Multimodal Feature Integration in the Angular Gyrus during Episodic and Semantic Retrieval

Abstract

Much evidence from distinct lines of investigation indicates the involvement of angular gyrus (AnG) in the retrieval of both episodic and semantic information, but the region's precise function and whether that function differs across episodic and semantic retrieval have yet to be determined. We used univariate and multivariate fMRI analysis methods to examine the role of AnG in multimodal feature integration during episodic and semantic retrieval. Human participants completed episodic and semantic memory tasks involving unimodal (auditory or visual) and multimodal (audio-visual) stimuli. Univariate analyses revealed the recruitment of functionally distinct AnG subregions during the retrieval of episodic and semantic information. Consistent with a role in multimodal feature integration during episodic retrieval, significantly greater AnG activity was observed during retrieval of integrated multimodal episodic memories compared with unimodal episodic memories. Multivariate classification analyses revealed that individual multimodal episodic memories could be differentiated in AnG, with classification accuracy tracking the vividness of participants' reported recollections, whereas distinct unimodal memories were represented in sensory association areas only. In contrast to episodic retrieval, AnG was engaged to a statistically equivalent degree during retrieval of unimodal and multimodal semantic memories, suggesting a distinct role for AnG during semantic retrieval. Modality-specific sensory association areas exhibited corresponding activity during both episodic and semantic retrieval, which mirrored the functional specialization of these regions during perception. The results offer new insights into the integrative processes subserved by AnG and its contribution to our subjective experience of remembering.

Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory

“…The various roles attributed to inferior parietal regions such as AnG during memory retrieval include attentional capture by retrieved information (Cabeza et al, 2008), the accumulation of evidence in memory (Wagner et al, 2005), or a 'buffer' that stores information for further evaluation during long-term memory retrieval (Vilberg and Rugg, 2008). Consistent with the latter account, recent work supports a role for AnG in carrying specific details of memory representations, finding that episodic memories are represented individually and can be decoded by multivariate classifier analyses in this area (Bonnici et al, 2016; Kuhl and Chun, 2014). These findings indicate that AnG may represent the information on which a mnemonic decision is based, with properties of the representation such as its level of detail or the fidelity of the information retrieved driving decisions about a memory’s origin and other associated features.…”

“…It is worth noting that previous studies have also linked activity in AnG with rated vividness (Bonnici et al, 2016; Kuhl and Chun, 2014) and confidence (Qin et al, 2011), and that hippocampal activity, too, has been reported to be associated with vividness ratings (Ford and Kensinger, 2016; Gilboa et al, 2004). Moreover, patients with lesions that include the lateral parietal lobe often report reduced memory detail and diminished recollection vividness (Berryhill et al, 2007; Simons et al, 2010).…”

“…This moderate correlation would imply that trials which were more precisely and/or successfully remembered would be, on average, associated with higher vividness ratings, possibly explaining previous reports of a link between vividness ratings and brain activity in AnG (cf. Bonnici et al, 2016; Kuhl and Chun, 2014), or hippocampus (Ford and Kensinger, 2016; Gilboa et al, 2004). Regarding reports of diminished vividness following parietal cortex lesions, such lesions are frequently not selective to lateral parietal cortex (Berryhill et al, 2007), often including medial parietal areas.…”

Knowing what from where: Hippocampal connectivity with temporoparietal cortex at rest is linked to individual differences in semantic and topographic memory

“…Left temporoparietal cortex is linked to many different forms of memory retrieval: Angular gyrus (within the default mode network) supports autobiographical memory (Spreng, Mar, & Kim, 2008;Cabeza, Ciaramelli, Olson, & Moscovitch, 2008;Bonnici, Richter, Yazar, & Simons, 2016) and more automatic aspects of semantic retrieval (Binder et al, 2009;Humphreys & Lambon Ralph, 2014, Seghier, 2012. Inhibitory TMS to the left angular gyrus region disrupts the retrieval of detailed conceptual knowledge (Davey et al, 2015b).…”

“…The superior temporal sulcus is linked to metalizing (Saxe & Kanwisher, 2003), and posterior middle temporal gyrus (at the ventral extent of the cluster) is associated with retrieval of weak semantic associations (Noonan, Jefferies, Visser, & Lambon Ralph, 2013 ;Davey et al, 2015;Davey et al, 2016). Thus, the cluster we identified is well-suited for the allocation of attention to activated memory representations (Cabeza et al, 2011) and maybe important in autobiographical memory because it allows multiple distributed features to be recombined together (Wagner, van Buuren, Bovy, & Fernandez, 2016;Kuhl & Chun, 2014, Wagner et al, 2015, Bonnici et al, 2016. Interestingly, inferior parietal cortex is also strongly associated with spatial attention, especially in the right hemisphere: for example, right-sided damage here often results in spatial neglect hemisphere (Mesulam, 1981) and meta-analytic decoding revealed a contribution to spatial processing in both the left and right.…”