Cerebellar contributions to sequence prediction in verbal working memory

Abstract

Verbal working memory is one of the most studied non-motor functions with robust cerebellar involvement. While the superior cerebellum (lobule VI) has been associated with articulatory control, the inferior cerebellum (lobule VIIIa) has been linked to phonological storage. The present study was aimed to elucidate the differential roles of these regions by investigating whether the cerebellum might contribute to verbal working memory via predictions based on sequence learning/detection. 19 healthy adult subjects completed an fMRI-based Sternberg task which included repeating and novel letter sequences that were phonologically similar or dissimilar. It was hypothesized that learning a repeating sequence of study letters would reduce phonological storage demand and associated right inferior cerebellar activations and that this effect would be modulated by phonological similarity of the study letters. Specifically, while increased phonological storage demand due to high phonological similarity was expected to be reflected in increased right inferior cerebellar activations for similar relative to dissimilar study letters, the reduction in activation for repeating relative to novel sequences was expected to be more profound for phonologically similar than for dissimilar study letters, especially at higher memory load. Results confirmed the typical effects of cognitive load (5 vs. 2 study letters) and phonological similarity in several cerebellar and neocortical brain regions as well as in behavioral data (accuracy and response time). Importantly, activations in superior and inferior cerebellar regions were differentially modulated as a function of similarity and sequence novelty, indicating that particularly lobule VIIIa may contribute to verbal working memory by generating predictions of letter sequences that reduce the likelihood of phonological loop failure before stored items need to be retrieved. The present study is consistent with other investigations that support prediction, which can be based on sequence learning or detection, as an overarching cerebellar function. Electronic supplementary material The online version of this article (10.1007/s00429-018-1784-0) contains supplementary material, which is available to authorized users.

Sensorimotor, language, and working memory representation within the human cerebellum

“…These results are in broad agreement with others, and suggest extensive areas of the cerebellum are involved in working memory (Chen & Desmond, 2005a;Chen & Desmond, 2005b;Desmond et al, 1997;Guell et al, 2018;Keren-Happuch et al, 2014;Stoodley et al, 2012;Tomlinson, Davis, Morgan, & Bracewell, 2014). A recent study (Peterburs, Blevins, Sheu, & Desmond, 2019), which also used a Sternberg paradigm, found that BOLD activity in Lobule VIII (previously shown to be involved in maintenance, Kirschen et al, 2010), increased with working memory load. Taken together, these findings provide evidence of a role for the cerebellum in sequence rehearsal, detection, and prediction in relation to VWM.…”

“…However, a recent imaging study has shown that performance of the Sternberg task does not result in contamination of cerebellar activity related to eye movements (Peterburs et al, 2016). A recent study (Peterburs, Blevins, Sheu, & Desmond, 2019), which also used a Sternberg paradigm, found that BOLD activity in Lobule VIII (previously shown to be involved in maintenance, Kirschen et al, 2010), increased with working memory load. Load was associated with widespread activity in bilateral Crus I, right Crus II, and right Lobules VI and VIII, with greatest activity in the right cerebellar hemisphere.…”

The posterior cerebellum supports the explicit sequence learning linked to trait attribution

“…Moreover, in a recent neuroimaging study, participants were asked to complete a Sternberg task that included repeating and novel letter sequences. The results indicated that activations in cerebellar regions contribute to verbal working memory by generating predictions of letter sequences, which supports the hypothesis of sequence learning, detection, and prediction (Peterburs, Blevins, Sheu, & Desmond, 2019 ).…”

“…This confirms the functional role of the cerebellum in social sequence detection and learning. Note that it is quite unlikely that the stronger activation of social sequence learning is simply due to higher memory load and executive effort required for social sentences in comparison with nonsocial sentences, because retrieval accuracy was almost identical across these two conditions, and activation was opposite to that reported for higher verbal memory load in recent research (deactivation: Peterburs et al, 2019). Other potential differences between these conditions, such as a greater motivational and emotional impact of social sentences might contribute to the stronger activation of the posterior cerebellum, although these are inherent (and often desired) aspects of social action, which cannot easily be eliminated.…”

Altered Patterns of Phase Position Connectivity in Default Mode Subnetwork of Subjective Cognitive Decline and Amnestic Mild Cognitive Impairment

“…Based on earlier finds, SCL is involved in articulatory control and non-motor cognitive function (Ferenci et al, 2002). The left FG plays a critical role in semantic dementia and is repeatedly reported to be involved in visual word processing (Peterburs et al, 2019). SFG, which is located on top of the brain, plays a role in several higher-level cognitive processes and working memory according to a previous report (Alagapan et al, 2019).…”