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Timing and sequence of brain activity in top-down control of visual-spatial attention.

Grent-'t-Jong T, Woldorff MG - PLoS Biol. (2007)

Bottom Line: These results indicate an activation sequence of key components of the attentional-control brain network, providing insight into their functional roles.More specifically, these results suggest that voluntary attentional orienting is initiated by medial portions of frontal cortex, which then recruit medial parietal areas.Together, these areas then implement biasing of region-specific visual-sensory cortex to facilitate the processing of upcoming visual stimuli.

View Article: PubMed Central - PubMed

Affiliation: Neuroscience, Duke University, Durham, North Carolina, United States of America.

ABSTRACT
Recent brain imaging studies using functional magnetic resonance imaging (fMRI) have implicated a frontal-parietal network in the top-down control of attention. However, little is known about the timing and sequence of activations within this network. To investigate these timing questions, we used event-related electrical brain potentials (ERPs) and a specially designed visual-spatial attentional-cueing paradigm, which were applied as part of a multi-methodological approach that included a closely corresponding event-related fMRI study using an identical paradigm. In the first 400 ms post cue, attention-directing and control cues elicited similar general cue-processing activity, corresponding to the more lateral subregions of the frontal-parietal network identified with the fMRI. Following this, the attention-directing cues elicited a sustained negative-polarity brain wave that was absent for control cues. This activity could be linked to the more medial frontal-parietal subregions similarly identified in the fMRI as specifically involved in attentional orienting. Critically, both the scalp ERPs and the fMRI-seeded source modeling for this orienting-related activity indicated an earlier onset of frontal versus parietal contribution ( approximately 400 versus approximately 700 ms). This was then followed ( approximately 800-900 ms) by pretarget biasing activity in the region-specific visual-sensory occipital cortex. These results indicate an activation sequence of key components of the attentional-control brain network, providing insight into their functional roles. More specifically, these results suggest that voluntary attentional orienting is initiated by medial portions of frontal cortex, which then recruit medial parietal areas. Together, these areas then implement biasing of region-specific visual-sensory cortex to facilitate the processing of upcoming visual stimuli.

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Evidence for Robustness of the Four-Source Frontal-Parietal Model of the Attentional Orienting Activity(A) Explained variance of three different source configurations (frontal only, parietal only, and both frontal and parietal) for the grand-average (n = 13) difference-wave activity between attend and interpret cue responses. These were computed across time (500–1,900 ms) in windows of 200 ms, using the locations and orientations of the sources from the initial fMRI-seeded solution. Note that in the earlier windows, the solution with only two frontal sources (thin black line) explains the variance in the data very well (and better than the solution with only two parietal sources). But later in time, both frontal and parietal sources (thick black line) are needed to explain the data.(B) Topographic distributions of the grand-average (n = 13) attentional-orienting activity at 500–600 ms (upper left map), at 1,100–1,200 ms (lower left map), and the calculated difference between these. Note that the residual activity after the subtraction has a clearly posterior parietal distribution, consistent with a model in which additional posterior sources activate later, rather than a model with only anterior sources that just become more strongly activated over time.(C) Same as (B) but with the attentional-orienting activity between 500–600 ms being scaled in amplitude first, before the subtraction from the activity during the distribution at the later window (i.e., amplitudes at all channels from the early activity were first multiplied by a factor 1.6 to approximately match the amplitude of the midfrontal activity in the later window between 1,100–1,200 ms). Note that the frontal activity is now even more subtracted out, but there still remains clear activity with a posterior parietal maximum.
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pbio-0050012-g004: Evidence for Robustness of the Four-Source Frontal-Parietal Model of the Attentional Orienting Activity(A) Explained variance of three different source configurations (frontal only, parietal only, and both frontal and parietal) for the grand-average (n = 13) difference-wave activity between attend and interpret cue responses. These were computed across time (500–1,900 ms) in windows of 200 ms, using the locations and orientations of the sources from the initial fMRI-seeded solution. Note that in the earlier windows, the solution with only two frontal sources (thin black line) explains the variance in the data very well (and better than the solution with only two parietal sources). But later in time, both frontal and parietal sources (thick black line) are needed to explain the data.(B) Topographic distributions of the grand-average (n = 13) attentional-orienting activity at 500–600 ms (upper left map), at 1,100–1,200 ms (lower left map), and the calculated difference between these. Note that the residual activity after the subtraction has a clearly posterior parietal distribution, consistent with a model in which additional posterior sources activate later, rather than a model with only anterior sources that just become more strongly activated over time.(C) Same as (B) but with the attentional-orienting activity between 500–600 ms being scaled in amplitude first, before the subtraction from the activity during the distribution at the later window (i.e., amplitudes at all channels from the early activity were first multiplied by a factor 1.6 to approximately match the amplitude of the midfrontal activity in the later window between 1,100–1,200 ms). Note that the frontal activity is now even more subtracted out, but there still remains clear activity with a posterior parietal maximum.

Mentions: Sixth, additional analyses were performed to assess the relative contribution of the frontal and parietal sources over the entire time period of significant sustained activity. More specifically, the explained variance was computed in successive 200-ms windows between 500–1,900 ms using the frontal sources alone, the parietal sources alone, and the frontal and parietal sources combined (Figure 4A). The figure reaffirms what was noted above, namely that in the early windows, the two medial frontal sources alone provided a particularly good fit by themselves and considerably better than the parietal locations alone. Thereafter, the frontal sources by themselves still explained most of the variance in the data, but substantially less well. This could be taken as further evidence that additional sources had become active in the later part of the window. Indeed, as shown in Figure 4A, adding the two parietal sources in the later part of the time window substantially improved the fit, whereas they added little in the earlier time range.


