Peter Skorupski

Speed–accuracy tradeoffs in animal decision making

The traditional emphasis when measuring performance in animal cognition has been overwhelmingly on accuracy, independent of decision time. However, more recently, it has become clear that tradeoffs exist between decision speed and accuracy in many ecologically relevant tasks, for example, prey and predator detection and identification; pollinators choosing between flower species; and spatial exploration strategies. Obtaining high-quality information often increases sampling time, especially under noisy conditions. Here we discuss the mechanisms generating such speed-accuracy tradeoffs, their implications for animal decision making (including signalling, communication and mate choice) and the significance of differences in decision strategies among species, populations and individuals. The ecological relevance of such tradeoffs can be better understood by considering the neuronal mechanisms underlying decision-making processes.

What is comparable in comparative cognition

To understand how complex, or ‘advanced’ various forms of cognition are, and to compare them between species for evolutionary studies, we need to understand the diversity of neural–computational mechanisms that may be involved, and to identify the genetic changes that are necessary to mediate changes in cognitive functions. The same overt cognitive capacity might be mediated by entirely different neural circuitries in different species, with a many-to-one mapping between behavioural routines, computations and their neural implementations. Comparative behavioural research needs to be complemented with a bottom-up approach in which neurobiological and molecular-genetic analyses allow pinpointing of underlying neural and genetic bases that constrain cognitive variation. Often, only very minor differences in circuitry might be needed to generate major shifts in cognitive functions and the possibility that cognitive traits arise by convergence or parallel evolution needs to be taken seriously. Hereditary variation in cognitive traits between individuals of a species might be extensive, and selection experiments on cognitive traits might be a useful avenue to explore how rapidly changes in cognitive abilities occur in the face of pertinent selection pressures.

Photoreceptor Spectral Sensitivity in the Bumblebee, Bombus impatiens (Hymenoptera: Apidae)

The bumblebee Bombus impatiens is increasingly used as a model in comparative studies of colour vision, or in behavioural studies relying on perceptual discrimination of colour. However, full spectral sensitivity data on the photoreceptor inputs underlying colour vision are not available for B. impatiens. Since most known bee species are trichromatic, with photoreceptor spectral sensitivity peaks in the UV, blue and green regions of the spectrum, data from a related species, where spectral sensitivity measurements have been made, are often applied to B impatiens. Nevertheless, species differences in spectral tuning of equivalent photoreceptor classes may result in peaks that differ by several nm, which may have small but significant effects on colour discrimination ability. We therefore used intracellular recording to measure photoreceptor spectral sensitivity in B. impatiens. Spectral peaks were estimated at 347, 424 and 539 nm for UV, blue and green receptors, respectively, suggesting that this species is a UV-blue-green trichromat. Photoreceptor spectral sensitivity peaks are similar to previous measurements from Bombus terrestris, although there is a significant difference in the peak sensitivity of the blue receptor, which is shifted in the short wave direction by 12–13 nm in B. impatiens compared to B. terrestris.

Information processing in miniature brains

Since a comprehensive understanding of brain function and evolution in vertebrates is often hobbled by the sheer size of the nervous system, as well as ethical concerns, major research efforts have been made to understand the neural circuitry underpinning behaviour and cognition in invertebrates, and its costs and benefits under natural conditions. This special feature of Proceedings of the Royal Society B contains an idiosyncratic range of current research perspectives on neural underpinnings and adaptive benefits (and costs) of such diverse phenomena as spatial memory, colour vision, attention, spontaneous behaviour initiation, memory dynamics, relational rule learning and sleep, in a range of animals from marine invertebrates with exquisitely simple nervous systems to social insects forming societies with many thousands of individuals working together as a ‘superorganism’. This introduction provides context and history to tie the various approaches together, and concludes that there is an urgent need to understand the full neuron-to-neuron circuitry underlying various forms of information processing—not just to explore brain function comprehensively, but also to understand how (and how easily) cognitive capacities might evolve in the face of pertinent selection pressures. In the invertebrates, reaching these goals is becoming increasingly realistic.

Animal Cognition: An Insect's Sense of Time?

For Immanuel Kant, time was the very form of the inner sense, the bedrock of our consciousness and also the origin of arithmetic ability. New research on bumblebees has shown that even an invertebrate with a brain the size of a pinhead can actively sense the passage of elapsed time, allowing it to predict when certain salient events will occur in the future.

