The Nucleus Accumbens: A Switchboard for Goal-Directed Behaviors

Abstract

Reward intake optimization requires a balance between exploiting known sources of rewards and exploring for new sources. The prefrontal cortex (PFC) and associated basal ganglia circuits are likely candidates as neural structures responsible for such balance, while the hippocampus may be responsible for spatial/contextual information. Although studies have assessed interactions between hippocampus and PFC, and between hippocampus and the nucleus accumbens (NA), it is not known whether 3-way interactions among these structures vary under different behavioral conditions. Here, we investigated these interactions with multichannel recordings while rats explored an operant chamber and while they performed a learned lever-pressing task for reward in the same chamber shortly afterward. Neural firing and local field potentials in the NA core synchronized with hippocampal activity during spatial exploration, but during lever pressing they instead synchronized more strongly with the PFC. The latter is likely due to transient drive of NA neurons by bursting prefrontal activation, as in vivo intracellular recordings in anesthetized rats revealed that NA up states can transiently synchronize with spontaneous PFC activity and PFC stimulation with a bursting pattern reliably evoked up states in NA neurons. Thus, the ability to switch synchronization in a task-dependent manner indicates that the NA core can dynamically select its inputs to suit environmental demands, thereby contributing to decision-making, a function that was thought to primarily depend on the PFC.

Differential behavioral profile induced by the injection of dipotassium chlorazepate within brain areas that project to the nucleus accumbens septi

“…These later findings are in accordance with the fact that NAS is considered today a switchboard for goaldirected behaviors [32]. Pharmacological glutamatergic NAS blockade induced an increase in PFC activity [4], in accordance to other evidences showing that a disinhibited prefrontal cortex impairs cognitive flexibility [31].…”

Olanzapine treatment of adolescent rats alters adult reward behaviour and nucleus accumbens function

“…Information from both structures converges upon the NAcC (Grace et al, 2007). Neural activity in the NAcC shifts between synchrony with the hippocampus and synchrony with the MPC in a task-dependent manner (Gruber et al, 2009), suggesting the weighting of inputs from those structures according to situational requirements. Hippocampus×MPC interactions appear to contribute to these shifts.…”

Behavioral Characteristics and Neural Mechanisms Mediating Performance in a Rodent Version of the Balloon Analog Risk Task

“…The mPFC innervates ventromedial aspects of the striatum, including the nucleus accumbens (Berendse et al, 1992;Sesack and Pickel, 1992), whereas the specific subdivision of the OFC targeted here innervates ventrolateral portions of the striatum, including the putamen (Schilman et al, 2008). Notably, prefrontal cortical fibers interact with inputs from medial temporal lobe structures, including the hippocampus and amygdala and the dopamine-rich ventral midbrain to drive goal-directed behavior Grace, 2005, 2008;Gruber et al, 2009;Sesack and Grace, 2010). Though functional neuroimaging studies have not yet resolved the influences of these posterior structures on BART performance in human beings, it remains possible that they exert independent and interactive effects on network function in striatal subregions to control different aspects of behavioral performance.…”