Different dorsal striatum circuits mediate action discrimination and action generalization

Abstract

Generalization is an important process that allows animals to extract rules from regularities of past experience and apply them to analogous situations. In particular, the generalization of previously learned actions to novel instruments allows animals to use past experience to act faster and more efficiently in an ever-changing environment. However, generalization of actions to a dissimilar instrument or situation may also be detrimental. In this study, we investigate the neural bases of action generalization and discrimination in mice trained on a lever-pressing task. Using specific schedules of reinforcement known to bias animals towards habitual or goal-directed behaviors, we confirmed that action generalization is more prominent in animals using habitual rather than goal-directed strategies. We uncovered that selective excitotoxic lesions of the dorsolateral and dorsomedial striatum have opposite effects on the generalization of a previously learned action to a novel lever. While lesions of the dorsolateral striatum impair action generalization, dorsomedial striatum lesions affect action discrimination and bias subjects towards action generalization. Importantly, these lesions do not affect the ability of animals to explore or match their lever-pressing rate to the reinforcement rate, or the ability to distinguish between different levers. The data presented here reveal that dorsolateral and dorsomedial striatal circuits have opposing roles in the generalization of previously learned actions to novel instruments, and suggest that these circuits compete for the expression of generalization in novel situations.

Endocannabinoid Modulation of Orbitostriatal Circuits Gates Habit Formation

“…Hence, in the within-subject procedure used in the current experiments, it is not the animal that is habitual or goal-directed; it is action control within a particular context that is habitual or goal-directed (Fig 1). Although there may be subtle differences, habitual control biased through use of both extended training or RI schedules recruits the dorsal lateral striatum, (Barnes et al, 2005; Dias-Ferreira et al, 2009; Gremel and Costa, 2013; Hilario et al, 2012; Smith and Graybiel, 2013; Thorn et al, 2010; Yin et al, 2006; 2004; Yin and Knowlton, 2006), goal-directed control biased through the use of RR depends on dorsomedial striatum (Barnes et al, 2005; Dias-Ferreira et al, 2009; Gremel and Costa, 2013; Hilario et al, 2012; Smith and Graybiel, 2013; Thorn et al, 2010; Yin et al, 2006; 2005a; 2005b; 2004; Yin and Knowlton, 2006). Using this within-subject approach, we took a chemogenetic approach to inhibit the activity of OFC-DS neurons, and found that inhibition of OFC-DS activity via activation of the G i/o -coupled hM4D receptor specifically during probe test sessions left the subject reliant on habit circuitry where normally goal-directed circuits are favored (Fig.…”

“…This raises the possibility that decision-making strategies compete for downstream behavioral control. Indeed, this has been observed in supporting neural circuits, with neural coding of habitual actions in the dorsal medial striatal (DMS), a region known to participate in support goal-directed control, and vice versa, neural coding of goal-directed actions in dorsal lateral striatal (DLS), a region known to support habitual processes (Graybiel, 2008; Gremel and Costa, 2013; Hilario et al, 2012; Stalnaker et al, 2010; Thorn et al, 2010; Yin et al, 2006; 2005a; 2004). Thus, disorders such as OCD and addiction may induce a pathology that results in an over-reliance on habitual circuitry in situations where greater goal-directed control would be more advantageous.…”

Discrete Circuits Support Generalized versus Context-Specific Vocal Learning in the Songbird

“…In contrast, when context-specificity is appropriate - for example, to modify central commands in a manner that accounts for context-dependent dynamics of the musculoskeletal system (Bouchard and Chang, 2014; Ostry et al, 1996; Schmidt and Wild, 2014; Wohlgemuth et al, 2010) - conflicting biasing signals will interfere with consolidation, and learning will continue to rely on moment-by-moment modulation by the AFP. Such a dependence of consolidation on the coherence of AFP bias may therefore be a natural way for the nervous system to transfer modifications that are generally appropriate to primary motor circuitry, while reserving frontal, “executive” circuitry for dynamically adjusting performance in response to context-specific requirements (Duan et al, 2015; Hilario et al, 2012; Kim and Hikosaka, 2013; Miller and Cohen, 2001; Narayanan and Laubach, 2006). …”

Cortico-Basal Ganglia Networks and the Neural Substrates of Actions

“…Lesions of the dorsomedial striatum, in particular the posterior parts, can abolish sensitivity to outcome devaluation in rats trained to perform specific actions for specific outcomes (Hilario, Holloway, Jin, & Costa, 2012;Yin, Ostlund, et al, 2005). Unlike lesions of the medial prefrontal cortex, both pretraining and posttraining lesions of the posterior dorsomedial striatum were effective in reducing sensitivity to outcome devaluation as well as contingency degradation.…”

“…Lesions of the dorsolateral striatum can render instrumental performance more sensitive to outcome devaluation or instrumental contingency reversal (Hilario et al, 2012;Yin et al, 2004. The system for goal-directed actions is still intact, as the animals can use the outcome representation to guide behavior.…”