Different Roles for Honey Bee Mushroom Bodies and Central Complex in Visual Learning of Colored Lights in an Aversive Conditioning Assay

Plath, Jenny Aino; Entler, Brian V.; Kirkerud, Nicholas H.; Schlegel, Ulrike; Galizia, C. Giovanni; Barron, Andrew B.

doi:10.3389/fnbeh.2017.00098

Cited by 35 publications

(55 citation statements)

References 82 publications

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“…While only a few studies use comparable automated measurements to study aversive learning in honey bees, similar performance is consistently reported. Across four other papers, many including multiple experiments and groups, we found that bees in groups that responded above chance had an average CCR of around 61% [38][39][40]44]. It appears that bees in our spatial group showed a typical response.…”

Section: Overviewmentioning

confidence: 49%

“…A growing body of research investigates aversive conditioning in a shuttle box, where unrestrained bees learn to alter their behavior to reduce shock or other aversive stimuli in a small runway. Research using this method has explored areas such as learning differences between drones and workers [38], learned helplessness [39], visual discrimination [40], modulation of phototaxis [41], detection of narcotics [42], and the roles of the dopamine, octopamine and the mushroom body in aversive learning [41,43,44].…”

Section: Introductionmentioning

confidence: 99%

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Conspecific and interspecific stimuli reduce initial performance in an aversive learning task in honey bees (Apis mellifera)

et al. 2020

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The purpose of this experiment was to investigate whether honey bees (Apis mellifera) are able to use social discriminative stimuli in a spatial aversive conditioning paradigm. We tested bees' ability to avoid shock in a shuttle box apparatus across multiple groups when either shock, or the absence of shock, was associated with a live hive mate, a dead hive mate, a live Polistes exclamans wasp or a dead wasp. Additionally, we used several control groups common to bee shuttle box research where shock was only associated with spatial cues, or where shock was associated with a blue or yellow color. While bees were able to learn the aversive task in a simple spatial discrimination, the presence of any other stimuli (color, another bee, or a wasp) reduced initial performance. While the color biases we discovered are in line with other experiments, the finding that the presence of another animal reduces performance is novel. Generally, it appears that the use of bees or wasps as stimuli initially causes an increase in overall activity that interferes with early performance in the spatial task. During the course of the experiment, the bees habituate to the insect stimuli (bee or wasp), and begin learning the aversive task. Additionally, we found that experimental subject bees did not discriminate between bees or wasps used as stimulus animals, nor did they discriminate between live or dead stimulus animals. This may occur, in part, due to the specialized nature of the worker honey bee. Results are discussed with implications for continual research on honey bees as models of aversive learning, as well as research on insect social learning in general.

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Section: Overviewmentioning

confidence: 49%

Section: Introductionmentioning

confidence: 99%

Conspecific and interspecific stimuli reduce initial performance in an aversive learning task in honey bees (Apis mellifera)

et al. 2020

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“…Furthermore, there is no anatomical evidence that the VUMmx1 neuron (or any other VUM neuron) is directly connected with any of the visual pathways (Schröter et al, 2007), suggesting that the reward system for visual learning might be different (and probably more complex) than that for the olfactory system. Recently, Plath et al (2017) showed that color learning in an aversive conditioning assay involves both MB ventral lobes and the central complex (CX). However, so far, no evidence for a direct connection between MB output neurons and the CX has been found in honey bees, and Plath et al (2017) thus suggested a more indirect connection, which would also prolong processing time compared with olfactory learning.…”

Section: Discussionmentioning

confidence: 99%

“…Recently, Plath et al (2017) showed that color learning in an aversive conditioning assay involves both MB ventral lobes and the central complex (CX). However, so far, no evidence for a direct connection between MB output neurons and the CX has been found in honey bees, and Plath et al (2017) thus suggested a more indirect connection, which would also prolong processing time compared with olfactory learning.…”

Section: Discussionmentioning

confidence: 99%

Length of stimulus presentation and visual angle are critical for efficient visual PER conditioning in the restrained honey bee,Apis mellifera

Lichtenstein

Spaethe

2018

Journal of Experimental Biology

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Learning visual cues is an essential capability of bees for vital behaviors such as orientation in space and recognition of nest sites, food sources and mating partners. To study learning and memory in bees under controlled conditions, the proboscis extension response (PER) provides a well-established behavioral paradigm. While many studies have used the PER paradigm to test olfactory learning in bees because of its robustness and reproducibility, studies on PER conditioning of visual stimuli are rare. In this study, we designed a new setup to test the learning performance of restrained honey bees and the impact of several parameters: stimulus presentation length, stimulus size (i.e. visual angle) and ambient illumination. Intact honey bee workers could successfully discriminate between two monochromatic lights when the color stimulus was presented for 4, 7 and 10 s before a sugar reward was offered, reaching similar performance levels to those for olfactory conditioning. However, bees did not learn at shorter presentation durations. Similar to free-flying honey bees, harnessed bees were able to associate a visual stimulus with a reward at small visual angles (5 deg) but failed to utilize the chromatic information to discriminate the learned stimulus from a novel color. Finally, ambient light had no effect on acquisition performance. We discuss possible reasons for the distinct differences between olfactory and visual PER conditioning.