Timing and sequence of brain activity in top-down control of visual-spatial attention.

Grent-'t-Jong T, Woldorff MG - PLoS Biol. (2007)

Evidence for Robustness of the Four-Source Frontal-Parietal Model of the Attentional Orienting Activity(A) Explained variance of three different source configurations (frontal only, parietal only, and both frontal and parietal) for the grand-average (n = 13) difference-wave activity between attend and interpret cue responses. These were computed across time (500–1,900 ms) in windows of 200 ms, using the locations and orientations of the sources from the initial fMRI-seeded solution. Note that in the earlier windows, the solution with only two frontal sources (thin black line) explains the variance in the data very well (and better than the solution with only two parietal sources). But later in time, both frontal and parietal sources (thick black line) are needed to explain the data.(B) Topographic distributions of the grand-average (n = 13) attentional-orienting activity at 500–600 ms (upper left map), at 1,100–1,200 ms (lower left map), and the calculated difference between these. Note that the residual activity after the subtraction has a clearly posterior parietal distribution, consistent with a model in which additional posterior sources activate later, rather than a model with only anterior sources that just become more strongly activated over time.(C) Same as (B) but with the attentional-orienting activity between 500–600 ms being scaled in amplitude first, before the subtraction from the activity during the distribution at the later window (i.e., amplitudes at all channels from the early activity were first multiplied by a factor 1.6 to approximately match the amplitude of the midfrontal activity in the later window between 1,100–1,200 ms). Note that the frontal activity is now even more subtracted out, but there still remains clear activity with a posterior parietal maximum.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1761048&req=5

pbio-0050012-g004: Evidence for Robustness of the Four-Source Frontal-Parietal Model of the Attentional Orienting Activity(A) Explained variance of three different source configurations (frontal only, parietal only, and both frontal and parietal) for the grand-average (n = 13) difference-wave activity between attend and interpret cue responses. These were computed across time (500–1,900 ms) in windows of 200 ms, using the locations and orientations of the sources from the initial fMRI-seeded solution. Note that in the earlier windows, the solution with only two frontal sources (thin black line) explains the variance in the data very well (and better than the solution with only two parietal sources). But later in time, both frontal and parietal sources (thick black line) are needed to explain the data.(B) Topographic distributions of the grand-average (n = 13) attentional-orienting activity at 500–600 ms (upper left map), at 1,100–1,200 ms (lower left map), and the calculated difference between these. Note that the residual activity after the subtraction has a clearly posterior parietal distribution, consistent with a model in which additional posterior sources activate later, rather than a model with only anterior sources that just become more strongly activated over time.(C) Same as (B) but with the attentional-orienting activity between 500–600 ms being scaled in amplitude first, before the subtraction from the activity during the distribution at the later window (i.e., amplitudes at all channels from the early activity were first multiplied by a factor 1.6 to approximately match the amplitude of the midfrontal activity in the later window between 1,100–1,200 ms). Note that the frontal activity is now even more subtracted out, but there still remains clear activity with a posterior parietal maximum.
Mentions: Sixth, additional analyses were performed to assess the relative contribution of the frontal and parietal sources over the entire time period of significant sustained activity. More specifically, the explained variance was computed in successive 200-ms windows between 500–1,900 ms using the frontal sources alone, the parietal sources alone, and the frontal and parietal sources combined (Figure 4A). The figure reaffirms what was noted above, namely that in the early windows, the two medial frontal sources alone provided a particularly good fit by themselves and considerably better than the parietal locations alone. Thereafter, the frontal sources by themselves still explained most of the variance in the data, but substantially less well. This could be taken as further evidence that additional sources had become active in the later part of the window. Indeed, as shown in Figure 4A, adding the two parietal sources in the later part of the time window substantially improved the fit, whereas they added little in the earlier time range.

Bottom Line: These results indicate an activation sequence of key components of the attentional-control brain network, providing insight into their functional roles.More specifically, these results suggest that voluntary attentional orienting is initiated by medial portions of frontal cortex, which then recruit medial parietal areas.Together, these areas then implement biasing of region-specific visual-sensory cortex to facilitate the processing of upcoming visual stimuli.

View Article: PubMed Central - PubMed

Affiliation: Neuroscience, Duke University, Durham, North Carolina, United States of America.

ABSTRACT
Recent brain imaging studies using functional magnetic resonance imaging (fMRI) have implicated a frontal-parietal network in the top-down control of attention. However, little is known about the timing and sequence of activations within this network. To investigate these timing questions, we used event-related electrical brain potentials (ERPs) and a specially designed visual-spatial attentional-cueing paradigm, which were applied as part of a multi-methodological approach that included a closely corresponding event-related fMRI study using an identical paradigm. In the first 400 ms post cue, attention-directing and control cues elicited similar general cue-processing activity, corresponding to the more lateral subregions of the frontal-parietal network identified with the fMRI. Following this, the attention-directing cues elicited a sustained negative-polarity brain wave that was absent for control cues. This activity could be linked to the more medial frontal-parietal subregions similarly identified in the fMRI as specifically involved in attentional orienting. Critically, both the scalp ERPs and the fMRI-seeded source modeling for this orienting-related activity indicated an earlier onset of frontal versus parietal contribution ( approximately 400 versus approximately 700 ms). This was then followed ( approximately 800-900 ms) by pretarget biasing activity in the region-specific visual-sensory occipital cortex. These results indicate an activation sequence of key components of the attentional-control brain network, providing insight into their functional roles. More specifically, these results suggest that voluntary attentional orienting is initiated by medial portions of frontal cortex, which then recruit medial parietal areas. Together, these areas then implement biasing of region-specific visual-sensory cortex to facilitate the processing of upcoming visual stimuli.

Show MeSH