Normalization by valence and motivational intensity in the sensorimotor cortices (PMd, M1, and S1)

Our brain’s ability to represent vast amounts of information, such as continuous ranges of reward spanning orders of magnitude, with limited dynamic range neurons, may be possible due to normalization. Recently our group and others have shown that the sensorimotor cortices are sensitive to reward value. Here we ask if psychological affect causes normalization of the sensorimotor cortices by modulating valence and motivational intensity. We had two non-human primates (NHP) subjects (one male bonnet macaque and one female rhesus macaque) make visually cued grip-force movements while simultaneously cueing the level of possible reward if successful, or timeout punishment, if unsuccessful. We recorded simultaneously from 96 electrodes in each the following: caudal somatosensory, rostral motor, and dorsal premotor cortices (cS1, rM1, PMd). We utilized several normalization models for valence and motivational intensity in all three regions. We found three types of divisive normalized relationships between neural activity and the representation of valence and motivation, linear, sigmodal, and hyperbolic. The hyperbolic relationships resemble receptive fields in psychological affect space, where a unit is susceptible to a small range of the valence/motivational space. We found that these cortical regions have both strong valence and motivational intensity representations.

Pleasure, reward value and prediction error in anhedonia

In order to develop effective treatments for anhedonia we need to understand its underlying neurobiological mechanisms. Anhedonia is conceptually strongly linked to reward processing, which involves a variety of cognitive and neural operations. This article reviews the evidence for impairments in experiencing hedonic response (pleasure), reward valuation, and reward learning based on outcomes (commonly conceptualised in terms of “reward prediction error”). Synthesizing behavioural and neuroimaging findings, we examine case-control studies of patients with depression and schizophrenia, including those focusing specifically on anhedonia. Overall, there is reliable evidence that depression and schizophrenia are associated with disrupted reward processing. In contrast to the historical definition of anhedonia, there is surprisingly limited evidence for impairment in the ability to experience pleasure in depression and schizophrenia. There is some evidence that learning about reward and reward prediction error signals are impaired in depression and schizophrenia, but the literature is inconsistent. The strongest evidence is for impairments in the representation of reward value and how this is used to guide action. Future studies would benefit from focusing on impairments in reward processing specifically in anhedonic samples, including transdiagnostically, and from using designs separating different components of reward processing, formulating them in computational terms, and moving beyond cross-sectional designs to provide an assessment of causality.

Fractionating the reward-memory literature: Instructed, item-related feedback, and item-unrelated feedback

Over the last two decades, nearly one hundred studies have been published examining reward influences on memory. Implementations of reward-value procedures have varied markedly, as have other study characteristics, including images vs. words, intentional vs. incidental memory encoding, and recall vs. recognition tests. As such, the resulting state of the field has become unwieldy and somewhat difficult to identify consistent reward-memory effects from those that are inconsistent due to critical differences in the study methods. Here we provide an overview of these studies and fractionate their methods into three distinct procedures: instructed, item-related feedback, and item-unrelated feedback. Instructed studies tell participants of item-value associations during encoding with rewards earned during memory retrieval. In contrast, feedback studies ask participants to make responses during encoding, with rewards provided as feedback; memory retrieval itself is unrewarded. Some feedback studies require participants to make responses related to the to-be-remembered items, while others require participants to respond to an initial prompt before presenting an unrelated stimulus. While both procedures involve feedback, the first set of studies involves item-related feedback, and the second set has item-unrelated feedback. By fractionating the reward-memory literature into distinct procedures, an otherwise heterogenous mixture of study design characteristics becomes much more interpretable and the underlying cognitive mechanisms more clear. This additional clarity should improve predictions for future studies, as this framework helps identify which prior findings are more relevant, while also providing a summary of the current state of the field.

Sex differences in behavioral responding and dopamine release during early Pavlovian learning

Learning associations between cues and rewards requires the mesolimbic dopamine system. The dopamine response to cues signals differences in reward value in well-trained animals. These value-related dopamine responses are absent during early learning when cues signal differences in the reward rate, which suggests cue-evoked dopamine release conveys differences between outcomes only after extensive training. However, it is unclear if this lack of value coding by cue-evoked dopamine release during early learning is unique to when cues signal differences in reward rate, or if this is also evident when cues signal differences in other value-related parameters such as reward size. To address this, we utilized a Pavlovian conditioning task in which one audio cue was associated with a small reward (one pellet) and another audio cue was associated with a large reward (three pellets). We performed fast-scan cyclic voltammetry to record changes in dopamine release in the nucleus accumbens of male and female rats throughout early learning. Cue-evoked dopamine release did not encode differences in reward value, and there were no differences in this response between males and females. However, female rats exhibited higher levels of conditioned responding and a faster latency to respond. Reward-evoked dopamine release scaled with reward size in both sexes, though there were transient sex differences in the dynamics of this response. We additionally identified sex differences in the number of post-reward head entries. Collectively these data illustrate sustained sex differences in behavioral responding as well as transient sex differences in reward-evoked dopamine release.

