Elsevier

NeuroImage

Volume 37, Issue 1, 1 August 2007, Pages 290-299
NeuroImage

A brief thought can modulate activity in extrastriate visual areas: Top-down effects of refreshing just-seen visual stimuli

https://doi.org/10.1016/j.neuroimage.2007.05.017Get rights and content

Abstract

Current models of executive function hold that the internal representations of stimuli used during reflective thought are maintained in the same posterior cortical regions initially activated during perception, and that activity in such regions is modulated by top-down signals originating in prefrontal cortex. In an event-related functional magnetic resonance imaging study, we presented participants with two pictures simultaneously, a face and a scene, immediately followed either by a repetition of one of the pictures (perception) or by a cue to think briefly of one of the just-seen, but no longer present, pictures (refreshing, a reflective act). Refreshing faces and scenes modulated activity in the fusiform face area (FFA) and parahippocampal place area (PPA), respectively, as well as other regions exhibiting relative perceptual selectivity for either faces or scenes. Four scene-selective regions (lateral precuneus, retrosplenial cortex, PPA, and middle occipital gyrus) showed an anatomical gradient of responsiveness to top-down reflective influences versus bottom-up perceptual influences. These results demonstrate that a brief reflective act can modulate posterior cortical activity in a stimulus-specific manner, suggesting that such modulatory mechanisms are engaged even during transient ongoing thought. Our findings are consistent with the hypothesis that refreshing is a component of more complex modulatory operations such as working memory and mental imagery, and that refresh-related activity may thus contribute to the common activation patterns seen across different cognitive tasks.

Introduction

Contemporary theories of cognitive control propose that a primary role of the prefrontal cortex (PFC) is to produce top-down signals that influence levels of neural activity, and hence the flow of information processing, in other brain regions (Miller and Cohen, 2001). Such top-down modulation is likely a key mechanism underlying working memory (WM; Baddeley, 1992, Baddeley and Hitch, 1974) and reflective processes more generally (e.g., the maintenance, manipulation, encoding, and revival of representations of external stimuli, ideas, beliefs, and goals; Johnson, 1992, Johnson and Hirst, 1993). For example, one current influential hypothesis about WM is that representations of recently perceived external stimuli that are no longer present are maintained by the top-down activation of posterior regions that are initially active during the perception of such stimuli (Curtis and D'Esposito, 2003, Petrides, 1994, Ranganath and D'Esposito, 2005, Ruchkin et al., 2003).

Evidence for this view has been obtained by examining activity in regions of inferior temporal cortex that are differentially responsive to different classes of stimuli. For example, the fusiform face area (FFA) and the parahippocampal place area (PPA) are known to activate differentially to faces and scenes, respectively, during perception (Epstein and Kanwisher, 1998, Kanwisher et al., 1997, Maguire et al., 2001, McCarthy et al., 1997). Several studies have demonstrated that these areas also exhibit selective delay-period activity during WM maintenance of the appropriate class of stimuli (e.g., Druzgal and D'Esposito, 2003, Postle et al., 2003, Ranganath et al., 2004). These findings are consistent with the idea that selective reflection produces top-down modulation of activity in posterior perceptual cortical regions.

Presumably, such top-down modulation occurs not only when individuals attempt to hold a target class of stimuli in mind over several seconds, but also during the more transient processes commonly engaged during ongoing thought. Often we do not know in advance which information will be relevant later and do not have the time, or a reason, to actively rehearse it for several seconds. In addition to extended maintenance that may be driven in a prospective top-down fashion, we often have to make rapid selections from activated representations based on information that becomes available only after the stimulus has disappeared. Furthermore, we may foreground or sustain such retroactively selected representations only very briefly as part of a continually changing stream of mental representations. The current study examined whether posterior areas show selective activation when a top-down signal is retroactive and relatively brief.

We obtained evidence relevant to this question by examining posterior activity associated with the cognitive process of refreshing. Refreshing is thinking briefly of an already active representation of a thought or percept (Johnson, 1992, Johnson and Hirst, 1993). Like perceptual repetition, refreshing often benefits memory for the targeted information (e.g., Johnson et al., 2005). Johnson and colleagues (Johnson et al., 2005, Raye et al., 2007) have proposed that refreshing serves both maintenance and executive functions, depending on task circumstances. They have identified PFC regions associated with refreshing, including refreshing selectively from among several active representations of the same type (e.g., words; Johnson et al., 2005; Raye et al., under review). Previous studies of refreshing have reported refresh-related activity in posterior areas as well as PFC (supramarginal gyrus, precuneus; Raye et al., 2002, Raye et al., 2007), and refreshing is assumed to involve interactions between PFC and posterior areas (including top-down modulation). Those studies were not designed, however, to demonstrate selective top-down modulation of activity in content-specific posterior areas. The present study thus asked whether a brief instance of refreshing would be sufficient to induce stimulus-specific changes in activity in extrastriate visual regions such as those sensitive to face and place information.

