Coordination of Actions and Habits in the Medial Prefrontal Cortex of Rats

0 Laboratoire de Neurosciences Cognitives , UMR 5106 CNRS, Universit de Bordeaux , France 1 Oxford University Press 2003. All rights reserved 2 School of Psychology, Cardiff University , Cardiff, UK As animals learn novel behavioural responses, performance is maintained by two dissociable influences. Initial responding is goal-directed and under voluntary control, but overtraining of the same response routine leads to behavioural autonomy and the development of habits that are no longer voluntary or goal-directed. Rats normally show goal-directed performance after limited training, indexed by sensitivity to changes in the value of reward, but this sensitivity to goal value is lost with extended training. Rats with selective lesions of the prelimbic medial prefrontal cortex showed no sensitivity to goal value after either limited or extended training, whereas rats with lesions of the infralimbic region of the medial prefrontal cortex showed the opposite pattern of deficit, a marked sensitivity to goal value after both limited and extended training. This double-dissociation suggests that the prelimbic region is responsible for voluntary response performance and the infralimbic cortex mediates the incremental ability of extended training to override this goal-directed behaviour. Introduction The ability to learn to perform purposive, goal-directed actions endows animals with a highly beneficial degree of behavioural f lexibility in the face of ever-changing environmental conditions. However, this voluntary control of performance comes with a price in terms of effortful control and monitoring of the response, frequently reducing the capacity for alternative cognitive processing (Gehring and Knight, 2000). One way in which animals can come to balance the twin desire for simplicity and f lexibility is through the development of habits (Dickinson, 1985). A venerable research history (James, 1890; Bryan and Harter, 1897; Kimble and Perlmuter, 1970; Boakes, 1993) documents the notion that an initially effortful and cognitively demanding response comes, with practice, to be produced f luidly and without difficulty. This two-process view is ref lected in the development of theories of behavioural responding that depends on both mechanistic, ref lexive stimulus response (SR) habits (either acquired or innate) and on actions that are voluntary and goal-directed. Although instrumental conditioning is frequently described only in terms of SR relationships, recent evidence suggests the involvement of at least two different forms of association, operating in tandem (Dickinson, 1985; Rescorla, 1991; Dickinson and Balleine, 1994). Empirical evidence from goal devaluation or revaluation experiments (Adams, 1982; Balleine and Dickinson, 1991, 1998a) indicates that during early stages of learning instrumental actions are goal-directed, requiring animals to encode the specific consequences of their actions as well as the causal relationship between the action and the goal, i.e. the nature of the responseoutcome (RO) association. As training proceeds, instrumental performance becomes habitual, stimulus-bound, and independent of the current value of the goal. This effect appears to depend not on repetition of the response per se, but perhaps on the fact that overtraining reduces the animals perceived correlation between performance of the response and achievement of the goal (Dickinson et al., 1995). Recent research has highlighted the role of the prefrontal cortex in the control and organization of goal-directed behaviour (Watanabe, 1996; Tremblay and Schultz, 1999), the monitoring of ongoing voluntary action sequences (Gehring and Knight, 2000) and the planning and selection of appropriate actions based on anticipated reward (Petrides, 1995; Rowe et al., 2000). In rats, the medial part of the prefrontal cortex has been associated with the ability to learn the contingency between actions and specific outcomes (Balleine and Dickinson, 1998a). Other research (mostly concerning the nature and localization of procedural memory) suggests that the SR associations likely to underpin habitual responding rely upon neural substrates that depend, at least in part, upon the integrity of the basal ganglia (Mishkin et al., 1984; Reading et al., 1991; Knowlton et al., 1996; White, 1997; Jog et al., 1999). However, even though psychological accounts of instrumental learning are frequently described in terms of a combination of these two processes, little work has examined the important issue of the neural underpinnings of the interaction between goal-directed and habitual processes that is responsible for everyday behaviour. As coordination of these two processes is perhaps best defined as an executive function (Shallice, 1988), one logical possibility is that this function is achieved by operations within different areas the prefrontal cortex, providing the basis both for the development of goal-directed actions, and a permissive role for the ability of habits to override voluntary performance. Both anatomical and behavioural data have shown that the medial prefrontal cortex is a heterogeneous structure, comprising the ventral infralimbic cortex underneath more dorsal prelimbic and anterior cingulate regions (Fisk and Wyss, 1999). The afferent, efferent and intrinsic connections of these regions can readily be dissociated (Sesack et al., 1989; Hurley et al., 1991; Takagishi and Tanemichi, 1991; Conde et al., 1995). The more ventral, infralimbic, region projects extrinsically to a variety of limbic and autonomic regions, including the hypothalamus, the amygdala, the bed nucleus of the stria terminalis, the periaqueductal gray, the dorsal motor vagal nucleus, the nucleus of the solitary tract and the parabrachial nucleus (Sesack et al., 1989; Hurley et al., 1991), as well as to the shell region of the nucleus accumbens (McGeorge and Faull, 1989; Berendse et al., 1992), and intrinsically shares restricted reciprocal connections to the prelimbic and dorsal peduncular cortices (Fisk and Wyss, 1999). In contrast, the more dorsal prelimbic region projects to core regions of the nucleus accumbens (Gorelova and Yang, 1997) as well as (from its dorsal extreme) to dorso-medial regions of the dorsal striatum (McGeorge and Faull, 1989; Berendse et al., 1992). Furthermore, reciprocal intrinsic connections exist between this region and the more dorsal anterior cingulate and medial agranular cortices, and from there to premotor and motor cortices (Bates and Goldman-Rakic, 1993; Morecroft and Van Hoesen, 1993; Lu et al., 1994). This interactive system in the medial wall of the prefrontal cortex is paralleled by a hierarchical f low of information through accumbens shell, core, central striatum and dorsal striatum under the inf luence of striato-nigrostriatal subcircuits (Haber et al., 2000). These two hierarchies may represent interconnected, parallel limbic, cognitive, motor systems, suggesting that components of t (...truncated)