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«By Zachary Alexander Rosner A dissertation submitted in partial satisfaction of the requirements for the degree of Doctor of Philosophy in Psychology ...»

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46 We were particularly interested in determining the neural processes that drive contrasts between generate and read conditions. We thus assessed the contrast of generate hits read hits, which resulted in significant activation in IFG, MFG, LOC, PrC, ITG, intraparietal sulcus (IPS), and ACC (see Figure 3.2A, Table 3.2). The reverse contrast (read hits generate hits) resulted in no significant activation differences. We next assessed neural activations associated with the generation effect for HC hits (generate read, HC hits), which revealed activations in bilateral IFG, MFG, LOC, ITG, IPS, PrC and ACC (see Figure 3.2B, regions in red, Table 3.3). The reverse contrast (read generate, HC hits) revealed activation in bilateral LOC and PrC, and left angular gyrus (AG) (see Figure 3.2B, regions in blue, Table 3.3).

Activations during retrieval were consistent with previous findings of the successful retrieval effect in which hits are compared with correction rejections (CR) (hits CRs). In the present study, the successful retrieval effect was associated with increased activation in the left IFG, MFG, superior frontal gyrus (SFG), LTC, LOC, ACC, supramarginal gyrus (SMG), and AG (Figure 3.3A). This retrieval-based network was observed when contrasts were restricted to generated items (hits CRs, generate items, Figure 3.3B) or to read items (hits CRs, read items, Figure 3.3C). Direct comparisons of retrieval-based generated versus read items revealed no reliable differences.

To evaluate neural correlates of the generation effect with respect to behavioral performance, we performed a covariate analysis of recognition performance and regional neural responses associated with the generation effect. We used as our covariate of interest overall memory performance (hit rate – false alarm rate) and correlated it with the contrast of generate read hits during encoding. With this analysis, we addressed the degree to which overall memory performance may be mediated by the magnitude of neural activations associated with the generation effect across individuals. As shown in Figure 3.4A, memory performance was significantly correlated with activity in the right parahippocampal gyrus (PHG), temporal fusiform cortex, MTG, AG, LOC, and PrC. Thus, the strength of activation within these regions elicited by self-generation at encoding predicted better memory performance. As the generation effect was particularly potent for HC hits, we performed a second covariate analysis in which the behavioral advantage of generation for HC hits (generate HC hit rate – read HC hit rate) was correlated with its neural counterpart, the contrast of generate HC hits read HC hits. In this analysis, we found correlated activity in the paracingulate, frontal pole, left ACC, and right SFG (Figure 3.4B), suggesting a medial-frontal network underlying the behavioral benefit of generation for producing strong recollective responses (i.e. HC hits).

Discussion The present findings addressed the neural correlates of the generation effect. Active generation was associated with a broad set of regions that included the IFG, MFG, ACC, PrC, IPS, ITG, and LOC. Significant prefrontal activity (IFG and MFG) confirmed the role of executive control processes important for establishing long-term memories. Thus, these findings mesh well with studies that have shown that these regions are particularly involved in stimulus refreshing, updating, and semantic access (D’Esposito et al., 1997; Johnson et al., 2005; Raye et al., 2002; Thompson-Schill et al., 1997). For example, previous studies have shown that these PFC regions are active when participants must refresh or re-activate recently presented words, drawings, or patterns (Johnson et al., 2005; Raye et al., 2002). The generation effect can thus be linked to related acts of refreshing and updating, which also involve internally mediated or generated information.

47 As suggested by theories of executive control (Miller & Cohen, 2001; Shimamura, 2000, 2008), prefrontal mechanisms act to modulate or control posterior cortical activity thus engaging a broad prefrontal-posterior network involved in selecting, maintaining, and manipulating information in working memory. In the present study, generation was associated with both PFC and posterior activity, particularly in regions involved in image generation (ITG) and object processing (LOC) (D’Esposito et al., 1997; Malach et al., 1995). Thus, the generation effect offers a useful analysis of the neural dynamics associated with executive or metacognitive monitoring and control (D’Esposito et al., 1999; Miller & Cohen, 2001; Postle, 2006;

Shimamura, 2008).