We presented participants with an initial display consisting of two stimuli, a face and a scene, followed by a cue to refresh (briefly think of) one of the stimuli. We examined the differential effects of refreshing a face or scene on activity in regions that included FFA, PPA, and other regions differentially sensitive to faces and scenes, as identified in a separate functional localizer task. This design allowed us to demonstrate that a transient reflective thought could indeed produce changes in posterior cortical activity that were related to which specific active representation was refreshed. We also compared the effect of refreshing a stimulus to seeing it again and identified scene-selective posterior areas where top-down (i.e., reflectively driven) and bottom-up (i.e., perceptually driven) processing produced similar or different levels of activity.

Section snippets

Participants

Fifteen young, right-handed, self-reported healthy adults with normal or corrected-to-normal vision participated in the study (6 males, mean ageĀ =Ā 21.3Ā yearsĀ Ā±Ā 2.7). One additional participant was excluded due to head movements during scanning. Participants were screened for MRI compatibility, gave written informed consent, and were compensated. The procedure was approved by the Yale University School of Medicine Human Investigation Committee.

Localizer task

In the scanner, all participants performed a standard

Top-down effects of refreshing in FFA/PPA

We first examined activity in the primary posterior areas of interest, FFA and PPA, during the two Refresh conditions: Ref_F and Ref_S. We predicted that we would find greater activity in PPA for refreshing scenes than faces, and greater activity in FFA for refreshing faces than scenes.

Example PPA and FFA locations for a representative participant are shown in Fig. 2A, and parameter estimates of activation for the two Refresh conditions are presented in Fig. 2B. A clear top-down effect was seen

Discussion

The present study demonstrates that (1) refreshing, a relatively simple cognitive process that reliably shows activation in PFC, is capable of modulating activity in FFA and PPA; (2) refreshing can also modulate activity in several other, less-well-studied areas exhibiting relative specificity for faces or scenes; and (3) among scene-selective regions, there was an anatomical gradient whereby perception evoked more activity than reflection in more posterior-inferior areas, but perception and

Acknowledgments

This research was supported by NIH AG15793. We thank the staff of the Yale Magnetic Resonance Research Center for their help with fMRI data acquisition.

References (51)

  • A. Mazard et al.

    Neural impact of the semantic content of visual mental images and visual percepts

    Brain Res. Cogn. Brain Res.

    (2005)
  • E. Mellet et al.

    Reopening the mental imagery debate: lessons from functional anatomy

    NeuroImage

    (1998)
  • B.R. Postle et al.

    Seeking the neural substrates of visual working memory storage

    Cortex

    (2003)
  • C. Ranganath et al.

    Directing the mind's eye: prefrontal, inferior and medial temporal mechanisms for visual working memory

    Curr. Opin. Neurobiol.

    (2005)
  • C. Ranganath et al.

    Category-specific modulation of inferior temporal activity during working memory encoding and maintenance

    Brain Res. Cogn. Brain Res.

    (2004)
  • C.L. Raye et al.

    Neuroimaging a single thought: dorsolateral PFC activity associated with refreshing just-activated information

    NeuroImage

    (2002)
  • C.L. Raye et al.

    Refreshing: a minimal executive function

    Cortex

    (2007)
  • A.D. Baddeley

    Working memory

    Science

    (1992)
  • A.D. Baddeley et al.

    Working memory

  • P.E. Downing et al.

    Domain specificity in visual cortex

    Cereb. Cortex

    (2006)
  • T.J. Druzgal et al.

    Dissecting contributions of prefrontal cortex and fusiform face area to face working memory

    J. Cogn. Neurosci.

    (2003)
  • R. Epstein et al.

    A cortical representation of the local visual environment

    Nature

    (1998)
  • L. Freire et al.

    What is the best similarity measure for motion correction in fMRI time series?

    IEEE Trans. Med. Imaging

    (2002)
  • A. Gazzaley et al.

    Top-down enhancement and suppression of the magnitude and speed of neural activity

    J. Cogn. Neurosci.

    (2005)
  • B. Gonsalves et al.

    Neural evidence that vivid imagining can lead to false remembering

    Psychol. Sci.

    (2004)
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