Brain Signature of Working Memory for Sentence Structure: Enriched Encoding and Facilitated Maintenance

Abstract

Sentences are easier to memorize than ungrammatical word strings, a phenomenon known as the sentence superiority effect. Yet, it is unclear how higher-order linguistic information facilitates verbal working memory and how this is implemented in the neural system. The goal of the current fMRI study was to specify the brain mechanisms underlying the sentence superiority effect during encoding and during maintenance in working memory by manipulating syntactic structure and working memory load. The encoding of sentence material, as compared with the encoding of ungrammatical word strings, recruited not only inferior frontal (BA 47) and anterior temporal language-related areas but also the medial-temporal lobe, which is not classically reported for language tasks. During maintenance, it was sentence structure as contrasted with ungrammatical word strings that led to activation decrease in Broca's area, SMA, and parietal regions. Furthermore, in Broca's area, an interaction effect revealed a load effect for ungrammatical word strings but not for sentences. The sentence superiority effect, thus, is neurally reflected in a twofold pattern, consisting of increased activation in classical language as well as memory areas during the encoding phase and decreased maintenance-related activation. This pattern reflects how chunking, based on sentential syntactic and semantic information, alleviates rehearsal demands and thus leads to improved working memory performance.

Memory integration in amnesia: Prior knowledge supports verbal short-term memory

“…These results support a prior observation of preserved sentence superiority in developmental amnesia (Baddeley et al, 2010) and extend these results to adult-onset amnesia. Although hippo-campal activity has previously been observed in association with the sentence superiority effect in healthy adults (Bonhage et al, 2014), the current results indicate that an intact hippocampus is not necessary in order for immediate memory to benefit from preexisting linguistic information stored in LTM.…”

“…Consistent with this possibility, several recent neuroimaging studies have reported increased hippocampal activity associated with facilitated immediate verbal recall in familiar versus unfamiliar encoding contexts (Bonhage et al, 2014; Bor et al, 2004; Bor and Owen, 2007). Bor et al (2004) found greater hippocampal activity when participants memorized mathematically structured digit sequences (2, 4, 6, 8, 9, 7, 5, 3) compared to unstructured digit sequences (9, 2, 7, 1, 4, 6, 5, 8) and Bonhage et al (2014) found greater hippocampal activity when participants memorized lists of words appearing in the context of sentences versus lists. Interestingly, Bonhage et al found that increased hippocampal activity during sentence encoding was accompanied by decreased frontal activity in classic language-related areas during sentence maintenance.…”

“…In the case of the sentence superiority effect, facilitated word recall in the context of sentences versus lists has been taken as a classic example of ‘chunking’, whereby stored linguistic knowledge serves to integrate individual verbal items into higher-order chunks that can be more easily recalled (Ericsson and Kintsch, 1995; Miller and Selfridge, 1950). Specifically, linguistic knowledge about the grammatical, syntactic and semantic structure of language is thought to combine activated verbal material into larger units, which reduces memory load and improves recall performance (Baddeley et al, 2009, 2010; Bonhage et al, 2014). Recently, it has been proposed that hippocampally-mediated relational binding supports this verbal chunking during STM, based on the observation that hippocampal activity increases when words are encoded in the context of sentences versus lists (Bonhage et al, 2014).…”

“…Specifically, linguistic knowledge about the grammatical, syntactic and semantic structure of language is thought to combine activated verbal material into larger units, which reduces memory load and improves recall performance (Baddeley et al, 2009, 2010; Bonhage et al, 2014). Recently, it has been proposed that hippocampally-mediated relational binding supports this verbal chunking during STM, based on the observation that hippocampal activity increases when words are encoded in the context of sentences versus lists (Bonhage et al, 2014). However, the current finding that the sentence superiority effect is preserved in amnesia reveals that this is not the case (see also Baddeley et al, 2010) and suggests that hippocampal activity during sentence encoding may simply reflect feed-forward projections from extra-MTL cortices that are responsible for the short-term maintenance of stimulus representations or the encoding of these representations into episodic LTM.…”

“…Understanding the nature and necessity of different extra-MTL regions for STM–LTM integration represents an important area for future research. Of particular interest is the potential contribution of medial and lateral PFC regions that have recently been implicated in the semantic facilitation of episodic memory (Bonhage et al, 2014; Bor et al, 2004; Bor and Owen, 2007; Schlichting and Preston, 2015; van Kesteren et al, 2012, 2013). Recent neuroimaging evidence suggests that the medial PFC guides the integration of new information into pre-existing memory models during encoding (van Kesteren et al, 2013; Schlichting and Preston, 2015).…”