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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

Behavioral fixation of frequency-tagged visual stimuli. (A) Experimental setup. Two glass electrodes (blue) are implanted into the brain of a fly tethered to a metal post (yellow). An infrared system (red) allows the fly to control the angular position of virtual objects (a green cross). (B) Three signals are recorded from each experiment: the wing-beat frequency (black, scale is 0–200 Hz), the local field potential (LFP, blue, scale is—2 to 6 μvolts), and the angular position of the image (green, scale is 0–360°). Behavioral fixation is observed when the fly stabilizes the angular position of the image (red shading). (C) Three behavioral states were identified (see “Materials and Methods”): Fixation (red), flight without fixation (yellow), and not flying (blue). Upper trace (black): wing-beat frequency, indicative of flight at 200 Hz. Lower trace (green): image position for the same recording. Unwrapped image position is shown below (to eliminate edges), and variance for the unwrapped data, below that. (D) Flies can fixate on a 30°-wide cross, composed of 20 LED pixels flickering together at 7 Hz. Image fixation is indicated by increased duration (relative time) in one part of the visual field, usually close to front (dotted line). Data are averaged from 6 wild-type male flies. (E) Fixation behavior was determined empirically per fly from the position variance statistics (see “Materials and Methods”). (F) LFP responses to a 7 or 9 Hz flickering cross. Middle panel: LFP (blue trace) recorded during fixation of a 9 Hz flickering cross. Green line: angular position of image (same axes as in C, second panel down); black trace: wing-beat frequency indicating flight. Fixation time is indicated by the red rectangle. Right panel: sample spectral analysis (see “Materials and Methods”) for a 7 Hz (blue) or a 9 Hz (red) cross during behavioral fixation. (G) Normalized 7 or 9 Hz power (log score ± SEM) for the three behavioral states (NF, blue, not flying; Fly, yellow, flight without fixation; Fix, red, flight with fixation, n = 6 male wild-type flies; *P < 0.05, ***P < 0.001 by t-test). All responses were significantly greater than zero (= the 8 Hz denominator, indicating the presence of a frequency tag, P < 0.001).
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Figure 1: Behavioral fixation of frequency-tagged visual stimuli. (A) Experimental setup. Two glass electrodes (blue) are implanted into the brain of a fly tethered to a metal post (yellow). An infrared system (red) allows the fly to control the angular position of virtual objects (a green cross). (B) Three signals are recorded from each experiment: the wing-beat frequency (black, scale is 0–200 Hz), the local field potential (LFP, blue, scale is—2 to 6 μvolts), and the angular position of the image (green, scale is 0–360°). Behavioral fixation is observed when the fly stabilizes the angular position of the image (red shading). (C) Three behavioral states were identified (see “Materials and Methods”): Fixation (red), flight without fixation (yellow), and not flying (blue). Upper trace (black): wing-beat frequency, indicative of flight at 200 Hz. Lower trace (green): image position for the same recording. Unwrapped image position is shown below (to eliminate edges), and variance for the unwrapped data, below that. (D) Flies can fixate on a 30°-wide cross, composed of 20 LED pixels flickering together at 7 Hz. Image fixation is indicated by increased duration (relative time) in one part of the visual field, usually close to front (dotted line). Data are averaged from 6 wild-type male flies. (E) Fixation behavior was determined empirically per fly from the position variance statistics (see “Materials and Methods”). (F) LFP responses to a 7 or 9 Hz flickering cross. Middle panel: LFP (blue trace) recorded during fixation of a 9 Hz flickering cross. Green line: angular position of image (same axes as in C, second panel down); black trace: wing-beat frequency indicating flight. Fixation time is indicated by the red rectangle. Right panel: sample spectral analysis (see “Materials and Methods”) for a 7 Hz (blue) or a 9 Hz (red) cross during behavioral fixation. (G) Normalized 7 or 9 Hz power (log score ± SEM) for the three behavioral states (NF, blue, not flying; Fly, yellow, flight without fixation; Fix, red, flight with fixation, n = 6 male wild-type flies; *P < 0.05, ***P < 0.001 by t-test). All responses were significantly greater than zero (= the 8 Hz denominator, indicating the presence of a frequency tag, P < 0.001).

Mentions: The tethered fly, implanted with two electrodes, was able to control the angular position of virtual objects displayed on an LED arena by modulating its flight behavior, as described previously (Lehmann and Dickinson, 1997; van Swinderen and Greenspan, 2003). Briefly, an infrared light above the fly creates a shadow of either wing (in flight) on two photodetectors positioned below the fly (see Figure 1A). Wing beats are detected as a standing wave, and a differential of the wing beat amplitudes represents the fly's attempt at steering. Feedback from the wing beat differential to the LED arena controls the angular position of a visual panorama on the arena, such that flies are able to fixate on virtual objects, and this tendency to fixate is recorded as a position signal (from 1 to 72, sampled at 300 Hz) through time.