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“…During the development of holometabolous insects, the brain changes drastically not only in size but also in structure, especially during the larval and pupal stages [1]. Prominent structures of the insect brain are the optic lobes (visual system), antennal lobes (olfactory system), the central complex (which plays an essential role in sky-compass orientation [2] and aversive colour learning in honeybees [3], and in other insects regulates a wide repertoire of behaviours including locomotion, stridulation, spatial orientation and spatial memory [4, 5]), and higher order centres that coordinate sensory integration called the mushroom bodies (MBs) [6-8]. The mushroom bodies, thought to be an analogue of the mammalian hippocampus, are paired brain structures responsible for learning and memory functions in insects [9, 10].…”

Section: Introductionmentioning

confidence: 99%

Temporal correlation of elevated PRMT1 gene expression with mushroom body neurogenesis during bumblebee brain development

Guan

Egertová

Perry

et al. 2018

Preprint

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11Proper neural development in insects depends on the controlled proliferation and differentiation of 12 neural precursors. In holometabolous insects, these processes must be coordinated during larval and 13 pupal development. Recently, protein arginine methylation has come into focus as an important 14 mechanism of controlling neural stem cell proliferation and differentiation in mammals. Whether a 15 similar mechanism is at work in insects is unknown. We investigated this possibility by determining 16 the expression pattern of three protein arginine methyltransferase mRNAs (PRMT1, 4 and 5) in the 17 developing brain of bumblebees by in situ hybridisation. We detected expression in neural precursors 18 and neurons in functionally important brain areas throughout development. We found markedly higher 19 expression of PRMT1, but not PRMT4 and PRMT5, in regions of mushroom bodies containing 20 dividing cells during pupal stages at the time of active neurogenesis within this brain area. At later 21 stages of development, PRMT1 expression levels were found to be uniform and did not correlate with 22 actively dividing cells. Our study suggests a role for PRMT1 in regulating neural precursor divisions 23 in the mushroom bodies of bumblebees during the period of neurogenesis. 24 25 Key words: development, mitotically-active cells, mushroom body, PRMT 26 4 neural progenitors and a GMC that divides again to generate two neurons [15]. There are 90 type I 54 and eight type II NBs found in each Drosophila brain lobe [15], where type II NBs produce many 55 neurons for important neuropile substructures of the brain, in particular the central complex [15]. 56 Type I neuroblast divisions occur during the development of the honeybee brain [1]. It is 57 unclear whether type II neuroblasts are present in bees. Farris et al. [1] reported no evidence in 58 honeybee mushroom bodies of neuroblast divisions other than the classic type I division pattern. 59However, this work was published before type II NBs were identified, leaving open the possibility 60 that such cells might exist in bees. In this study we focus on the mushroom bodies. In Drosophila the 61 neuroblasts that form the mushroom body do not undergo type II neuroblast divisions during 62 embryonic stage, as judged by a lack of cells in this lineage that express markers of transit amplifying 63 intermediate neural progenitors [16]. 64In the developing bee, neural precursor division and neurogenesis causes a dramatic change in 65 the cytoarchitecture of mushroom bodies [1]. During the larval and pre-pupal stages the neuropils 66 begin to form with the peduncular neuropil first observable during the third larval instar (six days 67 from egg laying) and the calycal neuropils first seen during the pre-pupal stage (10 to 11 days from 68 egg laying) [13]. Normally at pupal day 5, neurogenesis in the mushroom bodies of bees cease [1]. 69However, the growth of the mushroom body neuropil does not cease but continues throughout adult 70 life [17]. The developmental stages of worker h...

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Different Roles for Honey Bee Mushroom Bodies and Central Complex in Visual Learning of Colored Lights in an Aversive Conditioning Assay

Cited by 35 publications

References 82 publications

Conspecific and interspecific stimuli reduce initial performance in an aversive learning task in honey bees (Apis mellifera)

Conspecific and interspecific stimuli reduce initial performance in an aversive learning task in honey bees (Apis mellifera)

Length of stimulus presentation and visual angle are critical for efficient visual PER conditioning in the restrained honey bee,Apis mellifera

Temporal correlation of elevated PRMT1 gene expression with mushroom body neurogenesis during bumblebee brain development

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