Multichannel brain recordings in behaving<i>Drosophila</i>reveal oscillatory activity and local coherence in response to sensory stimulation and circuit activation

Paulk, Angelique C.; Zhou, Yuxing; Stratton, Peter; Liu, Li; Swinderen, Bruno van

doi:10.1152/jn.00414.2013

Cited by 36 publications

(60 citation statements)

References 68 publications

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“…2E), and the responses varied with brain region, as expected (26)(27)(28)(29). In general, flicker responses were of greater amplitude in the optic lobes than in the central brain (e.g., mushroom body) (Fig.…”

Section: Significancesupporting

confidence: 63%

Selective attention in the honeybee optic lobes precedes behavioral choices

Paulk

Stacey

Pearson

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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109

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Attention allows animals to respond selectively to competing stimuli, enabling some stimuli to evoke a behavioral response while others are ignored. How the brain does this remains mysterious, although it is increasingly evident that even animals with the smallest brains display this capacity. For example, insects respond selectively to salient visual stimuli, but it is unknown where such selectivity occurs in the insect brain, or whether neural correlates of attention might predict the visual choices made by an insect. Here, we investigate neural correlates of visual attention in behaving honeybees (Apis mellifera). Using a closed-loop paradigm that allows tethered, walking bees to actively control visual objects in a virtual reality arena, we show that behavioral fixation increases neuronal responses to flickering, frequency-tagged stimuli. Attention-like effects were reduced in the optic lobes during replay of the same visual sequences, when bees were not able to control the visual displays. When bees were presented with competing frequency-tagged visual stimuli, selectivity in the medulla (an optic ganglion) preceded behavioral selection of a stimulus, suggesting that modulation of early visual processing centers precedes eventual behavioral choices made by these insects.invertebrate | vision | electrophysiology | local field potential A ttention allows animals to respond selectively to competing stimuli (1, 2). Stimulus-selective responses in the human brain can be endogenously driven, and this volitional form of attention has been referred to as a "top-down" process, to distinguish it from salience-driven or "bottom-up" attention (3). Although even insects display bottom-up attention (4-10), it is unclear whether attention-like selection in the insect brain might also precede or predict behavioral choices. The case for top-down attention is especially compelling for honeybees, which have welldemonstrated visual discrimination and cognitive capabilities (11)(12)(13)(14). To effectively relate attention processes to behavior, however, requires sophisticated behavioral tracking or recording brain activity from behaving insects selecting distinct objects (15). Previous psychophysical studies in insects have measured whole body movements using tethered, closed-loop flight paradigms (4-8, 15). However, most studies of visual perception and memory in the bee have involved free flight (11, 13, 14; but see ref. 16). To address the neural mechanisms subserving these behaviors, researchers have traditionally recorded brain activity from immobilized bees performing elemental associative learning (e.g., refs. 17 and 18). Animal immobilization, however, is not ideal for gaining a better understanding of the relationship between the complex cognitive behaviors seen in freely moving bees and the underlying neural activity (13,14). To this end, we developed a closed-loop paradigm for walking honey bees (19), allowing them to select and fixate visual cues by rotating an air-supported ball. To simultaneously examine attentio...

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Section: Significancesupporting

confidence: 63%

Selective attention in the honeybee optic lobes precedes behavioral choices

Paulk

Stacey

Pearson

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

109

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“…C , Example of pre-processed LFPs data before anesthesia (0% isoflurane) from one fly. A standardized fly brain is shown for comparison (Paulk et al, 2013b, 2015). The electrode contacts are indicated by white dots (not to scale).…”

Section: Methodsmentioning

confidence: 99%

“…Previous work has shown that the fly heartbeat can manifest as low-frequency (2–4 Hz) oscillatory activity in central channels (Paulk et al, 2013b; Yap et al, 2017). Heartbeats are unlikely to affect the results presented here because we use bipolar rereferencing which eliminates common input to neighboring channels, as may be expected from a muscle artifact (Cohen and Tsuchiya, 2017).…”

