Differential engagement of brain regions within a 'core' network during scene construction

Abstract

Reliving past events and imagining potential future events engages a well-established "core" network of brain areas. How the brain constructs, or reconstructs, these experiences or scenes has been debated extensively in the literature, but remains poorly understood. Here we designed a novel task to investigate this (re)constructive process by directly exploring how naturalistic scenes are built up from their individual elements. We "slowed-down" the construction process through the use of auditorily presented phrases describing single scene elements in a serial manner. Participants were required to integrate these elements (ranging from three to six in number) together in their imagination to form a naturalistic scene. We identified three distinct sub-networks of brain areas, each with different fMRI BOLD response profiles, favouring specific points in the scene construction process. Areas including the hippocampus and retrosplenial cortex had a biphasic profile, activating when a single scene element was imagined and when 3 elements were combined together; regions including the intra-parietal sulcus and angular gyrus steadily increased activity from 1 to 3 elements; while activity in areas such as lateral prefrontal cortex was observed from the second element onwards. Activity in these sub-networks did not increase further when integrating more than three elements. Participants confirmed that three elements were sufficient to construct a coherent and vivid scene, and once this was achieved, the addition of further elements only involved maintenance or small changes to that established scene. This task offers a potentially useful tool for breaking down scene construction, a process that may be key to a range of cognitive functions such as episodic memory, future thinking and navigation.

Fig. 1

Task design. Timeline of an example trial, in this case a construction trial with four elements. See Section 2 for full details.

Fig. 2

Mean difficulty ratings during scanning. As expected, difficulty (1 = easy…5 = difficult) increased with increasing numbers of elements in construction trials. This was mirrored by ratings for the control trials (see also Section 2 and Table S1 in Supplementary Materials).

Fig. 3

Mean ratings of vividness and perceived integration during scanning. Vividness (1 = not vivid…5 = very vivid) and perceived integration between the elements (1 = not integrated…5 = very integrated) decreased with increasing numbers of elements in construction trials (see also Sections 2 and 3 and Table S1 in Supplementary Materials).

Fig. 4

Time courses of activity in brain areas associated with scene construction. This figure summarises the main areas activated in the inter-element contrasts simultaneously on one set of brain slices, with the activations colour coded dependent on response profile. The activations (left panel) are thresholded here at p < 0.005 (uncorrected) for display purposes, and shown on the averaged structural MRI scan of the 19 participants. Areas in red, including left hippocampus, retrosplenial cortex, bilateral parahippocampal gyrus, had a biphasic response, being most active for elements 1 and 3. By contrast, areas shown in blue, including IPS and angular gyrus, had responses that peaked at element 3. While regions shown in green, including dorsolateral prefrontal and lateral temporal cortices, peaked at element 2. To the right are example beta plots for each response type taken from a contrast neutral with respect to element position (all elements > all controls), as well as inset images of the actual activations and exact coordinates from the neutral contrast. In the Supplementary Materials (Fig. S1) we include a range of other examples of beta plots derived from the all elements > all controls contrast to further illustrate the three response profiles. ‘E’ on the x-axis refers to the number of elements received at that point in the scene construction process. The y-axis represents arbitrary unit of the parameter estimates (betas). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of the article.)