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Competing visual flicker reveals attention-like rivalry in the fly brain.

van Swinderen B - Front Integr Neurosci (2012)

Bottom Line: There is increasing evidence that invertebrates such as flies display selective attention (van Swinderen, 2011a), although parallel processing of simultaneous cues remains difficult to demonstrate in such tiny brains.Local field potential (LFP) activity in the fly brain is associated with stimulus selection and suppression (van Swinderen and Greenspan, 2003; Tang and Juusola, 2010), like in other animals such as monkeys (Fries et al., 2001), suggesting that similar processes may be working to control attention in vastly different brains.Visual competition dynamics in the fly brain were dependent on the rate of pattern presentation, suggesting that attention-like switching in insects is tuned to the pace of visual changes in the environment rather than simply the passage of time.

View Article: PubMed Central - PubMed

Affiliation: Queensland Brain Institute, The University of Queensland Brisbane, QLD, Australia.

ABSTRACT
There is increasing evidence that invertebrates such as flies display selective attention (van Swinderen, 2011a), although parallel processing of simultaneous cues remains difficult to demonstrate in such tiny brains. Local field potential (LFP) activity in the fly brain is associated with stimulus selection and suppression (van Swinderen and Greenspan, 2003; Tang and Juusola, 2010), like in other animals such as monkeys (Fries et al., 2001), suggesting that similar processes may be working to control attention in vastly different brains. To investigate selective attention to competing visual cues, I recorded brain activity from behaving flies while applying a method used in human attention studies: competing visual flicker, or frequency tags (Vialatte et al., 2010). Behavioral fixation in a closed-loop flight arena increased the response to visual flicker in the fly brain, and visual salience modulated responses to competing tags arranged in a center-surround pattern. Visual competition dynamics in the fly brain were dependent on the rate of pattern presentation, suggesting that attention-like switching in insects is tuned to the pace of visual changes in the environment rather than simply the passage of time.

No MeSH data available.


Related in: MedlinePlus

Visual novelty modulates frequency tag power. (A) Center-surround pattern, with visual changes in the center. The central object flickering at 7 or 9 Hz alternates between a 30° “+” and an “×,” with changes happening randomly every 5–50 s. The changing central object is surrounded by an unchanging 90° surround composed of dots flickering in synchrony at 7 or 9 Hz. (B) Epochs of behavioral fixation that included a visual change were analyzed for 7 and 9 Hz power. Power for either frequency 3 s after the change were contrasted, as a ratio, with 3 s before the event (dashed boxes). Blue trace: LFP; green line: image position, as in Figure 1C. (C) 7 and 9 Hz power after/before ratios for novelty events during fixation epochs, for either tag configuration. C, center; S, surround; n = 6 flies, *P < 0.05, **P < 0.01 by t-test compared to 1.0 (dashed line). (D) Novelty events occurring during flight epochs without fixation were analyzed for 7 and 9 Hz power before and after the visual change in the center. (E) 7 and 9 Hz power after/before ratios for novelty events during flight without fixation, for either tag configuration (n = same 6 flies as in C). (F) The compound 7 and 9 Hz pattern was moved around the fly with a period of 3 s (120°/s), with the center changing randomly (indicated by the red bar). LFP power for either frequency 3 s after the change were contrasted, as a ratio, with 3 s before the event (dashed boxes). Blue trace: LFP; green line: image position. (G) 7 and 9 Hz ratios for novelty events during non-flight epochs, for either tag configuration (C, center; S, surround). n = 12 flies, **P < 0.01, by t-test compared to 1.0 (dashed line = no effect). (H) The same data as in G was reanalyzed after binning into five separate categories depending on how much time had passed since the last change. A ratio was calculated for either tag, contrasting the 3 s after vs. 3 s before (dashed boxes). (I) 7 Hz (blue) and 9 Hz (red) ratios for visual changes during non-flight experiments, binned into 5 temporal groups. Shown are results for 7 Hz center vs. 9 Hz surround. n = 12 flies, **P < 0.01, by t-test compared to 1.0 (dashed line).
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Figure 3: Visual novelty modulates frequency tag power. (A) Center-surround pattern, with visual changes in the center. The central object flickering at 7 or 9 Hz alternates between a 30° “+” and an “×,” with changes happening randomly every 5–50 s. The changing central object is surrounded by an unchanging 90° surround composed of dots flickering in synchrony at 7 or 9 Hz. (B) Epochs of behavioral fixation that included a visual change were analyzed for 7 and 9 Hz power. Power for either frequency 3 s after the change were contrasted, as a ratio, with 3 s before the event (dashed boxes). Blue trace: LFP; green line: image position, as in Figure 1C. (C) 7 and 9 Hz power after/before ratios for novelty events during fixation epochs, for either tag configuration. C, center; S, surround; n = 6 flies, *P < 0.05, **P < 0.01 by t-test compared to 1.0 (dashed line). (D) Novelty events occurring during flight epochs without fixation were analyzed for 7 and 9 Hz power before and after the visual change in the center. (E) 7 and 9 Hz power after/before ratios for novelty events during flight without fixation, for either tag configuration (n = same 6 flies as in C). (F) The compound 7 and 9 Hz pattern was moved around the fly with a period of 3 s (120°/s), with the center changing randomly (indicated by the red bar). LFP power for either frequency 3 s after the change were contrasted, as a ratio, with 3 s before the event (dashed boxes). Blue trace: LFP; green line: image position. (G) 7 and 9 Hz ratios for novelty events during non-flight epochs, for either tag configuration (C, center; S, surround). n = 12 flies, **P < 0.01, by t-test compared to 1.0 (dashed line = no effect). (H) The same data as in G was reanalyzed after binning into five separate categories depending on how much time had passed since the last change. A ratio was calculated for either tag, contrasting the 3 s after vs. 3 s before (dashed boxes). (I) 7 Hz (blue) and 9 Hz (red) ratios for visual changes during non-flight experiments, binned into 5 temporal groups. Shown are results for 7 Hz center vs. 9 Hz surround. n = 12 flies, **P < 0.01, by t-test compared to 1.0 (dashed line).