Spectral sensitivity of the green photoreceptor of winged pea aphids

Intracellular recordings are obtained from photoreceptors in the retina of winged (alate) pea aphids Acyrthosiphon pisum (Harris). The responses to monochromatic light, applied in 10‐nm steps over the range 320–650 nm, reveal that all recordings are from green receptors and the spectral sensitivity function of these photoreceptors peaks at 518 nm. A comparison between the spectral sensitivity of the green receptors and extracellular electroretinogram recordings suggests that additional sensitivity to the short‐wavelength light (ultraviolet and/or blue) is also likely to be present in the compound eye of pea aphids. An analysis of the pea aphid genome, comparing its translated nucleotide sequences with the those of the opsin genes of other insect species, supports this electrophysiological finding, although it could not be established whether A. pisum, in addition to the green receptor, has both blue and ultraviolet receptors in the compound eye. The implications of these results for the visual ecology of herbivorous insects are discussed.

Photoreceptor processing speed and input resistance changes during light adaptation correlate with spectral class in the bumblebee, Bombus impatiens.

Colour vision depends on comparison of signals from photoreceptors with different spectral sensitivities. However, response properties of photoreceptor cells may differ in ways other than spectral tuning. In insects, for example, broadband photoreceptors, with a major sensitivity peak in the green region of the spectrum (>500 nm), drive fast visual processes, which are largely blind to chromatic signals from more narrowly-tuned photoreceptors with peak sensitivities in the blue and UV regions of the spectrum. In addition, electrophysiological properties of the photoreceptor membrane may result in differences in response dynamics of photoreceptors of similar spectral class between species, and different spectral classes within a species. We used intracellular electrophysiological techniques to investigate response dynamics of the three spectral classes of photoreceptor underlying trichromatic colour vision in the bumblebee, Bombus impatiens, and we compare these with previously published data from a related species, Bombus terrestris. In both species, we found significantly faster responses in green, compared with blue- or UV-sensitive photoreceptors, although all 3 photoreceptor types are slower in B. impatiens than in B. terrestris. Integration times for light-adapted B. impatiens photoreceptors (estimated from impulse response half-width) were 11.3±1.6 ms for green photoreceptors compared with 18.6±4.4 ms and 15.6±4.4 for blue and UV, respectively. We also measured photoreceptor input resistance in dark- and light-adapted conditions. All photoreceptors showed a decrease in input resistance during light adaptation, but this decrease was considerably larger (declining to about 22% of the dark value) in green photoreceptors, compared to blue and UV (41% and 49%, respectively). Our results suggest that the conductances associated with light adaptation are largest in green photoreceptors, contributing to their greater temporal processing speed. We suggest that the faster temporal processing of green photoreceptors is related to their role in driving fast achromatic visual processes.

Can bees see at a glance

Primates can analyse visual scenes extremely rapidly, making accurate decisions for presentation times of only 20 ms. We asked whether bumblebees, despite having potentially more limited processing power, could similarly detect and discriminate visual patterns presented for durations of 100 ms or less. Bumblebees detected stimuli and discriminated between differently oriented and coloured stimuli when presented as briefly as 25 ms but failed to identify ecologically relevant shapes (predatory spiders on flowers) even when presented for 100 ms. This suggests an important difference between primate and insect visual processing, so that while primates can capture entire visual scenes ‘at a glance’, insects might have to rely on continuous online sampling of the world around them, using a process of active vision, which requires longer integration times.

Electrophysiological responses of crayfish oocytes to biogenic amines

Intracellular recordings were made from immature, growing oocytes of the crayfish Pacifastacus leniusciulus. Oocytes had a relatively negative resting potential of -74.7+/-2.2 mV (n=26; range -53 to -90) and a mean input resistance of 0.86+/-0.19 MOmega (n=22; range 0.17-3.3). Octopamine induced a long-lasting response involving biphasic changes in input resistance, together with bi- or multiphasic changes in membrane potential. The resistance-decreasing phase involved (in different oocytes) membrane hyperpolarization, depolarization or both. The resistance-increasing phase was usually a depolarization. The hyperpolarizing form of the resistance-decreasing response, and the depolarizing resistance-increasing response reversed in polarity at membrane potentials of (respectively) -90 and -92 mV, suggesting increases and decreases in K(+) conductance underly the biphasic changes in input resistance. The threshold concentration for the response was remarkably low (>10(-12) M) and showed little or no dose-dependence over the concentration range 10(-12)-10(-6) M. Similar responses were evoked by dopamine and serotonin (at 10(-9) M), although a higher proportion of oocytes responded to octopamine and/or dopamine than to serotonin.