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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

The frequency tag. (A) Recording sites in the Drosophila brain (arrows). Texas Red dye was released from glass recording electrodes by iontophoresis, and the two recording sites determined by the region with greatest staining intensity, in the inner optic lobe. A differential recording was made between these sites. Inset scale bar = 100 μm. (B) A moving object (a cross moving 120°/s) flickering at different frequencies evokes distinct frequency responses in the recorded brain LFP, shown here for four different frequency tags. (C) A moving flickering object (a cross moving 120°/s) evokes a greater frequency response in the brain LFP than a static flickering object (positioned 45° to the left of the front of the fly) for either 7 or 9 Hz. (D) The LFP tag (blue trace) is time-locked to a cross flickering at 7 Hz (black trace). The response for a full rotation of the stimulus is shown. (E) The LFP tag (black trace) is time-locked to a field of dots flickering at 9 Hz (black trace). The response for a full rotation of the stimulus is shown. (F) Differential recordings to the thorax reveal the contribution from either optic lobe. (G) Coherence analysis (see “Materials and Methods”) between each differential recording (from F) and the physical stimulus (as in D and E, recorded with a photodiode) reveals a distinct profile for the combined brain recording (blue), vs. each single optic lobe references to the thorax (red and green). Coherence to the signal is weaker for the within-brain differential, indicating a different quality response than for each individual optic lobe. Data in the paper are all voltage differentials within the brain (blue).
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FA1: The frequency tag. (A) Recording sites in the Drosophila brain (arrows). Texas Red dye was released from glass recording electrodes by iontophoresis, and the two recording sites determined by the region with greatest staining intensity, in the inner optic lobe. A differential recording was made between these sites. Inset scale bar = 100 μm. (B) A moving object (a cross moving 120°/s) flickering at different frequencies evokes distinct frequency responses in the recorded brain LFP, shown here for four different frequency tags. (C) A moving flickering object (a cross moving 120°/s) evokes a greater frequency response in the brain LFP than a static flickering object (positioned 45° to the left of the front of the fly) for either 7 or 9 Hz. (D) The LFP tag (blue trace) is time-locked to a cross flickering at 7 Hz (black trace). The response for a full rotation of the stimulus is shown. (E) The LFP tag (black trace) is time-locked to a field of dots flickering at 9 Hz (black trace). The response for a full rotation of the stimulus is shown. (F) Differential recordings to the thorax reveal the contribution from either optic lobe. (G) Coherence analysis (see “Materials and Methods”) between each differential recording (from F) and the physical stimulus (as in D and E, recorded with a photodiode) reveals a distinct profile for the combined brain recording (blue), vs. each single optic lobe references to the thorax (red and green). Coherence to the signal is weaker for the within-brain differential, indicating a different quality response than for each individual optic lobe. Data in the paper are all voltage differentials within the brain (blue).

Mentions: Flies were anaesthetized on a 2°C cold block controlled by a Peltier element. Flies were secured to a tungsten wire, as described previously (van Swinderen, 2011b). The tungsten wire ended in a small hook. A small drop of dental cement (SynergyFlow A3.5/B3, Coltene Whaledent) was applied to the tungsten hook, and contact was made (using a micromanipulator) with the front/top of the thorax and the top of the head. The dental cement was cured with blue light, using a dental gun (SDI radii plus, Henry Schein Dental). Flies were then removed from the cold block and allowed to recover before electrodes were implanted. Glass electrodes (1.0 mm borosilicate with filament, World Precision Instruments) were made, implanted, and secured as described previously (van Swinderen and Greenspan, 2003; van Swinderen, 2011b) with a few modifications: the positioning of the tungsten hook along the center (front to back) of the flies' head allowed for an electrode to be implanted on either side at the dorsal rim of the eye. Electrodes were lowered (using a Narishige MM1000 micromanipulator holding a pair of forceps (van Swinderen, 2011b) ~100 μm into the fly head at a 45° angle from vertical, to ensure that the electrode tip ended up in the inner optic lobes on either side. Electrodes were secured in place with dental cement such that they were free standing. Position of the recording site was verified by releasing Texas Red dye by iontophoresis, fixing the head in 2% paraformaldehyde following an experiment, and visualizing under fluorescence microscopy (See Figure A1). Electrode positioning was accurate enough to ensure a reliable LFP in response to visual flicker (see below).


