The path to learning: Action acquisition is impaired when visual reinforcement signals must first access cortex

Animals, interacting with the environment, learn and exploit the consequences of their movements. Fundamental to this is the pairing of salient sensory input with recent motor output to form an action–outcome pair linking a performed movement with its outcome. Short-latency dopamine (DA) signalling in the basal ganglia has been proposed to support this crucial task. For visual stimuli, this DA signalling is triggered at short latency by input from the superior colliculus (SC). While some aspects of the visual signal (e.g. luminance), are relayed directly to the SC via the retinotectal projection, other information unavailable to this subcortical pathway must take a more circuitous route to the SC, first submitting to early visual processing in cortex. By comparing action–outcome pairing when the visual stimulus denoting success was immediately available to the SC, via the retinotectal pathway, against that when cortical processing of the signal was required, the impact this additional sensory processing has on action–outcome learning can be established. We found that action acquisition was significantly impaired when the action was reinforced by a stimulus ineligible for the retinotectal pathway. Furthermore, we found that when the stimulus was eligible for the retinotectal pathway but evoked an increased latency, action acquisition was not impaired. These results suggest that the afferent sensory pathway via the SC is certainly primary and possibly instrumental to the DA neurons’ role in the discovery of novel actions and that the differences found are not due to simple sensory latency.

► Action acquisition is impaired when reinforcement cannot directly access the SC.
► Signals which required cortical processing produce poorer action learning.
► Collicular signals evoking different latencies produce no learning difference.
► The retinotectal sensory afferent pathway is favoured for action acquisition.
► Differences in sensory latency cannot explain this preference.