Memory: enduring traces of perceptual and reflective attention

Abstract

Attention and memory are typically studied as separate topics, but they are highly intertwined. Here we discuss the relation between memory and two fundamental types of attention: perceptual and reflective. Memory is the persisting consequence of cognitive activities initiated by and/or focused on external information from the environment (perceptual attention) and initiated by and/or focused on internal mental representations (reflective attention). We consider three key questions for advancing a cognitive neuroscience of attention and memory: to what extent do perception and reflection share representational areas? To what extent are the control processes that select, maintain, and manipulate perceptual and reflective information subserved by common areas and networks? During perception and reflection, to what extent are common areas responsible for binding features together to create complex, episodic memories and for reviving them later? Considering similarities and differences in perceptual and reflective attention helps integrate a broad range of findings and raises important unresolved issues.

Figure 1. Comparing reflective (refresh) and perceptual (orient) attention

Task design. (A) Refresh condition: Participants first saw a fixation cross, then a face and a scene picture, followed by an arrow cueing them to briefly think back to, or visualize, either the face or the scene, as indicated by the direction of the arrow. (B) Orient condition: Participants first saw an arrow, cueing them to look only at the picture on the left or right side of the screen. This was followed by a face and a scene picture, and then a fixation cross. (C) Act (control) condition: Participants first saw a fixation cross, then a face and a scene picture, followed by a gray square cueing them simply to press a button (and not think about either picture). (D–J) Activation for each of seven scene-selective regions of interest across the five conditions of the task. (K) Locations of these regions overlaid on the MNI single-subject template brain (Adapted from Johnson and Johnson, 2009, Journal of Cognitive Neuroscience).

Figure 2. Comparing perceptual attention and reflective attention

(A) Regions active for high versus low selection in a perceptual selection task (top), memory selection task (middle), and the conjunction of both tasks (bottom). (B) Regions unique to perceptual selection (left) and memorial selection (right). (C) Differential activation of the rostromedial and rostrolateral PFC during attentional orientation to external and internal information, respectively. Center: Brain activation map showing significantly stronger activation of the anterior rostromedial PFC during the orientation of attention to external as compared to internal information (blue), and significantly stronger activation of the rostrolateral PFC during the orientation of attention to internal as compared to external information (red). The scale below shows the color-coding of the displayed T-values. Periphery: Parameter estimates extracted from the rostromedial PFC (left side) and rostrolateral PFC (right side) color coded for the different tasks (blue: Externally Oriented position task; purple: Externally Oriented target task; red: Internally Oriented task). [(A) and (B) from Nee and Jonides (2009, Neuroimage); (C) from Henseler et al. (2011, Neuroimage).

Figure 3. Perceptual and reflective resolution of competition

(A) Activity in posterior DLPFC (left SFS) during perceptual discrimination of faces vs. houses showing a higher response to suprathreshold images of faces and houses relative to perithreshold images, and a correlation with the difference in activity in face vs. house selective areas, suggesting that this region integrates evidence from sensory processing areas to make perceptual decisions. (B) Signal changes in the posterior portion of the DLPFC predicted task performance. Points represent average BOLD change and performance for each condition (suprathreshold face, perithreshold face, perithreshold house and suprathreshold house) and participant. (C) Frontoparietal regions that were more active during memory retrieval for trials on which a classifier showed less activity for a target category under conditions of A–B, A–C interference (B and C were faces and scenes). (D) Responses in several regions of interest was characterized by marked activation for AC trials associated with low-fidelity reactivation. (Panels A and B adapted from Heekeren et al., 2004, Nature; C and D adapted from Kuhl et al., 2011, PNAS).