Mentions: In previous work we have shown that visual salience, such as novelty, increases endogenous 20–30 Hz LFP activity in the Drosophila brain (van Swinderen and Greenspan, 2003; van Swinderen, 2007b; van Swinderen et al., 2009; van Swinderen and Brembs, 2010). To investigate whether such salience effects might change the responsiveness of flies to specific flicker frequencies, the preceding center-surround scenario was modified to include a changing central object, while the surround was left unchanged (Figure 3A). The central object alternated between a “+” and an “×” with random timing set between 5 s and 50 s. Power for either tag (7 or 9 Hz) after a change was compared to power before the change, expressed as a ratio, for either frequency (Figures 3B–G, see “Materials and Methods”). Changing the central object shape (but not the frequency tag) while the fly was actively fixating on the compound stimulus (Figure 3B, red bar) resulted in significantly increased 7 Hz power; effects on 9 Hz were less clear, although the tendency was for increased power following the change, regardless of the frequency tag (Figure 3C). Any significant effects were lost when novelty occurred (for the same animals) during flight without fixation (Figures 3D,E), although the trend to increased responsiveness was similar as for fixation, and these results were not significantly different from the novelty results under active fixation. In a separate set of open-loop experiments in non-flying animals (Figure 3F), changes to the central object shape also increased the power of the competing surrounding tag as well as the central tag, for either frequency combination (Figure 3G). This last, most significant set of results demonstrates that responsiveness to visual flicker can be modulated in the absence of flight behavior, and further, that a visual salience event (a novel object at the center) evokes increased responsiveness to a wider area than just the 30° central object that is changing. Together, the results so far suggest that novelty effects on the frequency tag may be independent of behavioral state of the animal. In addition, responsiveness to the competing tags 3 s after a change appears to be broad rather than selective. Since the novelty effect on tag power was also present in non-flying animals, subsequent analyses will focus on this more extensive dataset, specifically, looking at 7 Hz center competing with a 9 Hz surround (this combination produced a similar-sized novelty effect for both frequency tags, Figure 3G, left histograms).


