Multisensory integration supports configural learning of a home refuge in the whip spiderPhrynus marginemaculatus

Abstract

Whip spiders (Amblypygi) reside in structurally complex habitats and are nocturnally active yet display notable navigational abilities. From the theory that uncertainty in sensory inputs should promote multisensory representations to guide behavior, we hypothesized that their navigation is supported by a multisensory and perhaps configural representation of navigational inputs, an ability documented in a few insects and never reported in arachnids. We trained Phrynus marginemaculatus to recognize a home shelter characterized by both discriminative olfactory and tactile stimuli. In tests, subjects readily discriminated between shelters based on the paired stimuli. However, subjects failed to recognize the shelter in tests with either of the component stimuli alone. This result is consistent with the hypothesis that the terminal phase of their navigational behavior, shelter recognition, can be supported by the integration of multisensory stimuli as an enduring, configural representation. We hypothesize that multisensory learning occurs in the whip spiders’ extraordinarily large mushroom bodies, which may functionally resemble the hippocampus of vertebrates.

Exploring Higher-Order Conceptual Learning in an Arthropod with a Large Multisensory Processing Center

“…Specifically, we used black, heat-treated, waterproof aluminum oxide abrasive (Norton Abrasives, Worcester, MA, USA) in 80 coarse grit and 320 extra fine grit. These grit grades are similar to grades shown to be distinguishable by P. marginemaculatus [61,75].…”

“…In both experiments, we did not see clear evidence of improvement over the course of learning trials. This, combined with ample evidence of associational learning in P. marginemaculatus [74,75,77,78,97], suggests that either our training trials or the period of training were not sufficient for P. marginemaculaus and P. laevifrons to learn the intended associations in our experiments. The trends toward significance in the novel stimulus trials in both experiments may reflect that these novel trials were conducted after more training trials than the trained stimulus trials.…”

“…With this in mind, it is expected that the species is capable of fielding complex navigational challenges that demand the neuroanatomy and sensory physiology integral for higher-order learning. Indeed, it is this species that has been the focus of most prior research on learning and navigation [61,75,77]. For this first experiment, we purchased 12 P. marginemaculatus from an online source ("Ken the Bug Guy").…”

“…Phrynus marginemaculatus learn to discriminate tactile and visual stimuli and can associate specific stimuli in each modality with an available shelter [61,74]. This species has also been shown to integrate multimodal cues into a single representation of a home refuge-i.e., configural learning [75]. Paraphrynus laevifrons can navigate to their home shelters on a vertical maze and can return to their previously inhabited shelter based on scent, not location [76].…”

Odour Learning Bees Have Longer Foraging Careers Than Non-learners in a Natural Environment

“…The selection pressures operating on cognitive traits are likely influenced by multiple sensory modalities. In addition to visual cues, most animals will use a combination of sound, taste, touch, and/or smell when forming learnt associations (Dukas, 2008;De Agrò et al, 2020;Flanigan et al, 2021). The relative importance of different sensory modalities can sometimes be obvious with regards to species ecology; depending on whether the animal is active at day or night, either vision or olfaction are often a more prominent modality than the other (Balkenius et al, 2006).…”