Selective attention in the honeybee optic lobes precedes behavioral choices

Abstract

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...

What insects can tell us about the origins of consciousness

“…neural responses to stimuli that are points of visual fixation (103). These exciting new electrophysiological studies demonstrate more compellingly than behavioral studies alone the subjective and egocentric nature of the neural representation of the environment in insects, and their capacity for selective attention supports our assertion that insects have a capacity for subjective experience.…”

“…There is now both behavioral and electrophysiological evidence that the neural modeling of the environment performed by insects involves multiple layers of filtering of sensory information to support selective attention to stimuli that are salient and suppression of representation of irrelevant stimuli (101)(102)(103)(104). The amount and amplitude of firing activity within certain defined frequency bands in the central brain of tethered flies in response to visual stimuli is dependent on whether the fly is visually fixed on the stimulus or whether the context of the stimulus has changed (101).…”

The forest or the trees: preference for global over local image processing is reversed by prior experience in honeybees

“…Our results suggest that visual processing in bees can be related to attentional-like processes, which, depending on the training procedure, may enhance the relevance of specific features while filtering other cues. Attentional-like mechanisms have been shown to mediate visual performances in insects [79][80][81][82][83]. In fruitflies, Drosophila melanogaster, attention in a visual tracking task [79,[84][85][86]] could be retraced to the level of the mushroom bodies, which are higher-order structures of the insect brain.…”

“…In fruitflies, Drosophila melanogaster, attention in a visual tracking task [79,[84][85][86]] could be retraced to the level of the mushroom bodies, which are higher-order structures of the insect brain. In honeybees walking stationarily in the middle of a visual arena, neural signatures underlying attentional tracking of moving bars were found in different visual neuropiles of the brain [83]. Yet the neural mechanisms underlying both the precedence of global configurations and the capacity to revert this precedence to local analysis in visual image processing remain to be determined.…”

The answer is blowing in the wind: free flying honeybees can integrate visual and mechano-sensory inputs for making complex foraging decisions

“…In natural environments there is an enormous amount of sensory information that needs to be either processed or ignored in order for an animal to make accurate decisions (Paulk et al, 2014;Posner et al, 1980;Sareen et al, 2011). Honeybees have emerged as an important biological model for understanding signal-receiver relationships because their goal(s) can be well mapped (Dyer and Arikawa, 2014;Morawetz and Spaethe, 2012;Von Frisch, 1967).…”