Dorsal Striatal Circuits for Habits, Compulsions and Addictions

Abstract

Here, we review the neural circuit bases of habits, compulsions, and addictions, behaviors which are all characterized by relatively automatic action performance. We discuss relevant studies, primarily from the rodent literature, and describe how major headway has been made in identifying the brain regions and neural cell types whose activity is modulated during the acquisition and performance of these automated behaviors. The dorsal striatum and cortical inputs to this structure have emerged as key players in the wider basal ganglia circuitry encoding behavioral automaticity, and changes in the activity of different neuronal cell-types in these brain regions have been shown to co-occur with the formation of automatic behaviors. We highlight how disordered functioning of these neural circuits can result in neuropsychiatric disorders, such as obsessive-compulsive disorder (OCD) and drug addiction. Finally, we discuss how the next phase of research in the field may benefit from integration of approaches for access to cells based on their genetic makeup, activity, connectivity and precise anatomical location.

Keywords: dorsolateral striatum; dorsomedial striatum; goal-directed behavior; habits; prefrontal cortex; striatum.

Figure 1

Characteristics of the shift from goal-directed to habitual behavior. (A) Left: Goal-directed and habitual behaviors are competitive processes that act in balance. Goal-directed behavior is characterized by a high requirement for attention, is highly contingent on present reward value, and demonstrates flexibility of responding. Habitual behavior is stimulus-driven, less dependent on present reward value, and governed by behavioral automaticity. Right: Addiction/compulsion represents an extreme state of habit. (B) The transition from goal-directed behavior to habitual behavior and then into compulsion, or addiction is graded. Shift from goal-directed to habitual behavior and then to compulsion/addiction corresponds to strengthened stimulus-response association and reduced action-outcome contingency. These processes are bidirectional, i.e., a behavior can shift on the spectrum from goal-directed to habitual performance, and back again—though in the extremes of addiction whether it is possible to return fully to habit/goal-directed states is less clear. (C) During instrumental training, rates of responding for a reward increase. Post-training reward devaluation reduces response rates more quickly for goal-directed behaviors than it does for habitual behaviors, which take many more extinction trials to fully dissipate. The extremes of addiction are characterized by compulsive responding that is resistant even to punishment. (D) The balance between goal-directed and habitual behavioral states corresponds to relative levels of neural activity in the dorsomedial (DMS) vs. dorsolateral (DLS) striatum. (E) Task-bracketing activity pattern emerges in the DLS as animals are over-trained on a rewarded behavioral sequence (e.g., running a T-maze for a tasty reward). Spiny Projection Neurons (SPNs) exhibit high activity at the beginning of a learned motor sequence and again at the end as the animal approaches the reward. Fast-spiking interneurons (FSIs) exhibit high activity during the middle stages of a behavioral sequence.

Figure 2

Functional definitions of striatal neurons. (A–D) Different dimensions/layers/’masks’ describing striatal neurons. (A) Striatal subregion. (B) Molecular/genetic: principal striatal cell types include Drd1+ SPNs, Drd2+ SPNs, PV+ FSIs, ChAT+ cholinergic interneurons, and several other important subtypes of interneuron populations. (C) Homuncular: striatal cells preferentially receive inputs from different regions of cortex. Sensorimotor inputs corresponding to specific body parts map to specific regions of the striatum adapted from Robbe (2018). (D) Task-specific recruitment: segregated clusters of neurons recruited by specific behavioral sequences (Behavior A vs. Behavior B) are shown.