys and humans

“…Physiological studies indicate that the areas of this cluster are involved in directed visual attention (Bushnell et al, 1981;Lynch et al, 1977, area 7), saliency, including salient distractors (LIP; Bisley and Goldberg, 2010;Colby and Goldberg, 1999;Gottlieb et al, 1998;Qi et al, 2015;Suzuki and Gottlieb, 2013), novelty (LIP; Foley et al, 2014), and reorienting of attention (LIP; Steinmetz and Constantidinis, 1995). In LIP neurons with mirror properties (Shepherd et al, 2009) discharge when a monkey moves the focus of attention toward the cell's receptive field and when observing another monkey attending in the same direction.…”