Atypical neuronal activation during a spatial working memory task in 13-year-old very preterm children

Abstract

Children born very preterm (VP; <32 weeks' gestational age) are at risk for unfavorable outcomes in several cognitive domains, including spatial working memory (WM). The underlying neural basis of these cognitive impairments is poorly understood. We investigated differences in neuronal activation during spatial WM using a backward span (BS) task relative to a control (C) task in 45 VP children and 19 term-born controls aged 13 years. VP children showed significantly more activation in the bilateral superior frontal gyrus and significantly less activation in the left parahippocampal gyrus compared with controls. We further explored the distinct contributions of maintenance and manipulation processes of WM using forward span (FS)>C and BS > FS, respectively. There were no significant group differences in neuronal activation for FS > C. However, BS > FS revealed that VP children had significantly greater activation in the left middle frontal gyrus, in the left superior parietal gyrus and right cerebellar tonsil, and significantly less activation in the right precentral and postcentral gyrus and left insula compared with controls. Taken together these results suggest that VP children at 13 years of age show an atypical neuronal activation during spatial WM, specifically related to manipulation of spatial information in WM. It is unclear whether these findings reflect delayed maturation and/or recruitment of alternative neuronal networks as a result of neuroplasticity. Hum Brain Mapp 38:6172-6184, 2017. © 2017 Wiley Periodicals, Inc.

Keywords: behavior and behavior mechanisms; child development; memory; mental competency; mental processes; neurobehavioral manifestations; premature birth; short-term.

Figure 1

Presentation of the fMRI task offline (A) and during scanning (B). Children able to complete the fMRI task offline attempted the same offline task in a mock MRI, using a 4‐button response device (C). In the FS task, a 3 s cue phase with the text “Forward!” appeared in the middle of the screen, followed by a 5 s encoding phase with 3 flashing boxes at a rate of 1 per second, and a 5 s retrieval phase, during which children were required to repeat the sequence using the response device (D).

Figure 2

Significant activation for Backward Span (BS)>Control (C) Task, after cluster correction (Z > 2.3 and P < 0.05). Heat maps and heat bar represent positive (warm color) and negative (cool color) Z scores. Transverse slice view is labeled with Z coordinates in MNI space as indicated by the sagittal slice view, unless otherwise specified. Graph bars represent mean % blood‐oxygen‐level dependent (BOLD) signal change within significant clusters revealed in very preterm (VP) > controls. Error bars represent 95% confidence intervals. Abbreviations: A = anterior; R = right.

Figure 3

Significant activation for forward span (FS) > control (C) task, after cluster correction (Z > 2.3 and P < 0.05). Heat maps and heat bar represent positive Z scores. Transverse slice view is labeled with Z coordinates in MNI space as indicated by the sagittal slice view. Abbreviations: VP = very preterm; A = anterior; R = right; n.s. =not significant.

Figure 4

Significant activation for Backward Span (BS)>Forward Span (FS) Task, after cluster correction (Z > 2.3 and P < 0.05). Heat maps and heat bar represent positive (warm color) and negative (cool color) Z scores. Transverse slice view is labeled with Z coordinates in MNI space as indicated by the sagittal slice view. Graph bars represent mean % blood‐oxygen‐level dependent (BOLD) signal change within significant clusters revealed in very preterm (VP) > controls. Error bars represent 95% confidence intervals. Abbreviations: A = anterior; R = right.