Differential effects of intra-modal and cross-modal reward value on visual perception: ERP evidence

Stimuli associated with high reward modulate perception and such value-driven effects have been shown to originate from the modulation of the earliest stages of sensory processing in the brain. In natural environments objects comprise multiple features (imagine a rolling soccer ball, with its black and white patches and the swishing sound made during its motion), where each feature may signal different associations with previously encountered rewards. How perception of such an object is affected by the value associations of its constituent parts is unknown. The present study compares intra- and cross-modal value-driven effects on behavioral and electrophysiological correlates of visual perception. Human participants first learned the reward associations of visual and auditory cues. Subsequently, they performed a visual orientation discrimination task in the presence of previously rewarded visual or auditory cues (intra- and cross-modal cues, respectively) that were concurrently presented with the target stimulus. During the conditioning phase, when reward associations were learned and reward cues were the target of the task, reward value of both modalities enhanced the electrophysiological correlates of sensory processing in visual cortex. During the post-conditioning phase, when reward delivery was halted and previously rewarded stimuli were task-irrelevant, cross-modal value-enhanced behavioral measures of visual sensitivity whereas intra-modal value led to a trend for suppression. A similar pattern of modulations was found in the simultaneously recorded event-related potentials (ERPs) of posterior electrodes. We found an early (90-120 ms) suppression of ERPs evoked by high-value, intra-modal stimuli. Cross-modal cues led to a later value-driven modulation, with an enhancement of response positivity for high- compared to low-value stimuli starting at the N1 window (180-250 ms) and extending to the P3 (300-600 ms) responses of the posterior electrodes. These results indicate that visual cortex is modulated by the reward value of visual as well as auditory cues. Previously rewarded, task-irrelevant cues from the same or different sensory modality have a different effect on visual perception, as intra-modal high-value cues may interfere with the target processing, whereas cross-modal high-value cues boost the perception of the target.

Exploring reward-related attention selectivity deficits in Parkinson’s disease

An important aspect of managing a limited cognitive resource like attention is to use the reward value of stimuli to prioritize the allocation of attention to higher-value over lower-value stimuli. Recent evidence suggests this depends on dopaminergic signaling of reward. In Parkinson’s disease, both reward sensitivity and attention are impaired, but whether these deficits are directly related to one another is unknown. We tested whether Parkinson’s patients use reward information when automatically allocating their attention and whether this is modulated by dopamine replacement. We compared patients, tested both ON and OFF dopamine replacement medication, to older controls using a standard attention capture task. First, participants learned the different reward values of stimuli. Then, these reward-associated stimuli were used as distractors in a visual search task. We found that patients were generally distracted by the presence of the distractors but that the degree of distraction caused by the high-value and low-value distractors was similar. Furthermore, we found no evidence to support the possibility that dopamine replacement modulates the effect of reward on automatic attention allocation. Our results suggest a possible inability in Parkinson’s patients to use the reward value of stimuli when automatically allocating their attention, and raise the possibility that reward-driven allocation of resources may affect the adaptive modulation of other cognitive processes.

Sugars and Sweet Taste: Addictive or Rewarding?

The notion of food “addiction” often focuses on the overconsumption of sweet tasting foods or so-called sugar “addiction”. In the extreme, some have suggested that sugar and sweet tastes elicit neural and behavioral responses analogous to those observed with drugs of abuse. These concepts are complicated by the decades long uncertainty surrounding the validity and reproducibility of functional magnetic resonance imaging (fMRI) methodologies used to characterize neurobiological pathways related to sugar and sweet taste stimuli. There are also questions of whether sweet taste or post-ingestion metabolic consequences of sugar intake would lead to addiction or excessive caloric intake. Here, we present a focused narrative review of literature related to the reward value of sweet taste which suggests that reward value can be confounded with the construct of “addictive potential”. Our review seeks to clarify some key distinctions between these constructs and questions the applicability of the addiction construct to human over-eating behaviors. To adequately frame this broad discussion requires the flexibility offered by the narrative review paradigm. We present selected literature on: techniques used to link sugar and sweet tastes to addiction neurobiology and behaviors; sugar and sweet taste “addiction”; the relationship of low calorie sweetener (LCS) intake to addictive behaviors and total calorie intake. Finally, we examined the reward value of sweet tastes and contrasted that with the literature describing addiction. The lack of reproducibility of fMRI data remains problematic for attributing a common neurobiological pathway activation of drugs and foods as conclusive evidence for sugar or sweet taste “addiction”. Moreover, the complicated hedonics of sweet taste and reward value are suggested by validated population-level data which demonstrate that the consumption of sweet taste in the absence of calories does not increase total caloric intake. We believe the neurobiologies of reward value and addiction to be distinct and disagree with application of the addiction model to sweet food overconsumption. Most hypotheses of sugar “addiction” attribute the hedonics of sweet foods as the equivalent of “addiction”. Further, when addictive behaviors and biology are critically examined in totality, they contrast dramatically from those associated with the desire for sweet taste. Finally, the evidence is strong that responses to the palatability of sweets rather than their metabolic consequences are the salient features for reward value. Thus, given the complexity of the controls of food intake in humans, we question the usefulness of the “addiction” model in dissecting the causes and effects of sweet food over-consumption.

Coherent theta activity in the medial and orbital frontal cortices encodes reward value

This study examined how the medial frontal (MFC) and orbital frontal (OFC) cortices process reward information. We simultaneously recorded local field potentials in the two areas as rats consumed liquid sucrose rewards. Both areas exhibited a 4–8 Hz ‘theta’ rhythm that was phase-locked to the lick cycle. The rhythm tracked shifts in sucrose concentrations and fluid volumes, demonstrating that it is sensitive to differences in reward magnitude. The coupling between the rhythm and licking was stronger in MFC than OFC and varied with response vigor and absolute reward value in the MFC. Spectral analysis revealed zero-lag coherence between the cortical areas, and found evidence for a directionality of the rhythm, with MFC leading OFC. Our findings suggest that consummatory behavior generates simultaneous theta range activity in the MFC and OFC that encodes the value of consumed fluids, with the MFC having a top-down role in the control of consumption.