Importantly, covariate analyses showed that memory performance could be predicted by the degree to which neural networks associated with the generation effect were active.

Specifically, we found that overall memory performance was correlated with increased generate activity in the PHG, temporal fusiform cortex, MTG, AG, LOC, and PrC. In addition, the behavioral benefit of generating at encoding to produce subsequent HC hits was correlated with activity in medial anterior PFC regions known to be important for attending to internally generated versus externally perceived stimuli (Lagioia et al., 2011; Simons, Davis, Gilbert, Frith, & Burgess, 2006; Simons, Henson, Gilbert, & Fletcher, 2008). These findings link the generation effect to regional activations during encoding that are known to be critical for the establishment of long-term memories (Paller & Wagner, 2002). Generation increased both prefrontal activity and activity in posterior regions involved in verbal processing, object analysis, and visuospatial imagery. Additionally, participants who benefited the most from generation showed the greatest activation in regions known to be important for memory binding and retrieval, such as the PHG, AG, and PrC (Davachi, 2006).

Recently, Moss, Schunn, Schneider, McNamara, and VanLehn (2011) compared neural activity when participants reread, paraphrased, or explained biology texts. While self-explaining led to the greatest memory benefit, regional activity in ACC, bilateral superior parietal cortex, and left IFG also increased along with complexity of semantic processing. In the present study, different regions within the DMN were active when reading or generating items during encoding (IPL, PrC, dMPFC for generate read, HC hits; IPL, PrC for read generate, HC hits), suggesting that the DMN is responsible for internally driven processing, though different regions may mediate different top-down processes. It is possible that on some trials, active generation oriented participants to internally generated information arising from semantic analysis or conceptual processes, while reading kept participants less on-task and allowed for increased mind wandering. It is acknowledged that the DMN is associated with many internally mediate processes and that there may be regional specificity within the network depending on the particular process being engaged (Buckner & Carroll, 2007; Shimamura, 2011; Spreng et al., 2009).

At retrieval, successful recognition (hits CRs) was associated with activation in lateral and medial PPC, two regions associated with memory recollection (Cabeza, 2008; Shimamura, 2011; Vilberg & Rugg, 2008). Interestingly, this pattern of activity was observed for both successfully retrieved generated and read items, and there were no differences during retrieval that differentiated remembered items between the two conditions. Within the confines of the encoding conditions used in the study, our findings suggest that a remembered item (hit or highconfident hit) elicits the same pattern of activation during retrieval regardless of whether it was previously generated or read.

48 With respect to mapping psychological theories of the generation effect onto our fMRI findings, it is clear that multiple brain regions are responsible for different aspects of the mnemonic benefit associated with the generation effect. Certainly, PFC regions involved with semantic analysis, refreshing, and updating are included. However, a host of posterior regions, such as the PHG, temporal fusiform cortex, MTG, AG, and LOC, is also involved. It is possible that active generation increases attention and cognitive effort (prefrontal and posterior cortical activation; Miller & Cohen, 2001; Shimamura, 2000, 2008), conceptual and semantic processing (IFG and MTG; Bookheimer, 2002; Poldrack et al., 1999), and item distinctiveness (LOC and ACC; Malach et al., 1995; van Veen et al., 2001). Perhaps one of the reasons memory researchers have not reached a consensus regarding the underlying mechanism of the generation effect is that active generation engages a large range of cognitive processes. Depending on the task at hand, active generation may promote increases in attention, cognitive effort, item distinctiveness, semantic processing, and conceptual processing. Indeed, our findings affirm the fact that these memory-related influences associated particularly with strong recollective responses are driven by a broad network of both PFC and posterior regions during encoding (Shimamura, 2010).

–  –  –

Figure 3.1 – Experimental design and behavioral data.

(A) Experimental design for encoding phase and (B) retrieval phase. (C) Recognition accuracy for read and generate items. Hits are items correctly identified as old. HC hits are items correctly identified as old with HC.

