Review
From ventral-medial to dorsal-lateral striatum: Neural correlates of reward-guided decision-making

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Abstract

The striatum is critical for reward-guided and habitual behavior. Anatomical and interference studies suggest a functional heterogeneity within striatum. Medial regions, such as nucleus accumbens core and dorsal medial striatum play roles in goal-directed behavior, while dorsal lateral striatum is critical for control of habitual action. Subdivisions of striatum are topographically connected with different cortical and subcortical structures forming channels that carry information related to limbic, associative, and sensorimotor functions. Here, we describe data showing that as one progresses from ventral-medial to dorsal-lateral striatum, there is a shift from more prominent value encoding to activity more closely related to associative and motor aspects of decision-making. In addition, we will describe data suggesting that striatal circuits work in parallel to control behavior and that regions within striatum can compensate for each other when functions are disrupted.

Introduction

Decision-making is governed by goal-directed and stimulus–response (S–R) driven mechanisms, with the former being more closely associated with medial regions of striatum, including nucleus accumbens core (NAc) and dorsal medial striatum (DMS), and the latter with dorsal lateral striatum (DLS). During learning, the transition from goal-directed behavior to S–R driven habits is thought to depend on “spiraling” connectivity from ventral-medial regions in striatum to dopamine (DA) neurons, which then project to more dorsal lateral portions of striatum (Haber et al., 2000, Houk et al., 1995, Ikemoto, 2007, Joel et al., 2002, Niv and Schoenbaum, 2008, Takahashi et al., 2008, van der Meer and Redish, 2011). This network (Fig. 1) allows for feed-forward propagation of information from limbic networks to associative and sensorimotor networks (Haber, 2003, Haber and Knutson, 2010, Haber et al., 2000, Ikemoto, 2007).

Here, we review neural correlates from our labs related to reward-guided decision-making in NAc, DMS, and DLS (Fig. 1). We will specifically focus on neural correlates from studies where animals performed the same behavioral task, thus allowing for direct comparison. Along the way we will describe neural and behavioral changes that occur when these subdivisions are selectively interfered with, offering insight into how these networks guide decision-making. From these studies it appears that different regions in striatum can compensate for each other when function in one is disrupted, suggesting that these structures can work in parallel.

The review is broken down into three sections based on popular ways to subdivide striatum. The classic division has been to subdivide striatum along the dorsal–ventral axis. We will begin our discussion of neural correlates by focusing on neural selectivity from the extremes of this division, nucleus accumbens and dorsal lateral striatum (Fig. 1). Next, we will examine correlates from dorsal striatum along the medial–lateral axis. This work has focused on the finding that DMS and DLS function can be clearly dissociated using devaluation and contingency degradation paradigms showing their respective roles in goal-driven and habitual behaviors (Balleine & O’Doherty, 2010). Finally, we will discuss a synthesis of the dorsal–ventral and the medial–lateral distinction of striatum, namely, a ventromedial to dorsolateral functional organization based on connectivity (Haber and Knutson, 2010, Nakamura et al., 2012, Voorn et al., 2004). Afferents innervating striatum progress from limbic to associative to sensorimotor, moving from ventral-medial to central to dorsal-lateral striatum, respectively (Haber, 2003, Haber and Knutson, 2010, Haber et al., 2000, Voorn et al., 2004). In this section, we will describe primate data illustrating how reward, motor, and cognitive neural correlates progress across the diagonal of striatum (Fig. 5B). Collectively these studies suggest that as one progresses from ventral-medial to dorsal-lateral striatum, there is a shift from more prominent value encoding to encoding that better reflects associative and sensorimotor functions.

Section snippets

Nucleus accumbens core versus dorsal lateral striatum

Several studies have reported that neural activity in both NAc and DLS is correlated with the value of expected outcomes. We examined these correlates using an odor-guided decision-making task during which we manipulated anticipated value by independently varying reward size and the length of delay preceding reward delivery (Roesch, Singh, Brown, Mullins, & Schoenbaum, 2009). As illustrated in Fig. 2A, rats were trained to nose-poke in a central odor port where one of three different odors was

Medial versus lateral dorsal striatum

So far, we have discussed the functional segregation between NAc and DLS, which is a common way to divide striatal function (i.e., dorsal–ventral plane). Other studies have focused on segregation of function across medial and lateral aspects of striatum, specifically within dorsal striatum (DS). Reward-related actions controlled by DS are thought to reflect the integration of two different learning processes, one that controls goal-directed behavior and the other the acquisition of habits (

From ventromedial to dorsolateral striatum

The majority of rodent work in DS has focused on dissociating medial versus lateral function. Unfortunately, little attention has been given to the examination of neural correlates across the dorsal–ventral plane of DS. In monkeys, Nakamura and colleagues recently dissected neural correlates in primate caudate, closely examining differences not only in the medial–lateral plane, but also in the dorsal–ventral plane (Nakamura et al., 2012).

In this study, monkeys made saccades to target stimuli

Conclusions

In conclusion, we describe data showing that although there is considerable overlap of neural correlates across striatum, as one progresses from ventral-medial striatum to dorsal-lateral striatum, there is a shift from more prominent value encoding to activity more closely related to associative and motor aspects of decision-making. Neural activity in NAc appears to be strongly correlated with the expected value of outcomes critical for motivating behavior in the pursuit of reward. Neural

Acknowledgments

This work was supported by Grants from the NIDA (R01DA031695, MR). Correspondence and requests for materials should be addressed to MR (email: [email protected]).

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