This paper reviews the fate of the central ideas behind the complementary learning systems (CLS) framework as originally articulated in McClelland, McNaughton, and O’Reilly (1995). This framework explains why the brain requires two differentially specialized learning and memory systems, and it nicely specifies their central properties (i.e., the hippocampus as a sparse, pattern-separated system for rapidly learning episodic memories, and the neocortex as a distributed, overlapping system for gradually integrating across episodes to extract latent semantic structure). We review the application (...) of the CLS framework to a range of important topics, including the following: the basic neural processes of hippocampal memory encoding and recall, conjunctive encoding, human recognition memory, consolidation of initial hippocampal learning in cortex, dynamic modulation of encoding versus recall, and the synergistic interactions between hippocampus and neocortex. Overall, the CLS framework remains a vital theoretical force in the field, with the empirical data over the past 15 years generally confirming its key principles. (shrink)

Compared to our understanding of positive prediction error signals occurring due to unexpected reward outcomes, less is known about the neural circuitry in humans that drives negative prediction errors during omission of expected rewards. While classical learning theories such as Rescorla–Wagner or temporal difference learning suggest that both types of prediction errors result from a simple subtraction, there has been recent evidence suggesting that different brain regions provide input to dopamine neurons which contributes to specific components of this prediction error (...) computation. Here, we focus on the brain regions responding to negative prediction error signals, which has been well-established in animal studies to involve a distinct pathway through the lateral habenula. We examine the activity of this pathway in humans, using a conditioned inhibition paradigm with high-resolution functional MRI. First, participants learned to associate a sensory stimulus with reward delivery. Then, reward delivery was omitted whenever this stimulus was presented simultaneously with a different sensory stimulus, the conditioned inhibitor. Both reward presentation and the reward-predictive cue activated midbrain dopamine regions, insula and orbitofrontal cortex. While we found significant activity at an uncorrected threshold for the CI in the habenula, consistent with our predictions, it did not survive correction for multiple comparisons and awaits further replication. Additionally, the pallidum and putamen regions of the basal ganglia showed modulations of activity for the inhibitor that did not survive the corrected threshold. (shrink)