Section: Methodsmentioning

confidence: 99%

Isoflurane Impairs Low-Frequency Feedback but Leaves High-Frequency Feedforward Connectivity Intact in the Fly Brain

Cohen

Swinderen

Tsuchiya

2018

eNeuro

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Hierarchically organized brains communicate through feedforward (FF) and feedback (FB) pathways. In mammals, FF and FB are mediated by higher and lower frequencies during wakefulness. FB is preferentially impaired by general anesthetics in multiple mammalian species. This suggests FB serves critical functions in waking brains. The brain of Drosophila melanogaster (fruit fly) is also hierarchically organized, but the presence of FB in these brains is not established. Here, we studied FB in the fly brain, by simultaneously recording local field potentials (LFPs) from low-order peripheral structures and higher-order central structures. We analyzed the data using Granger causality (GC), the first application of this analysis technique to recordings from the insect brain. Our analysis revealed that low frequencies (0.1–5 Hz) mediated FB from the center to the periphery, while higher frequencies (10–45 Hz) mediated FF in the opposite direction. Further, isoflurane anesthesia preferentially reduced FB. Our results imply that the spectral characteristics of FF and FB may be a signature of hierarchically organized brains that is conserved from insects to mammals. We speculate that general anesthetics may induce unresponsiveness across species by targeting the mechanisms that support FB.

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“…Tethered flies were positioned above a 45.5 mg air-supported Styrofoam ball (Fig. 1 a , b ), similar to that described by Paulk et al (2013).…”

Section: Methodsmentioning

confidence: 99%

“…We used a recently developed multielectrode preparation (Paulk et al, 2013) to record evoked local field potentials (LFPs) across the fly brain in response to flickering visual stimuli. The flickering stimuli produced a periodic response, known as steady-state visually evoked potentials (SSVEPs; Norcia et al, 2015), that allowed us to accurately track the responses in the frequency domain across brain structures, from the optic lobes to the central brain.…”

Section: Introductionmentioning

confidence: 99%

Local Versus Global Effects of Isoflurane Anesthesia on Visual Processing in the Fly Brain

Cohen

Zalucki

Swinderen

et al. 2016

eneuro

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What characteristics of neural activity distinguish the awake and anesthetized brain? Drugs such as isoflurane abolish behavioral responsiveness in all animals, implying evolutionarily conserved mechanisms. However, it is unclear whether this conservation is reflected at the level of neural activity. Studies in humans have shown that anesthesia is characterized by spatially distinct spectral and coherence signatures that have also been implicated in the global impairment of cortical communication. We questioned whether anesthesia has similar effects on global and local neural processing in one of the smallest brains, that of the fruit fly (Drosophila melanogaster). Using a recently developed multielectrode technique, we recorded local field potentials from different areas of the fly brain simultaneously, while manipulating the concentration of isoflurane. Flickering visual stimuli (‘frequency tags’) allowed us to track evoked responses in the frequency domain and measure the effects of isoflurane throughout the brain. We found that isoflurane reduced power and coherence at the tagging frequency (13 or 17 Hz) in central brain regions. Unexpectedly, isoflurane increased power and coherence at twice the tag frequency (26 or 34 Hz) in the optic lobes of the fly, but only for specific stimulus configurations. By modeling the periodic responses, we show that the increase in power in peripheral areas can be attributed to local neuroanatomy. We further show that the effects on coherence can be explained by impacted signal-to-noise ratios. Together, our results show that general anesthesia has distinct local and global effects on neuronal processing in the fruit fly brain.

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Multichannel brain recordings in behavingDrosophilareveal oscillatory activity and local coherence in response to sensory stimulation and circuit activation

Cited by 36 publications

References 68 publications

Selective attention in the honeybee optic lobes precedes behavioral choices

Selective attention in the honeybee optic lobes precedes behavioral choices

Isoflurane Impairs Low-Frequency Feedback but Leaves High-Frequency Feedforward Connectivity Intact in the Fly Brain

Local Versus Global Effects of Isoflurane Anesthesia on Visual Processing in the Fly Brain

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