53 Figure 3.2 – Statistical activation maps for the generation effect during encoding. (A) Hits.

Generate read (red): Regional activations include bilateral IFG, MFG, LOC, PrC, ITG, IPS,

ACC. Read generate (blue): no significant activation. (B) HC hits. Generate read (red):

Regional activations include bilateral IFG, MFG, LOC, ITG, IPS, ACC, right PrC. Read generate (blue): bilateral LOC, PrC, left AG.

54 Figure 3.3 – Statistical activation maps during retrieval. (A) Overall hits correct rejections.

Regional activations include left IFG, MFG, SFG, ITG, MTG, LOC, ACC, SMG, AG. (B) Generate hits correct rejections. Regional activations include left LOC, ACC, SMG, AG. (C) Read hits correct rejections. Regional activations include left IFG, MFG, SFG, ITG, MTG, ACC, SMG, AG, PHG.

55 Figure 3.4 – Covariate Analyses. (A) Shown in red are regions related to the generation effect (generate read, all items) that covaried with overall memory performance (hits – false alarms).

Regional activations include PHG, MTG, AG, LOC, temporal fusiform cortex, PrC. (B) Shown in red are regions related to the generation effect (generate read, HC items) that covaried with the behavioral generation effect (HC hits – false alarms). Regional activations include bilateral paracingulate cortex and frontal pole, left ACC, right SFG.

–  –  –

The purpose of the collection of experiments contained within this dissertation is to improve our understanding of the generation effect. This included exploring boundaries and conditions of positive and negative generation effects within 2 cultures of contrasting cognitive styles to illustrate in which ways active generation influences memory for various types of information. Additionally, the neural mechanisms underlying the generation effect were investigated to help elucidate not only the effects of generation, but why these effects occur.

Through a richer understanding of the influences and mechanisms of generation, these experiments also tested various theories of the generation effect.

Active learning, which includes techniques such as paraphrasing information, selfexplaining, self-testing, and learning through experience, is a classic encoding strategy.

Championed by educators and studied by cognitive psychologists for nearly 40 years, the true pattern of the consequences of active generation, and the underlying mechanisms of the generation effect have remained elusive. In 1978, Slamecka and Graf (1978) demonstrated the positive effects of active generation on verbal item information by having participants generate antonyms, synonyms, categories, and rhymes to cues. These effects have since been demonstrated under conditions of intentional and incidental learning, and cued and uncued recognition and recall (Bertsch et al., 2007). They have also been extended to the domains of arithmetic problems (McNamara & Healy, 2000; R. W. Smith & Healy, 1998), pictures (Kinjo & Snodgrass, 2000), actions (Zimmer et al., 2001), and arguments (Petty, 1981). Further, active generation has proven beneficial in older adults (Taconnat et al., 2006; Taconnat & Isingrini, 2004), patients with various traumatic brain injuries, (Lengenfelder et al., 2007) and even in patients with mild cognitive impairment or early stages of Alzheimer’s Disease (Souliez et al., 1996).

Indeed, the experiments presented here demonstrate the power and versatility of the positive generation effect on item memory, which existed when employing various stimuli including synonyms, antonyms, idioms, pictures, and categories, when participants generated information covertly and overtly, and in front of a computer and in a scanner. Further, these positive generation effects persisted over a 24-hour delay and in the face of divided attention.

The cross-cultural Idiom experiments also demonstrated that active generation may be a universally beneficial encoding strategy, as the generation effect was as strong in China as it was in the United States. This is interesting, as a Chinese Confucian learning style is less similar on its face to active generation than is an American Socratic learning style (Tweed & Lehman, 2002).

At the neural level, active generation was associated with a broad set of regions that included the IFG, MFG, ACC, PrC, IPS, ITG, and LOC. Prefrontal activity in the IFG and MFG confirmed the role of executive control processes (Miller & Cohen, 2001; Shimamura, 2000,

2008) that modulate posterior cortical activity, thus engaging a prefrontal-posterior network involved in selecting, maintaining, and manipulating information in working memory.

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