Competing visual flicker reveals attention-like rivalry in the fly brain.

van Swinderen B - Front Integr Neurosci (2012)

Visual novelty modulates frequency tag power. (A) Center-surround pattern, with visual changes in the center. The central object flickering at 7 or 9 Hz alternates between a 30° “+” and an “×,” with changes happening randomly every 5–50 s. The changing central object is surrounded by an unchanging 90° surround composed of dots flickering in synchrony at 7 or 9 Hz. (B) Epochs of behavioral fixation that included a visual change were analyzed for 7 and 9 Hz power. Power for either frequency 3 s after the change were contrasted, as a ratio, with 3 s before the event (dashed boxes). Blue trace: LFP; green line: image position, as in Figure 1C. (C) 7 and 9 Hz power after/before ratios for novelty events during fixation epochs, for either tag configuration. C, center; S, surround; n = 6 flies, *P < 0.05, **P < 0.01 by t-test compared to 1.0 (dashed line). (D) Novelty events occurring during flight epochs without fixation were analyzed for 7 and 9 Hz power before and after the visual change in the center. (E) 7 and 9 Hz power after/before ratios for novelty events during flight without fixation, for either tag configuration (n = same 6 flies as in C). (F) The compound 7 and 9 Hz pattern was moved around the fly with a period of 3 s (120°/s), with the center changing randomly (indicated by the red bar). LFP power for either frequency 3 s after the change were contrasted, as a ratio, with 3 s before the event (dashed boxes). Blue trace: LFP; green line: image position. (G) 7 and 9 Hz ratios for novelty events during non-flight epochs, for either tag configuration (C, center; S, surround). n = 12 flies, **P < 0.01, by t-test compared to 1.0 (dashed line = no effect). (H) The same data as in G was reanalyzed after binning into five separate categories depending on how much time had passed since the last change. A ratio was calculated for either tag, contrasting the 3 s after vs. 3 s before (dashed boxes). (I) 7 Hz (blue) and 9 Hz (red) ratios for visual changes during non-flight experiments, binned into 5 temporal groups. Shown are results for 7 Hz center vs. 9 Hz surround. n = 12 flies, **P < 0.01, by t-test compared to 1.0 (dashed line).
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Figure 3: Visual novelty modulates frequency tag power. (A) Center-surround pattern, with visual changes in the center. The central object flickering at 7 or 9 Hz alternates between a 30° “+” and an “×,” with changes happening randomly every 5–50 s. The changing central object is surrounded by an unchanging 90° surround composed of dots flickering in synchrony at 7 or 9 Hz. (B) Epochs of behavioral fixation that included a visual change were analyzed for 7 and 9 Hz power. Power for either frequency 3 s after the change were contrasted, as a ratio, with 3 s before the event (dashed boxes). Blue trace: LFP; green line: image position, as in Figure 1C. (C) 7 and 9 Hz power after/before ratios for novelty events during fixation epochs, for either tag configuration. C, center; S, surround; n = 6 flies, *P < 0.05, **P < 0.01 by t-test compared to 1.0 (dashed line). (D) Novelty events occurring during flight epochs without fixation were analyzed for 7 and 9 Hz power before and after the visual change in the center. (E) 7 and 9 Hz power after/before ratios for novelty events during flight without fixation, for either tag configuration (n = same 6 flies as in C). (F) The compound 7 and 9 Hz pattern was moved around the fly with a period of 3 s (120°/s), with the center changing randomly (indicated by the red bar). LFP power for either frequency 3 s after the change were contrasted, as a ratio, with 3 s before the event (dashed boxes). Blue trace: LFP; green line: image position. (G) 7 and 9 Hz ratios for novelty events during non-flight epochs, for either tag configuration (C, center; S, surround). n = 12 flies, **P < 0.01, by t-test compared to 1.0 (dashed line = no effect). (H) The same data as in G was reanalyzed after binning into five separate categories depending on how much time had passed since the last change. A ratio was calculated for either tag, contrasting the 3 s after vs. 3 s before (dashed boxes). (I) 7 Hz (blue) and 9 Hz (red) ratios for visual changes during non-flight experiments, binned into 5 temporal groups. Shown are results for 7 Hz center vs. 9 Hz surround. n = 12 flies, **P < 0.01, by t-test compared to 1.0 (dashed line).
Mentions: In previous work we have shown that visual salience, such as novelty, increases endogenous 20–30 Hz LFP activity in the Drosophila brain (van Swinderen and Greenspan, 2003; van Swinderen, 2007b; van Swinderen et al., 2009; van Swinderen and Brembs, 2010). To investigate whether such salience effects might change the responsiveness of flies to specific flicker frequencies, the preceding center-surround scenario was modified to include a changing central object, while the surround was left unchanged (Figure 3A). The central object alternated between a “+” and an “×” with random timing set between 5 s and 50 s. Power for either tag (7 or 9 Hz) after a change was compared to power before the change, expressed as a ratio, for either frequency (Figures 3B–G, see “Materials and Methods”). Changing the central object shape (but not the frequency tag) while the fly was actively fixating on the compound stimulus (Figure 3B, red bar) resulted in significantly increased 7 Hz power; effects on 9 Hz were less clear, although the tendency was for increased power following the change, regardless of the frequency tag (Figure 3C). Any significant effects were lost when novelty occurred (for the same animals) during flight without fixation (Figures 3D,E), although the trend to increased responsiveness was similar as for fixation, and these results were not significantly different from the novelty results under active fixation. In a separate set of open-loop experiments in non-flying animals (Figure 3F), changes to the central object shape also increased the power of the competing surrounding tag as well as the central tag, for either frequency combination (Figure 3G). This last, most significant set of results demonstrates that responsiveness to visual flicker can be modulated in the absence of flight behavior, and further, that a visual salience event (a novel object at the center) evokes increased responsiveness to a wider area than just the 30° central object that is changing. Together, the results so far suggest that novelty effects on the frequency tag may be independent of behavioral state of the animal. In addition, responsiveness to the competing tags 3 s after a change appears to be broad rather than selective. Since the novelty effect on tag power was also present in non-flying animals, subsequent analyses will focus on this more extensive dataset, specifically, looking at 7 Hz center competing with a 9 Hz surround (this combination produced a similar-sized novelty effect for both frequency tags, Figure 3G, left histograms).

