Novel Flicker-Sensitive Visual Circuit Neurons Inhibited by Stationary Patterns

Haan, Roel de; Lee, Yu–Jen; Nordström, Karin

doi:10.1523/jneurosci.5713-12.2013

Cited by 10 publications

(22 citation statements)

References 61 publications

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“…A role for the medulla or lobula in insect visual selective attention is compelling, particularly in light of a number of recent studies on neurons connecting contralateral optic lobes with the central brain in insects (42)(43)(44) have shown that centrifugal feedback neurons also display attention-like properties at a single-cell level (44). Similar long-ranging neurons may be key for inducing the coherent population activity we observe in the medulla and lobula.…”

Section: Discussionmentioning

confidence: 77%

Selective attention in the honeybee optic lobes precedes behavioral choices

Paulk

Stacey

Pearson

et al. 2014

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

111

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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: Discussionmentioning

confidence: 77%

Selective attention in the honeybee optic lobes precedes behavioral choices

Paulk

Stacey

Pearson

et al. 2014

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

111

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“…cSIFE is also inhibited by stationary gratings, regardless of their orientation ( Fig. 1b , N =16) 26 .…”

Section: Resultsmentioning

confidence: 83%

“…As opposed to the more well-studied classic lobula plate tangential cells (LPTCs) that are clearly direction-selective 27 , cSIFE responds strongly to moving sinusoidal gratings, regardless of the direction of motion ( Fig. 1a , N =16) 26 . cSIFE is also inhibited by stationary gratings, regardless of their orientation ( Fig.…”

Section: Resultsmentioning

confidence: 84%

“…Furthermore, cSIFE's inhibition is not only limited by the spatial resolution of the eye, but is confined to a specific bandwidth of spatial frequencies between 0.06 and 1 c.p.d. 26 . Therefore, to get a more realistic account of the amplitude slope constants that are relevant for cSIFE's inhibition we calculate the slope constants of the amplitude spectra of 109 natural images using linear curve fitting between 0.06 and 1 c.p.d.…”

Section: Resultsmentioning

confidence: 99%

“…Here, we quantify how the response of an insect higher order visual neuron depends on the strictly spatial characteristics of natural scenes. For this, we utilize a recently described neuron that is excited by flicker, and thus responds non-directionally to motion, and more valid for our purposes here, is inhibited by stationary images 26 . The inhibition of centrifugal Stationary Inhibited Flicker Excited, cSIFE, by stationary images provides a unique opportunity for investigating visual responses to natural scenes that vary only in the spatial domain, while remaining constant in the temporal domain.…”

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confidence: 99%

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A higher order visual neuron tuned to the spatial amplitude spectra of natural scenes

et al. 2015

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Animal sensory systems are optimally adapted to those features typically encountered in natural surrounds, thus allowing neurons with limited bandwidth to encode challengingly large input ranges. Natural scenes are not random, and peripheral visual systems in vertebrates and insects have evolved to respond efficiently to their typical spatial statistics. The mammalian visual cortex is also tuned to natural spatial statistics, but less is known about coding in higher order neurons in insects. To redress this we here record intracellularly from a higher order visual neuron in the hoverfly. We show that the cSIFE neuron, which is inhibited by stationary images, is maximally inhibited when the slope constant of the amplitude spectrum is close to the mean in natural scenes. The behavioural optomotor response is also strongest to images with naturalistic image statistics. Our results thus reveal a close coupling between the inherent statistics of natural scenes and higher order visual processing in insects.

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Hoverfly locomotor activity is resilient to external influence and intrinsic factors

Thyselius

Nordström

2015

J Comp Physiol A

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Hoverflies are found across the globe, with approximately 6000 species described worldwide. Many hoverflies are being used in agriculture and some are emerging as model species for laboratory experiments. As such it is valuable to know more about their activity. Like many other dipteran flies, Eristalis hoverflies have been suggested to be strongly diurnal, but this is based on qualitative visualization by human observers. To quantify how hoverfly activity depends on internal and external factors, we here utilize a locomotor activity monitoring system. We show that Eristalis hoverflies are active during the entire light period when exposed to a 12 h light:12 h dark cycle, with a lower activity if exposed to light during the night. We show that the hoverflies’ locomotor activity is stable over their lifetime and that it does not depend on the diet provided. Surprisingly, we find no difference in activity between males and females, but the activity is significantly affected by the sex of an accompanying conspecific. Finally, we show that female hoverflies are more resilient to starvation than males. In summary, Eristalis hoverflies are resilient to a range of internal and external factors, supporting their use in long-term laboratory experiments.Electronic supplementary materialThe online version of this article (doi:10.1007/s00359-015-1051-2) contains supplementary material, which is available to authorized users.

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Novel Flicker-Sensitive Visual Circuit Neurons Inhibited by Stationary Patterns

Cited by 10 publications

References 61 publications

Selective attention in the honeybee optic lobes precedes behavioral choices

Selective attention in the honeybee optic lobes precedes behavioral choices

A higher order visual neuron tuned to the spatial amplitude spectra of natural scenes

Hoverfly locomotor activity is resilient to external influence and intrinsic factors

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