Although there are numerous unanswered questions, we have shown here that there is likely to be a great deal of commonality in the way the cortico-basal ganglia network functions to control adaptive behavior in mammalian species. Thus, we have described here two learning processes and two motivational processes that subserve goal-directed and habitual actions and that not only appear to exert similar behavioral control but also to depend on homologous neural networks in humans and rodents. Of course, we are not proposing that these networks are identical or reducible on a point-to-point basis. It does appear, however, that the functional anatomy and underlying organizational principles of the basal ganglia in humans and rodents are extremely similar and it will be an important task of future research to establish whether and in what ways they differ functionally.
There is, for example, striking similarity in the functional network controlling goal-directed actions. As we describe above, objective and subjective measures of action–outcome learning correlate with activity in regions of medial prefrontal, medial orbital cortex, and the caudate nucleus in humans (). Similarly, we reviewed the now considerable evidence that prelimbic cortex and dorsomedial striatum in rats subserves a very similar function. Generally, the homology between the rodent dorsomedial striatum and human caudate nucleus is relatively secure, although there are clearly functional differences in the rostro-caudal plane that remain to be explored (Balleine et al, 2007b
). There has, however, been considerably more controversy as to whether the rat possesses similar prefrontal cortical regions to humans and other primates (Preuss, 1995
). Nevertheless, this controversy has largely been concerned with narrower issues such as whether there is a rodent homology to primate dorsolateral prefrontal cortex (with Preuss (1995)
claiming that there is not and Uylings et al, 2003
arguing that there certainly is) or frontal pole (Wise, 2008
), whereas there is growing evidence based on connectivity and density of connections, neurotransmitter types, embryological development, cytoarchitectonic characteristics, and (last but, obviously, not least from, our perspective) functional similarity that rodent prelimbic-medial orbital cortex region is analogous to human ventromedial prefrontal-medial orbital cortex (see Brown and Bowman, 2002
; Uylings et al, 2003
for discussion). Generally, however, there has been insufficient systematic research of prefrontal cortex functions in rodent and human subjects using similarly structured tasks. More research along these lines would contribute meaningfully to an understanding of functional homologies in prefrontal cortex.
We also describe commonalities in the network mediating habit learning. Although, given the literature, this is perhaps somewhat less surprising (Graybiel, 2008
), it is important to recognize that much of the previous evidence has not only come from very different tasks but also the relevance of these tasks to S–R learning has often largely been inferred from the experimenters' description of the task rather than direct tests of the factors controlling performance. There has, for example, been a large literature linking sensorimotor cortex and its efferents to dorsolateral striatum in rat in various maze learning tasks and other nominally S–R tasks involving discrimination learning. As we describe above, this is, however, something that has now been confirmed more directly using behavioral measures that confirm habitual control of overtrained actions both in rats and, using a very similar task, in humans and found to depend on dorsolateral striatum in rat and on the analogous region of striatum, the putamen, in human. At present, little is known about the structure of habit learning. For example, although reinforcement learning models provide clear predictions on the nature of the reinforcement signal supporting habit learning, it is not currently known if this constitutes the dopamine error signal alone, some integral of that signal involving local neuromodulators of the dopaminergic input to the striatum, or some combination of these or other potential processes. Likewise, although we have argued that amygdala has a central role in both reward and reinforcement processes, we do not know how these twin functions of outcome delivery are parsed neurally.
Although the goal-directed and habit learning processes that support the two major forms of adaptive behavioral control can be observed in both humans and rats and appear to depend on homologous corticostriatal circuits, it is unknown how these forms of learning interact and what conditions modulate whether they cooperate or inhibit/interfere with one another. As presented above, it is clear that under some circumstances they interact; goal-directed and habitual control of performance often appears to be all or none rather than some mixture of the two. In other situations, these processes appear to be temporally related to one another and to function in synergy during the selection, evaluation, and implementation of actions. This will be a critical problem to resolve if we are to formulate accurate models of real life decision making in the course of which ongoing routine actions have often to be suspended, interference between concurrent choices has to be overcome, and new information has to be incorporated into the decision process while, nevertheless, remaining adaptive, at least for the most part.
Finally, we also described considerable evidence suggesting that homologous structures in rat and human mediate the influence of motivational processes on the performance of goal-directed and habitual actions, particularly the influence of Pavlovian cues on choice. Central and lateral OFC and ventral striatum appear to be particularly important for calculating and deploying the influence of Pavlovian values and, as described above, similar structures have also been implicated in rats in this process. This is perhaps most clear in the influence of outcome-specific Pavlovian values on choice in Pavlovian-instrumental transfer; in rodent, this effect depends on a circuit involving accumbens shell, mediodorsal thalamus, and lateral obitofrontal cortex. In humans, to date we have found evidence that the ventral putamen, a region coextensive with the shell, is activated in the presence of cues predicting the same outcome as the action when that action is performed, and is reduced when an action associated with a different outcome is performed. Similarly, outcome values encoded as a consequence of exposure to, and consummatory contact with, the consequences of actions have been found to depend on amygdala, insular, and medial orbitofrontal cortex in humans and to rely on similar structures in rats. Unfortunately, apart from very few notable exceptions, little of this research has been undertaken using comparable tasks or motivational manipulations organized to influence the same or comparable regulatory systems. Again, it is clearly research along these lines that will make the most rapid progress in understanding functional homologies in motivation. Finally, we do not have a clear understanding of the way that motivational and emotional processes regulate the networks that control choice and decision making in either humans or rodents. The common features of the influence of outcome and Pavlovian values on choice in rodent and human subjects described above points to the fact that similar neural systems organized along similar lines likely underlie this integrative process at least in mammals but, for the moment, it would be pure speculation to attempt to specify those in any greater detail.