Oscillations in the central brain of Drosophila are phase locked to attended visual features

Abstract

Object-based attention describes the brain’s capacity to prioritize one set of stimuli while ignoring others. Human research suggests that the binding of diverse stimuli into one attended percept requires phase-locked oscillatory activity in the brain. Even insects display oscillatory brain activity during visual attention tasks, but it is unclear if neural oscillations in insects are selectively correlated to different features of attended objects. We addressed this question by recording local field potentials in theDrosophilacentral complex, a brain structure involved in visual navigation and decision making. We found that attention selectively increased the neural gain of visual features associated with attended objects and that attention could be redirected to unattended objects by activation of a reward circuit. Attention was associated with increased beta (20- to 30-Hz) oscillations that selectively locked onto temporal features of the attended visual objects. Our results suggest a conserved function for the beta frequency range in regulating selective attention to salient visual features.

Integrated information structure collapses with anesthetic loss of conscious arousal in Drosophila melanogaster

“…In this context, there is accumulating evidence to suggest that flies indeed have varying levels of consciousness [ 20 , 21 , 10 ]. There is even some evidence to suggest similar psychological processes in flies as in humans, such as attention [ 16 , 21 , 67 ], memory [ 13 – 15 ] and feature binding [ 19 ]. Further similarities have been found for other insects, such as perception of illusory contours, metacognition, false memory, and long-term planning in bees [ 68 – 71 ].…”

“…As stated, complex behavioural repertoires of animals, ranging from humans to insects, all seem to reduce in a similar manner from highly active wakefulness to loss of consciousness. During wakefulness, flies, for instance, have been shown to exhibit processes such as working memory [ 13 – 15 ], attention [ 16 – 18 ], and feature binding [ 19 ]. Flies also seem to experience varying states of arousal which are physiologically regulated in a similar manner to mammals, such as sleep [ 9 , 20 , 21 ] and anesthesia [ 11 , 12 ].…”

Balancing Prediction and Surprise: A Role for Active Sleep at the Dawn of Consciousness?

“…This suggests a conserved mechanism in the fly brain attuned to first detecting surprising stimuli (i.e., novelty), and then to paying attention to them for a period of time (Sareen et al, 2011;van Swinderen, 2011). Interestingly, when an arousal system in the fly (neuropeptide F) is transiently activated, this increases 20-30 Hz phase locking in the fly brain and redirects the insect's attention to novel objects irrespective of their innate valence (Grabowska et al, 2020). Such findings again suggest an evolutionarily conserved link between arousal systems and novelty detection mechanisms.…”

“…Earlier electrophysiological recordings from behaving flies showed that visual novelty is associated with transient oscillations in their central brain, in the range of 20-30 Hz (van Swinderen and Greenspan, 2003;van Swinderen, 2007). A more recent study recording directly from the central complex of behaving flies revealed a selective phase-locking mechanism between the endogenous 20-30 Hz oscillations and the attended object (Grabowska et al, 2020). This suggests a conserved mechanism in the fly brain attuned to first detecting surprising stimuli (i.e., novelty), and then to paying attention to them for a period of time (Sareen et al, 2011;van Swinderen, 2011).…”

Gamma rhythms in the visual cortex: functions and mechanisms

“…. Rodents (Cardin et al 2005(Cardin et al , 2009Saleem et al 2017;Storchi et al 2017;Welle and Contreras 2017) and insects (Kirschfeld 1992;Grabowska et al 2020) also became animal models for understanding the neural mechanisms of gamma-band activity.…”