Nucleus Accumbens Activity Dissociates Different Forms of Salience: Evidence from Human Intracranial Recordings

Abstract

Theoretical models and empirical work indicate a critical role of the NAcc in salience processing. For instance, the NAcc not only responds to appetitive and aversive information, but it also signals novelty, contextual deviance, and action monitoring. However, because most studies have investigated only one specific type of salience independently, it remains unclear how the NAcc concurrently differentiates between different forms of salience. To investigate this issue, we used intracranial electroencephalography in human epilepsy patients together with a previously established visual oddball paradigm. Here, three different oddball categories (novel, neutral, and target images) were infrequently presented among a standard scene image, and subjects responded to the target via button press. This task allowed us to differentiate "item novelty" (new vs neutral oddballs) from "contextual deviance" (neutral oddballs vs standard images) and "targetness" (target vs neutral oddballs). Time-frequency analysis revealed a dissociation between item novelty and contextual deviance on the basis of decreases in either (4 -8 Hz) or ␤ power (20 -30 Hz). Targetness, on the other hand, was signaled by positive deflections in the stimulus-locked local field potentials, which, importantly, correlated with subjects' reaction times. These findings indicate that, in an ongoing stream of information, the NAcc differentiates between types of salience by distinct neural mechanisms to guide goal-directed behavior.

Representations of Distinct Salience Signals in the Nucleus Accumbens

“…This hypothesis is consistent with emerging evidence suggesting that while highfrequency oscillations (for example gamma, 30 -90 Hz) index local neural computations, lower frequency oscillations (Ͻ30 Hz) may be the product of longer-range interactions (for review, see Donner and Siegel, 2011). Thus, we speculate that change in theta and beta oscillations (both Ͻ30 Hz) in response to item novelty and contextual deviance in the NAcc may index long-range interactions between NAcc and other brain regions.…”

“…Given that distinct brain networks are thought to code different salience signals, and that the NAcc is a locus of convergence for a diverse set of inputs (Goto and Grace, 2008), we speculate that the observed frequency-specific oscillatory patterns in the NAcc might arise from interactions with separate brain networks. This hypothesis is consistent with emerging evidence suggesting that while highfrequency oscillations (for example gamma, 30 -90 Hz) index local neural computations, lower frequency oscillations (Ͻ30 Hz) may be the product of longer-range interactions (for review, see Donner and Siegel, 2011).…”

“…Finally, a large literature has shown that engagement of the mesolimbic dopamine system, specifically midbrain projections to the NAcc, is critical in initiating motivated/adaptive behavior. In fact, VTA/dopaminergic signaling has been demonstrated to modulate both LFPs in the NAcc and the initiation of goaldirected behavior (Goto and Grace, 2008 …”

“…This study, however, does not directly address one core function of the NAcc: the translation of basic salience signals into contextually appropriate behaviors. The NAcc has a diverse set of sensory, affective, and motivational afferents and motor efferents, making it well positioned to translate environmental salience signals into motor action plans (Goto and Grace, 2008). Additionally, the NAcc has been demonstrated to modulate response vigor, locomotion, and exploration (McGinty et al, 2013).…”

Sustained attention in psychosis: Neuroimaging findings

“…The most commonly used tasks to assess sustained attention are the "oddball paradigms", where subjects are required to identify rare and unpredictable target stimuli presented among a stream of frequent non-target stimuli [36,37] or among both frequent and rare non-target stimuli, usually called "standards" and "novels" respectively [38,39] . A particular kind of oddball paradigm is the Continuous Performance Test (CPT), initially developed by Beck et al [40] and nowadays considered a well validated instrument to measure sustained attention in both research and clinical settings [41] .…”