The Role of the Amygdala-Striatal Pathway in the Acquisition and Performance of Goal-Directed Instrumental Actions

Abstract

The posterior dorsomedial striatum (pDMS) is essential for the acquisition and expression of the specific response-outcome (R-O) associations that underlie goal-directed action. Here we examined the role of a pathway linking the basolateral amygdala (BLA) and pDMS in such goal-directed learning. In Experiment 1, rats received unilateral lesions of the BLA and were implanted with cannula targeting the pDMS in either the ipsilateral (control) or contralateral (disconnection) hemisphere. After initial training, rats received infusions of muscimol to inactivate the pDMS immediately before sessions in which novel R-O associations were introduced. Sensitivity to devaluation by specific satiety was then assessed. Whereas rats in the ipsilateral group used the recently acquired associations to direct performance following devaluation, those in the contralateral group could not, indicating that BLA-pDMS disconnection prevented the acquisition of the new R-O associations. Indeed, evidence suggested that these rats relied instead on learning acquired during prior training to direct performance following devaluation. In Experiment 2, rats underwent similar surgery and training except they received muscimol infusions immediately before devaluation testing. Those in the ipsilateral group showed a selective devaluation effect, again based on the most recently introduced R-O associations. In contrast, rats in the contralateral group showed nonselective performance after devaluation indicating that the BLA-DMS pathway is also required for the expression of selective R-O associations. Together these results suggest that input from the BLA is essential for specific R-O learning by the pDMS.

Appetitive associative learning recruits a distinct network with cortical, striatal, and hypothalamic regions

“…Furthermore, the PL, ILA, and BLAa are all recruited during late tone-food training, and Fos induction in these areas correlated significantly with Fos induction in the DMS. Taken together our findings are consistent with the idea that the BLA acts as the primary processor of emotional information, which through cooperation with cortical and striatal regions results in the appropriate appetitive behavioral response (Schoenbaum et al, 1998; Piette et al, 2012: Corbit et al, 2013; Parkes and Balleine, 2013). One possibility is that the DMS activation seen here may reflect its role in encoding of an association between the cue and the unique properties of the food pellets and its current value, as suggested in a recent study by Corbit and Janak (2010).…”

“…Current accounts of dorsal striatal function in reward learning emphasize a role in acquiring instrumental actions for food (e.g. lever-press for sucrose) (Yin et al, 2005; Shiflett et al, 2010; Bradfield et al, 2013; Corbit et al, 2013). Consequently, the present results are exciting because they suggest that the DMS is also involved during Pavlovian cue-food associations.…”

“…However, the DMS has a unique connectional pattern, with afferents from higher order associational areas (see Voorn et al, 2004). Notably, the DMS receives heavy innervation from the PL and lighter projections from the ILA (Berendse et al, 1992), while the amygdalar inputs are from the BLAa (Kita and Kitai, 1990; Corbit et al, 2013). These connections suggest the DMS could be an important integrative site mediating appetitive associative learning and behavior.…”

The algorithmic anatomy of model-based evaluation

“…Perhaps for a similar reason, infralimbic cortex (which is more associated with ventral striatum than with dorsolateral) is also involved in habitual instrumental behaviour [23]. In addition, recent results with disconnection lesions suggest that the basolateral and central nuclei of the amygdala, in communication with dorsomedial and dorsolateral striatum, are required for acquiring MB and MF instrumental behaviours, respectively [86,87].…”

Connections of the Mouse Orbitofrontal Cortex and Regulation of Goal-Directed Action Selection by Brain-Derived Neurotrophic Factor

“…From a circuit-level perspective, most reports in this domain have focused on BLA interactions with the nucleus accumbens and dorsal striatum (10–12), meaning top-down cortical regulation of BLA-dependent goal-directed decision-making is under-characterized. Further, these and related studies have largely used lesion approaches in rats, leaving molecular mechanisms unclear.…”