Posterior parietal cortex is critical for the encoding, consolidation, and retrieval of a memory that guides attention for learning

Abstract

Within most contemporary learning theories, reinforcement prediction error, the difference between the obtained and expected reinforcer value, critically influences associative learning. In some theories, this prediction error determines the momentary effectiveness of the reinforcer itself, such that the same physical event produces more learning when its presentation is surprising than when it is expected. In other theories, prediction error enhances attention to potential cues for that reinforcer by adjusting cue-specific associability parameters, biasing the processing of those stimuli so that they more readily enter into new associations in the future. A unique feature of these latter theories is that such alterations in stimulus associability must be represented in memory in an enduring fashion. Indeed, considerable data indicate that altered associability may be expressed days after its induction. Previous research from our laboratory identified brain circuit elements critical to the enhancement of stimulus associability by the omission of an expected event, and to the subsequent expression of that altered associability in more rapid learning. Here, for the first time, we identified a brain region, the posterior parietal cortex, as a potential site for a memorial representation of altered stimulus associability. In three experiments using rats and a serial prediction task, we found that intact posterior parietal cortex function was essential during the encoding, consolidation, and retrieval of an associability memory enhanced by surprising omissions. We discuss these new results in the context of our previous findings and additional plausible frontoparietal and subcortical networks.

Effects of amygdala lesions on overexpectation phenomena in food cup approach and autoshaping procedures.

“…Finally, we have identified several regions that are critical to the expression of enhanced associability in faster learning but not to the original encoding of altered associability, including substantia innominata/nucleus basalis magnocellularis, the secondary visual cortex, the dorsolateral striatum, and the lateral hypothalamus. Circuitry by which recalculated associability values are conveyed to PPC for storage and by which these altered associability memories are transmitted to components of the expression module remains a subject of speculation (Schiffino, 2015; Schiffino, Zhou, & Holland, 2014). …”

Consolidation of altered associability information by amygdala central nucleus

“…Post-surprise infusions of anisomycin, lidocaine, or muscimol prevented subsequent display of surprise-enhanced associability. Because previous studies indicated that CeA function is unnecessary for the expression of associability enhancements that were induced previously when CeA function was intact (Holland & Gallagher, 2006), we interpreted these results as indicating that post-surprise activity of CeA (“surprise replay”) is necessary for the consolidation of altered associability memories elsewhere in the brain, such as the posterior parietal cortex (Schiffino, et al, 2014a). …”

“…Interestingly, Schiffino et al (2014a) found that function of the posterior parietal cortex (PPC) was critical at both the time of surprise and the time of expression. Because PPC function was required both when surprise-induced changes in associability were encoded and when they were retrieved for new learning, Schiffino et al (2014a) suggested that PPC might be the site of a relatively permanent memory of altered cue associability.…”

“…Because PPC function was required both when surprise-induced changes in associability were encoded and when they were retrieved for new learning, Schiffino et al (2014a) suggested that PPC might be the site of a relatively permanent memory of altered cue associability. In support of that assertion, Schiffino et al (2014a) also found that infusion of the protein-synthesis inhibitor anisomycin into PPC immediately after surprise sessions prevented (in a time-dependent manner) cue associability enhancements, as if it prevented the consolidation of an altered associability memory.…”

“…Because PPC function was required both when surprise-induced changes in associability were encoded and when they were retrieved for new learning, Schiffino et al (2014a) suggested that PPC might be the site of a relatively permanent memory of altered cue associability. In support of that assertion, Schiffino et al (2014a) also found that infusion of the protein-synthesis inhibitor anisomycin into PPC immediately after surprise sessions prevented (in a time-dependent manner) cue associability enhancements, as if it prevented the consolidation of an altered associability memory. This consolidation process likely relies upon interactions among multiple brain regions, and given the historical importance of amygdala function to memory consolidation (McGaugh, 2004) and the observation that CeA activity during encoding is critical to associability enhancements (Holland & Gallagher, 2006) it seems reasonable to consider a role for this nucleus in the consolidation of altered associability memories.…”