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

van Swinderen B - Front Integr Neurosci (2012)

Behavioral fixation of frequency-tagged visual stimuli. (A) Experimental setup. Two glass electrodes (blue) are implanted into the brain of a fly tethered to a metal post (yellow). An infrared system (red) allows the fly to control the angular position of virtual objects (a green cross). (B) Three signals are recorded from each experiment: the wing-beat frequency (black, scale is 0–200 Hz), the local field potential (LFP, blue, scale is—2 to 6 μvolts), and the angular position of the image (green, scale is 0–360°). Behavioral fixation is observed when the fly stabilizes the angular position of the image (red shading). (C) Three behavioral states were identified (see “Materials and Methods”): Fixation (red), flight without fixation (yellow), and not flying (blue). Upper trace (black): wing-beat frequency, indicative of flight at 200 Hz. Lower trace (green): image position for the same recording. Unwrapped image position is shown below (to eliminate edges), and variance for the unwrapped data, below that. (D) Flies can fixate on a 30°-wide cross, composed of 20 LED pixels flickering together at 7 Hz. Image fixation is indicated by increased duration (relative time) in one part of the visual field, usually close to front (dotted line). Data are averaged from 6 wild-type male flies. (E) Fixation behavior was determined empirically per fly from the position variance statistics (see “Materials and Methods”). (F) LFP responses to a 7 or 9 Hz flickering cross. Middle panel: LFP (blue trace) recorded during fixation of a 9 Hz flickering cross. Green line: angular position of image (same axes as in C, second panel down); black trace: wing-beat frequency indicating flight. Fixation time is indicated by the red rectangle. Right panel: sample spectral analysis (see “Materials and Methods”) for a 7 Hz (blue) or a 9 Hz (red) cross during behavioral fixation. (G) Normalized 7 or 9 Hz power (log score ± SEM) for the three behavioral states (NF, blue, not flying; Fly, yellow, flight without fixation; Fix, red, flight with fixation, n = 6 male wild-type flies; *P < 0.05, ***P < 0.001 by t-test). All responses were significantly greater than zero (= the 8 Hz denominator, indicating the presence of a frequency tag, P < 0.001).
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Related In: Results  -  Collection

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Figure 1: Behavioral fixation of frequency-tagged visual stimuli. (A) Experimental setup. Two glass electrodes (blue) are implanted into the brain of a fly tethered to a metal post (yellow). An infrared system (red) allows the fly to control the angular position of virtual objects (a green cross). (B) Three signals are recorded from each experiment: the wing-beat frequency (black, scale is 0–200 Hz), the local field potential (LFP, blue, scale is—2 to 6 μvolts), and the angular position of the image (green, scale is 0–360°). Behavioral fixation is observed when the fly stabilizes the angular position of the image (red shading). (C) Three behavioral states were identified (see “Materials and Methods”): Fixation (red), flight without fixation (yellow), and not flying (blue). Upper trace (black): wing-beat frequency, indicative of flight at 200 Hz. Lower trace (green): image position for the same recording. Unwrapped image position is shown below (to eliminate edges), and variance for the unwrapped data, below that. (D) Flies can fixate on a 30°-wide cross, composed of 20 LED pixels flickering together at 7 Hz. Image fixation is indicated by increased duration (relative time) in one part of the visual field, usually close to front (dotted line). Data are averaged from 6 wild-type male flies. (E) Fixation behavior was determined empirically per fly from the position variance statistics (see “Materials and Methods”). (F) LFP responses to a 7 or 9 Hz flickering cross. Middle panel: LFP (blue trace) recorded during fixation of a 9 Hz flickering cross. Green line: angular position of image (same axes as in C, second panel down); black trace: wing-beat frequency indicating flight. Fixation time is indicated by the red rectangle. Right panel: sample spectral analysis (see “Materials and Methods”) for a 7 Hz (blue) or a 9 Hz (red) cross during behavioral fixation. (G) Normalized 7 or 9 Hz power (log score ± SEM) for the three behavioral states (NF, blue, not flying; Fly, yellow, flight without fixation; Fix, red, flight with fixation, n = 6 male wild-type flies; *P < 0.05, ***P < 0.001 by t-test). All responses were significantly greater than zero (= the 8 Hz denominator, indicating the presence of a frequency tag, P < 0.001).
Mentions: The tethered fly, implanted with two electrodes, was able to control the angular position of virtual objects displayed on an LED arena by modulating its flight behavior, as described previously (Lehmann and Dickinson, 1997; van Swinderen and Greenspan, 2003). Briefly, an infrared light above the fly creates a shadow of either wing (in flight) on two photodetectors positioned below the fly (see Figure 1A). Wing beats are detected as a standing wave, and a differential of the wing beat amplitudes represents the fly's attempt at steering. Feedback from the wing beat differential to the LED arena controls the angular position of a visual panorama on the arena, such that flies are able to fixate on virtual objects, and this tendency to fixate is recorded as a position signal (from 1 to 72, sampled at 300 Hz) through time.

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