Attentional modulation of background connectivity between ventral visual cortex and the medial temporal lobe

Highlights

• Attention increases coupling of visual areas that process task-relevant information.

• May explain how information is prioritized for processing in medial temporal lobe.

• Visual cortex connects to PHC when scenes attended and to PRC when faces attended.

• Switching of background connectivity most pronounced for unselective visual voxels.

• Candidate mechanism for how attention can influence learning and memory behavior.

Abstract

Attention prioritizes information that is most relevant to current behavioral goals. This prioritization can be accomplished by amplifying neural responses to goal-relevant information and by strengthening coupling between regions involved in processing this information. Such modulation occurs within and between areas of visual cortex, and relates to behavioral effects of attention on perception. However, attention also has powerful effects on learning and memory behavior, suggesting that similar modulation may occur for memory systems. We used fMRI to investigate this possibility, examining how visual information is prioritized for processing in the medial temporal lobe (MTL). We hypothesized that the way in which ventral visual cortex couples with MTL input structures will depend on the kind of information being attended. Indeed, visual cortex was more coupled with parahippocampal cortex when scenes were attended and more coupled with perirhinal cortex when faces were attended. This switching of MTL connectivity was more pronounced for visual voxels with weak selectivity, suggesting that connectivity might help disambiguate sensory signals. These findings provide an initial window into an attentional mechanism that could have consequences for learning and memory.

Introduction

Attention during encoding enhances subsequent recognition memory and can modulate activity in regions of the medial temporal lobe (MTL) that support such memory (Carr et al., 2013, Dudukovic et al., 2011, Uncapher and Rugg, 2009, Yi and Chun, 2005). The purpose of the current study was to investigate a particular way in which attention might enhance MTL processing, inspired by studies about how attention modulates the visual system. Specifically, top-down attention has been shown to modulate the coupling between visual areas, strengthening functional connectivity between areas that code for attended information (Al-Aidroos et al., 2012, Bosman et al., 2012). By establishing such functional pathways, attention may improve the transmission of task-relevant information (Fries, 2005).

If attention modulates coupling at the highest levels of the visual hierarchy, this mechanism could also prioritize which information is transmitted to the MTL and ultimately the hippocampus. Parahippocampal cortex (PHC) and perirhinal cortex (PRC) provide an interface between the visual system and the hippocampus and thus are good targets for evaluating attentional modulation of functional connectivity. PHC and PRC have different functional characteristics (Eichenbaum et al., 2007, Ranganath and Ritchey, 2012): for example, PHC processes spatial and contextual information such as scenes, whereas PRC processes items, such as objects and faces (Davachi, 2006, Lee et al., 2012).

We thus manipulated selective attention to scenes and faces in composite images (Al-Aidroos et al., 2012, O’Craven et al., 1999, Yi and Chun, 2005), predicting that this would influence functional connectivity with PHC and PRC. Much of ventral visual cortex processes low- and mid-level features that are common to both scenes and faces (e.g., contours, colors, textures) and these areas might couple with distinct MTL regions depending on attention. In particular, we hypothesized that ventral visual cortex would show stronger functional connectivity with PHC during scene attention and with PRC during face attention.

To measure functional connectivity, we examined the correlation of BOLD activity over time between regions or voxels. This approach has long been used to uncover the coupling between brain regions during rest (Fox & Raichle, 2007). However, such measures can be confounded during tasks because regions that respond synchronously to stimuli will be spuriously correlated over time even in the absence of any interaction. There are several approaches for dealing with this issue (Friston et al., 1997, Rissman et al., 2004). Here we adopt a “background connectivity” approach in which stimulus-evoked responses and noise sources are projected out of the data and correlations are calculated in the residuals during different experimental conditions (Al-Aidroos et al., 2012, Duncan et al., 2014, Griffis et al., 2015, Norman-Haignere et al., 2012, Tompary et al., 2015). The resulting connectivity reflects spontaneous, intrinsic interactions within the functional networks engaged by each condition.

By comparing background connectivity across epochs in which attention was oriented to scenes vs. faces, we identified patterns of PHC and PRC connectivity selective to each attentional state. We predicted that areas of ventral visual cortex would show higher background connectivity both with PHC during scene attention and with PRC during face attention. Moreover, we predicted that such switching would be most pronounced for voxels in ventral visual cortex that responded robustly to both scenes and faces, as connectivity is needed in such cases to determine how the information conveyed by this activity will be processed (Fries, 2005). That is, the influence of voxels with unselective evoked activity in broader networks might arise from selective functional connectivity.