Hippocampal-prefrontal engagement and dynamic causal interactions in the maturation of children's fact retrieval

Abstract

Children's gains in problem-solving skills during the elementary school years are characterized by shifts in the mix of problem-solving approaches, with inefficient procedural strategies being gradually replaced with direct retrieval of domain-relevant facts. We used a well-established procedure for strategy assessment during arithmetic problem solving to investigate the neural basis of this critical transition. We indexed behavioral strategy use by focusing on the retrieval frequency and examined changes in brain activity and connectivity associated with retrieval fluency during arithmetic problem solving in second- and third-grade (7- to 9-year-old) children. Children with higher retrieval fluency showed elevated signal in the right hippocampus, parahippocampal gyrus (PHG), lingual gyrus (LG), fusiform gyrus (FG), left ventrolateral PFC (VLPFC), bilateral dorsolateral PFC (DLPFC), and posterior angular gyrus. Critically, these effects were not confounded by individual differences in problem-solving speed or accuracy. Psychophysiological interaction analysis revealed significant effective connectivity of the right hippocampus with bilateral VLPFC and DLPFC during arithmetic problem solving. Dynamic causal modeling analysis revealed strong bidirectional interactions between the hippocampus and the left VLPFC and DLPFC. Furthermore, causal influences from the left VLPFC to the hippocampus served as the main top-down component, whereas causal influences from the hippocampus to the left DLPFC served as the main bottom-up component of this retrieval network. Our study highlights the contribution of hippocampal-prefrontal circuits to the early development of retrieval fluency in arithmetic problem solving and provides a novel framework for studying dynamic developmental processes that accompany children's development of problem-solving skills.

Figure 1

Behavioral results from strategy assessment. (A) Median RTs were shorter for trials in which a retrieval strategy was used, when compared with counting strategy use. (B) Individual differences showing retrieval fluency is correlated with faster RTs.

Figure 2

Behavioral results from the in-scanner addition task. (A) Children were significantly faster in their RTs for the control task compared with the addition task. (B) Children were significantly more accurate on the control task compared with the addition task. (C, D) Children with higher retrieval fluency were faster and more accurate on the addition task.

Figure 3

Brain responses associated with greater retrieval fluency. Activity levels were positively correlated with retrieval fluency in the right hippocampus and PHG, FG and LG, left VLPFC, bilateral DLPFC (B DLPFC), bilateral posterior angular gyrus (AG), right SPL, and superior occipital gyrus (SOG). No brain areas showed negative correlations with retrieval fluency. L = left; R = right.

Figure 4

PPI with the right hippocampus. Using the right hippocampus as an ROI (top-left inset), PPI analyses revealed regions that showed greater effective connectivity with the right hippocampus during the addition, compared with the control task. Greater connectivity was observed in the bilateral hippocampus (B hippocampus), bilateral VLPFC, bilateral DLPFC, left SFG, bilateral insula, bilateral LG, bilateral PHG, and right FG. L = left; R = right.

Figure 5

MDS modeling of hippocampal–prefrontal retrieval network. Analysis of causal interactions between left VLPFC, left and right DLPFC, and right hippocampus. Both the left VLPFC and the left DLPFC showed highly significant direct causal influences with the right hippocampus (all ps < .00001). Causal links depicted were all significant using p < .01, after Bonferroni correction. L = left; R = right.