A Role for the Medial Temporal Lobe in Feedback-Driven Learning: Evidence from Amnesia

Abstract

The ability to learn from feedback is a key component of adaptive behavior. This type of learning is traditionally thought to depend on neural substrates in the striatum and not on the medial temporal lobe (MTL). Here we show that in humans the MTL becomes necessary for feedback-based learning when feedback is delayed. Specifically, amnesic patients with MTL damage were impaired at probabilistic learning of cue-outcome associations when response-contingent feedback was delayed by a few seconds, but not when feedback was immediate. By contrast, patients with striatal dysfunction due to Parkinson's disease demonstrated the opposite pattern: impaired learning when trial-by-trial feedback was immediate but not when feedback was delayed, indicating that the striatum is necessary for learning only when feedback is immediate. Together, these results reveal that multiple complementary learning processes support what appears to be identical behavior in healthy individuals and point to an important role for the MTL in feedback-driven learning.

Mechanisms for widespread hippocampal involvement in cognition.

“…We found that rather than contributing broadly to probabilistic learning, the striatum selectivity supports learning when it is driven by immediate, trial-by-trial feedback — consistent with the reward prediction error coding in dopamine neurons. Learning the same information without feedback, or with delayed feedback — even when this learning is not consciously accessible — depends instead on the hippocampus (Foerde, Race, Verfaellie, & Shohamy, 2013; Foerde & Shohamy, 2011b; Poldrack et al, 2001; Shohamy et al, 2004; cf. Clark & Squire, 1998).…”

Apathy and noradrenaline

“…Indeed, a meta-analysis found Parkinson's disease patients to be significantly impaired in implicit learning across 27 studies using the serial reaction time task [48]. While implicit learning is thought to depend on the basal ganglia, explicit, declarative learning relies on the hippocampus and medial temporal lobe [49]. The interplay between the two systems has yet to be defined [50], but a selective impairment in Parkinson's disease would suggest implicit learning occurs in the dorsal striatum.…”

Separating the effect of reward from corrective feedback during learning in patients with Parkinson’s disease

“…If this is the case, one would predict that, for PD patients, observational learning of rewarded associations would be greater than learning unrewarded associations. Second, feedback timing is critical for PD patients during feedback-based learning (Foerde et al, 2013;Foerde & Shohamy, 2011a, b); PD patients perform as well as controls on feedback-based tasks (e.g., the WPT) when feedback is delayed, but perform worse than controls when feedback is immediate (Foerde et al, 2013). Thus, a second potential way to induce a reward effect in patients with PD is to delay the timing of rewards.…”

“…A. Poldrack et al, 2001;R. Poldrack, Prabhakaran, Seger, & Gabrieli, 1999), so it is not surprising that patients with Parkinson's disease (PD) who experience basal ganglia dysfunction as a result of dopamine neuron loss (Agid, 1991;Agid, Javoy-Agid, & Ruberg, 1987;Hornykiewicz, 1966) experience feedback learning deficits (Ashby et al, 2003;Cools, Barker, Sahakian, & Robbins, 2001;Foerde, Race, Verfaellie, & Shohamy, 2013;Knowlton et al, 1996;D. Shohamy, Myers, Onlaor, et al, 2004;Swainson et al, 2000).…”

“…Additionally, because participants generally do not gain awareness of which pairs were rewarded, and thus are rarely certain whether each trial is rewarded or not, we are able to minimize (but not abolish) the motivational influence of reward to better understand the reinforcing role of reward on learning. Because PD is associated with procedural and feedback learning deficits (Ashby et al, 2003;Cools et al, 2001;Foerde et al, 2013;Knowlton et al, 1996;Muslimović, Post, Speelman, & Schmand, 2007; D. Shohamy, Myers, Onlaor, et al, 2004;Swainson et al, 2000), we hypothesized that HCs would demonstrate significantly stronger learning of rewarded S-R pairs compared to unrewarded S-R pairs, but that PD patients would benefit less from reward. Because we were interested in studying PD patients under circumstances related to their daily functioning and because medicated patients have been shown to demonstrate comparable reward-related learning to HCs (Bódi et al, 2009;Frank et al, 2004;Palminteri et al, 2009), we studied patients while on their usual antiparkinsonian medications.…”