Dissociation between Dorsal and Ventral Posterior Parietal Cortical Responses to Incidental Changes in Natural Scenes

Spiers HJ (2013) Dissociation between Dorsal and Ventral Posterior Parietal Cortical Responses to Incidental Changes in Natural Scenes. PLoS ONE 8(7): e67988. doi:10.1371/journal.pone.0067988 Dissociation between Dorsal and Ventral Posterior Parietal Cortical Responses to Incidental Changes in Natural Scenes Lorelei R. Howard 0 Dharshan Kumaran 0 H. Freyja O lafsdo ttir 0 Hugo J. Spiers 0 Chris Chambers, Cardiff University, United Kingdom 0 1 Institute of Behavioural Neuroscience, Research Department of Cognitive, Perceptual and Brain Sciences, Division of Psychology and Language Sciences, University College London , London , United Kingdom , 2 Institute of Cognitive Neuroscience, University College London , London , United Kingdom Background: The posterior parietal cortex (PPC) is thought to interact with the medial temporal lobe (MTL) to support spatial cognition and topographical memory. While the response of medial temporal lobe regions to topographical stimuli has been intensively studied, much less research has focused on the role of PPC and its functional connectivity with the medial temporal lobe. Methodology/Principle Findings: Here we report a dissociation between dorsal and ventral regions of PPC in response to different types of change in natural scenes using an fMRI adaptation paradigm. During scanning subjects performed an incidental target detection task whilst viewing trial unique sequentially presented pairs of natural scenes, each containing a single prominent object. We observed a dissociation between the superior parietal gyrus and the angular gyrus, with the former showing greater sensitivity to spatial change, and the latter showing greater sensitivity to scene novelty. In addition, we observed that the parahippocampal cortex has increased functional connectivity with the angular gyrus, but not superior parietal gyrus, when subjects view change to the scene content. Conclusions/Significance: Our findings provide support for proposed dissociations between dorsal and ventral regions of PPC and suggest that the dorsal PPC may support the spatial coding of the visual environment even when this information is incidental to the task at hand. Further, through revealing the differential functional interactions of the SPG and AG with the MTL our results help advance our understanding of how the MTL and PPC cooperate to update representations of the world around us. - Our ability to learn, recall and navigate large-scale space is thought to rely on a network including the posterior parietal cortex (PPC), retrosplenial cortex and medial temporal lobe (MTL) [16]. Among these regions, the PPC has been implicated in egocentric spatial processing (e.g. [1,7]). However, the contribution of different subregions within PPC to processing topographical stimuli remains unclear. Some neuroimaging studies find increased activity in the angular gyrus (AG) [810], others find increased activity in superior parietal gyrus (SPG) [4,11], while several report co-activation of AG and SPG [1220]. Previous neuroimaging work has elucidated the role of the PPC in visual attention [21,22]. These studies have provided evidence that a dorsal system (including the SPG) provides top-down control of visual attention and a ventral system (including the AG) supports bottom-up stimulus detection and re-orienting to salient events [2124]. Recent work also suggests that such a dorsal/ ventral division may also apply to episodic memory processes [25 37]. Here we use an fMRI adaptation (fMRA) approach to probe the nature of information represented within regions of the PPC. Whilst fMRA has been widely used to characterize the neural representations and computations in regions within the ventral visual stream (e.g. [38]) and more recently the MTL (e.g. [39]), this technique has been less often used to study the nature of information processing carried out by the PPC (although see e.g. [40]). Whilst an early study [41] which used a broadly related approach (i.e. oddball paradigm) observed both object and location coding in the PPC, it did not illuminate a putative dissociation between the contribution of different posterior parietal regions (e.g. AG vs SPG), nor exclude the possibility that the observations could reflect coding of surprise engendered by the occurrence of oddballs. In recent work we used fMRA to explore the response of MTL regions to change in natural scenes and a parallel eye-tracking control study to examine saccadic responses to the same stimuli [42]. We reported a double dissociation between the parahippocampal cortex and the hippocampus, with the former responsive to change in the scene content and the latter responsive to a spatial change in the scene content. Here, by applying a set of new analyses to these data, we ask three main questions: firstly, what kind of information is coded within the PPC? Secondly, do different regions within the PPC (i.e. AG and SPG) code information in a similar fashion? Thirdly, does the functional connectivity between individual posterior parietal regions and the MTL differ during novelty processing? Despite recent evidence of dissociable connectivity between parietal regions and the MTL, both anatomically [43] and functionally during resting/default states [4447], there has been little examination of the functional connectivity between these regions during the processing of topographical stimuli. As such, understanding how parietal and MTL regions interact is important for constraining models in which they jointly support novelty processing [48], memory encoding and retrieval [26,30,33], and spatial memory [2]. We report a dissociation between the AG and the SPG: while the SPG was purely responsive to spatial change (i.e. and not to scene novelty), we find that the maximal response of the AG was to scene novelty findings that cannot be easily explained by differences in eye movements obtained in a separate behavioural study. We also observed an increase in functional connectivity between the AG and parahippocampal cortex in relation to scene novelty. Independent of this novelty response, increased activity in both AG and parahippocampal cortex was associated with subsequent familiarity for scenes re-presented post-scan. Our findings provide new insights into the types of neural representations supported by different regions within the PPC, and the nature of their interactions (i.e. functional connectivity) with regions within the MTL. Materials and Methods Experiment 1: fMRI The present study provides novel analyses of a previously published dataset. All aspects of the experimental materials and methodology are identical to those described in detail in the previously published manuscript; hence, we refer the reader to Howard et al. [42] for a full description of this section. Here, we provide a brief summary of the key aspects of the experimental materials and methods in addition to a detailed description of the new fMRI data (...truncated)