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

van Swinderen B - Front Integr Neurosci (2012)

The frequency tag. (A) Recording sites in the Drosophila brain (arrows). Texas Red dye was released from glass recording electrodes by iontophoresis, and the two recording sites determined by the region with greatest staining intensity, in the inner optic lobe. A differential recording was made between these sites. Inset scale bar = 100 μm. (B) A moving object (a cross moving 120°/s) flickering at different frequencies evokes distinct frequency responses in the recorded brain LFP, shown here for four different frequency tags. (C) A moving flickering object (a cross moving 120°/s) evokes a greater frequency response in the brain LFP than a static flickering object (positioned 45° to the left of the front of the fly) for either 7 or 9 Hz. (D) The LFP tag (blue trace) is time-locked to a cross flickering at 7 Hz (black trace). The response for a full rotation of the stimulus is shown. (E) The LFP tag (black trace) is time-locked to a field of dots flickering at 9 Hz (black trace). The response for a full rotation of the stimulus is shown. (F) Differential recordings to the thorax reveal the contribution from either optic lobe. (G) Coherence analysis (see “Materials and Methods”) between each differential recording (from F) and the physical stimulus (as in D and E, recorded with a photodiode) reveals a distinct profile for the combined brain recording (blue), vs. each single optic lobe references to the thorax (red and green). Coherence to the signal is weaker for the within-brain differential, indicating a different quality response than for each individual optic lobe. Data in the paper are all voltage differentials within the brain (blue).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3475995&req=5

FA1: The frequency tag. (A) Recording sites in the Drosophila brain (arrows). Texas Red dye was released from glass recording electrodes by iontophoresis, and the two recording sites determined by the region with greatest staining intensity, in the inner optic lobe. A differential recording was made between these sites. Inset scale bar = 100 μm. (B) A moving object (a cross moving 120°/s) flickering at different frequencies evokes distinct frequency responses in the recorded brain LFP, shown here for four different frequency tags. (C) A moving flickering object (a cross moving 120°/s) evokes a greater frequency response in the brain LFP than a static flickering object (positioned 45° to the left of the front of the fly) for either 7 or 9 Hz. (D) The LFP tag (blue trace) is time-locked to a cross flickering at 7 Hz (black trace). The response for a full rotation of the stimulus is shown. (E) The LFP tag (black trace) is time-locked to a field of dots flickering at 9 Hz (black trace). The response for a full rotation of the stimulus is shown. (F) Differential recordings to the thorax reveal the contribution from either optic lobe. (G) Coherence analysis (see “Materials and Methods”) between each differential recording (from F) and the physical stimulus (as in D and E, recorded with a photodiode) reveals a distinct profile for the combined brain recording (blue), vs. each single optic lobe references to the thorax (red and green). Coherence to the signal is weaker for the within-brain differential, indicating a different quality response than for each individual optic lobe. Data in the paper are all voltage differentials within the brain (blue).
Mentions: Flies were anaesthetized on a 2°C cold block controlled by a Peltier element. Flies were secured to a tungsten wire, as described previously (van Swinderen, 2011b). The tungsten wire ended in a small hook. A small drop of dental cement (SynergyFlow A3.5/B3, Coltene Whaledent) was applied to the tungsten hook, and contact was made (using a micromanipulator) with the front/top of the thorax and the top of the head. The dental cement was cured with blue light, using a dental gun (SDI radii plus, Henry Schein Dental). Flies were then removed from the cold block and allowed to recover before electrodes were implanted. Glass electrodes (1.0 mm borosilicate with filament, World Precision Instruments) were made, implanted, and secured as described previously (van Swinderen and Greenspan, 2003; van Swinderen, 2011b) with a few modifications: the positioning of the tungsten hook along the center (front to back) of the flies' head allowed for an electrode to be implanted on either side at the dorsal rim of the eye. Electrodes were lowered (using a Narishige MM1000 micromanipulator holding a pair of forceps (van Swinderen, 2011b) ~100 μm into the fly head at a 45° angle from vertical, to ensure that the electrode tip ended up in the inner optic lobes on either side. Electrodes were secured in place with dental cement such that they were free standing. Position of the recording site was verified by releasing Texas Red dye by iontophoresis, fixing the head in 2% paraformaldehyde following an experiment, and visualizing under fluorescence microscopy (See Figure A1). Electrode positioning was accurate enough to ensure a reliable LFP in response to visual flicker (see below).

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