The Meaning of Behavior: Discriminating Reflex and Volition in the Brain

Abstract

The ability to establish behaviorally what psychological capacity an animal is deploying-to discern accurately what an animal is doing-is key to functional analyses of the brain. Our current understanding of these capacities suggests, however, that this task is complex; there is evidence that multiple capacities are engaged simultaneously and contribute independently to the control of behavior. As such, establishing the contribution of a cell, circuit, or neural system to any one function requires careful dissection of that role from its influence on other functions and, therefore, the careful selection and design of behavioral tasks fit for that purpose. Here I describe recent research that has sought to utilize behavioral tools to investigate the neural bases of instrumental conditioning, particularly the circuits and systems supporting the capacity for goal-directed action, as opposed to conditioned reflexes and habits, and how these sources of action control interact to generate adaptive behavior.

Amygdala-cortical control of striatal plasticity drives the acquisition of goal-directed action

“…The ability of humans and other animals to engage in goal-directed action has been found to rely on their capacity to encode the relationship between actions and their consequences or outcome, and to integrate that information with the current value of the outcome (Balleine and Dickinson, 1998;Dickinson and Balleine, 1994). Furthermore, recent evidence suggests that the acquisition of goal-directed actions relies on a cortical-limbic-striatal circuit centered on the posterior dorsomedial striatum (pDMS; Balleine, 2019;Balleine and O'Doherty, 2009). Inputs to the pDMS from prelimbic cortex (PL; Hart et al, 2018bHart et al, , 2018a and the basolateral amygdala (BLA; Balleine et al, 2003;Corbit et al, 2013) have been argued to be particularly important for this form of learning, although their relative importance in the cellular changes underlying the specific plasticity processes that control such learning is unknown.…”

Differential robustness to specific potassium channel deletions in midbrain dopaminergic neurons

“…In summary, the SK3 KO mice showed a slightly increased number of rearings while Kv4.3 displayed a slight alteration in motor learning. Overall, the modifications in motor behavior observed in SK3 or Kv4.3 KO mice, although rather weak, are consistent with alterations in the function of the nigrostriatal pathway (Balleine, 2019;Yin & Knowlton, 2006). Therefore, we next investigated whether the electrophysiological phenotype of SNc DA neurons displayed significant variations in both KO mice.…”

“…SNc DA neurons project onto the dorsal striatum (forming the nigrostriatal pathway) where they release DA. As a consequence, their activity has been demonstrated to critically influence motor learning, habitual and goal-directed actions (Balleine, 2019;Wise, 2004;Yin & Knowlton, 2006).…”

Loss of the Er81 Transcription Factor in Cholinergic Cells Alters Striatal Activity and Habit Formation

“…Er81 cKO mice hence displayed intact learning capacities (Days 1 to 3) as well as cognitive flexibility (Days 4 to 8). Mice were then overtrained for 5 days after they reached their performance plateau, in order to induce habit formation (Balleine, 2019) (Figure 7A, middle). Interestingly, Er81 cKO mice performed significantly higher compared to controls during the second reversal (Day 14; Figure 7A, right).…”

“…CINs control habit formation via the synchronisation and strengthening of the activity of the striatal output neurons (Gritton et al, 2019) (O'Hare et al, 2016 (Yin et al, 2004) (Balleine, 2019). Strong pauses have been shown to emerge during learning in response to rewardassociated stimuli but not to neutral stimuli (Graybiel et al, 1994) (Morris et al, 2004).…”