Visual acuity of the honey bee retina and the limits for feature detection

Abstract

Visual abilities of the honey bee have been studied for more than 100 years, recently revealing unexpectedly sophisticated cognitive skills rivalling those of vertebrates. However, the physiological limits of the honey bee eye have been largely unaddressed and only studied in an unnatural, dark state. Using a bright display and intracellular recordings, we here systematically investigated the angular sensitivity across the light adapted eye of honey bee foragers. Angular sensitivity is a measure of photoreceptor receptive field size and thus small values indicate higher visual acuity. Our recordings reveal a fronto-ventral acute zone in which angular sensitivity falls below 1.9°, some 30% smaller than previously reported. By measuring receptor noise and responses to moving dark objects, we also obtained direct measures of the smallest features detectable by the retina. In the frontal eye, single photoreceptors respond to objects as small as 0.6° × 0.6°, with >99% reliability. This indicates that honey bee foragers possess significantly better resolution than previously reported or estimated behaviourally, and commonly assumed in modelling of bee acuity.

Spatial Resolving Power and Contrast Sensitivity Are Adapted for Ambient Light Conditions in Australian Myrmecia Ants

“…These anatomical estimates differ markedly from those obtained using behavioural discrimination tests, which were 0.26 cpd, giving a ø of 1.92 • (Srinivasan and Lehrer, 1988), or ø of 1.78 based on the spatial resolving power of 0.28 cpd (Horridge, 2003). A recent study using intracellular recording techniques showed that single photoreceptors in the light-adapted state are capable of responding to objects as small as 0.6 × 0.6 • (Rigosi et al, 2017), which is at least 5 times smaller than the smallest features bees are known to behaviourally resolve (Lehrer and Bischof, 1995;Giurfa et al, 1996;Giurfa and Vorobyev, 1998). The differences in results may be due to different experimental conditions including light intensity or the eye's adaptation state, and the recording level in the visual processing pathway.…”

“…From their anatomy, it appears that the nocturnal Myrmecia pyriformis has lower spatial resolving power (interommatidial angle of 2.1 • ; Reid, 2010) compared to the diurnal Myrmecia gulosa (interommatidial angle of 1.7 • ; Via, 1977). Intracellular recordings also provide the information about the visual field of photoreceptors (Rigosi et al, 2017). One technique that can provide information of both the spatial resolving power and contrast sensitivity simultaneously is pattern electroretinography [PERG; (Porciatti, 2007)].…”

Bumblebee visual allometry results in locally improved resolution and globally improved sensitivity

“…S2B), which would result in local differences in focal length and may lead to topological variation in acceptance angle and, thus, the optical cut-off frequency. An approximately 25% increase in acceptance angle has indeed been found between frontally and laterally facing ommatidia in honeybees (Rigosi et al 2017). Two additional confounds for determining visual acuity from anatomical measurements are that acceptance angle varies between states of light and dark adaptation (Warrant and McIntyre 1993), and that both object illumination and contrast also influence an eye's effective resolution (Snyder et al 1977, Warrant 1999.…”

Spatial Vision and Visually Guided Behavior in Apidae

“…or, most accurately, be determined electrophysiologically. Rigosi et al [17] measured mean acceptance angles of worker honeybee photoreceptors in the equatorial eye region as 2.2 • in the horizontal and 2.3 • in the vertical direction, and minimal acceptance angles down to 1.6…”