Bottom Line: There is increasing evidence that invertebrates such as flies display selective attention (van Swinderen, 2011a), although parallel processing of simultaneous cues remains difficult to demonstrate in such tiny brains.Local field potential (LFP) activity in the fly brain is associated with stimulus selection and suppression (van Swinderen and Greenspan, 2003; Tang and Juusola, 2010), like in other animals such as monkeys (Fries et al., 2001), suggesting that similar processes may be working to control attention in vastly different brains.Visual competition dynamics in the fly brain were dependent on the rate of pattern presentation, suggesting that attention-like switching in insects is tuned to the pace of visual changes in the environment rather than simply the passage of time.

View Article: PubMed Central - PubMed

Affiliation: Queensland Brain Institute, The University of Queensland Brisbane, QLD, Australia.

ABSTRACT
There is increasing evidence that invertebrates such as flies display selective attention (van Swinderen, 2011a), although parallel processing of simultaneous cues remains difficult to demonstrate in such tiny brains. Local field potential (LFP) activity in the fly brain is associated with stimulus selection and suppression (van Swinderen and Greenspan, 2003; Tang and Juusola, 2010), like in other animals such as monkeys (Fries et al., 2001), suggesting that similar processes may be working to control attention in vastly different brains. To investigate selective attention to competing visual cues, I recorded brain activity from behaving flies while applying a method used in human attention studies: competing visual flicker, or frequency tags (Vialatte et al., 2010). Behavioral fixation in a closed-loop flight arena increased the response to visual flicker in the fly brain, and visual salience modulated responses to competing tags arranged in a center-surround pattern. Visual competition dynamics in the fly brain were dependent on the rate of pattern presentation, suggesting that attention-like switching in insects is tuned to the pace of visual changes in the environment rather than simply the passage of time.

No MeSH data available.


Related in: MedlinePlus