Hive minded: like neurons, honey bees collectively integrate negative feedback to regulate decisions

Borofsky, Talia; Barranca, Victor J.; Zhou, Rebecca; Trentini, Dora von; Broadrup, Robert L.; Mayack, Christopher

doi:10.1016/j.anbehav.2020.07.023

Cited by 12 publications

(8 citation statements)

References 56 publications

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“…For instance, if resources are scarce and distributed in patches, individual learners experience large energy costs and predation risk which social learners can avoid by copying individual learners (Kameda andNakanishi 2002, Webster andLaland 2008). For example, the honeybee dance language, such as the famous waggle dance, allows honeybee colonies to forage at flower patches far away from the hive (I'Anson Price and Gr üter 2015) and adjust forager allocation when conditions change (Lau and Nieh 2010, Nieh 2010, Jack-McCollough and Nieh 2015, Borofsky et al 2020. Another way that social learning and even conformity can help individuals forage for food when resources are scarce is through cultural accumulation: if each generation builds upon the knowledge gained by the previous generation and improves foraging strategies, then more social learning could be advantageous (Whiten 2019).…”

Section: Discussionmentioning

confidence: 99%

Static environments with limited resources select for multiple foraging strategies rather than conformity

Borofsky

Feldman

2021

Ecological Monographs

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Social learning and conformity, or positive frequency-biased transmission, are important components of the evolution of culture and group identities in animals and humans. Previous theoretical work on the evolution of social learning and conformity when environmental states change found that conformity evolves for a large range of environmental conditions. However, the foraging environment can affect the adaptive benefits of social learning and conformity. Conformity can cause a population to focus mainly on one resource while ignoring other available resources, which can incite competition if the first resource is limited. We study the evolution of social learning and frequency-biased transmission in a limitedresource environment using a replicator model of a forager population feeding on two resources in which foragers set their resource preferences during an early learning stage. In sharp contrast with previous models, anti-conformity, or negative frequency-biased transmission, rather than conformity, evolves from a population of non-conformists under most environmental conditions. Numerical simulations suggest that both social learning and conformity cause the foragers to favor one resource over the other even though the resources provide the same benefit to foragers. Resource limitation favors anti-conformity because anti-conformity tends to force both resources to be exploited equally. Similarly, depletion of resources selects against social learning. However, increasing social learning is adaptive when independent discovery of foraging cues is difficult because it increases the rate at which individuals learn to find food. Consequently, in an environment with difficult-to-learn food cues, increased social learning is more likely to evolve. However, social learning does not emerge from a population of individual learners. Our results show that competition and consumer-resource interactions can alter the evolutionary course of social learning and transmission bias. As there are many examples of conformity in the animal kingdom, and especially in humans, future studies should explore what extensions of the model would allow conformity to first evolve.

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Section: Discussionmentioning

confidence: 99%

Static environments with limited resources select for multiple foraging strategies rather than conformity

Borofsky

Feldman

2021

Ecological Monographs

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“…Negative feedback has been considered in collective decisions, particularly as a means of symmetry breaking [22, 23, 24, 34], and in foraging, as a means of adapting to dynamically changing environments [10, 7, 12, 13]. Other than in entomology, negative feedback has been observed as a tool for noise reduction in gene networks [35, 36, 37] and in electronic systems [38, 39].…”

Section: Discussionmentioning

confidence: 99%

“…Here we have shown that negative feedback may play an important role in reducing variance in colony foraging performance. For example, considering the honeybee system that inspired our model, field observations have reported that levels of stop signalling increase in response to changes such as dangerous, overcrowded, or depleted food patches [13, 40, 11, 10]; however, it has not yet been fully understood why, even in static conditions, honeybees always deliver a small number of stop signals to foragers visiting the same forage patch [13, 10]. This pattern is consistent with our model, and the analysis presented is an interpretation for such observed behaviour.…”

Section: Discussionmentioning

confidence: 99%

Negative feedback may suppress variation to improve collective foraging performance

Reina

Marshall

2020

Preprint

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Social insect colonies use negative as well as positive feedback signals to regulate foraging behaviour. In ants and bees individual foragers have been observed to use negative pheromones or mechano-auditory signals to indicate that forage sources are not ideal, for example being unrewarded, crowded, or dangerous. Here we propose an alternative function for negative feedback signals during foraging, variance reduction. We show that while on average populations will converge to desired distributions over forage patches both with and without negative feedback signals, in small populations negative feedback reduces variation around the target distribution compared to the use of positive feedback alone. Our results are independent of the nature of the target distribution, providing it can be achieved by foragers collecting only local information. Since robustness is a key aim for biological systems, and deviation from target foraging distributions may be costly, we argue that this could be a further important and hitherto overlooked reason that negative feedback signals are used by foraging social insects.

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“…In collectively selecting a food source akin to decision making among neurons in the brain, each bee lacks knowledge of the detailed state of the colony, yet the entire group is able to effectively coordinate choices when accumulated positive feedback passes a threshold. Honeybees use waggle dances to encourage additional bees to forage at a profitable food source and also utilize stop signals to discourage other bees from foraging at a sub-optimal location (Seeley et al, 2012 ; Von Frisch, 2013 ; Borofsky et al, 2020 ). In contrast to the classical notion of Dale's law, a single honeybee can send out either type of feedback signal depending on its circumstances.…”

Section: Introductionmentioning

confidence: 99%

Functional Implications of Dale's Law in Balanced Neuronal Network Dynamics and Decision Making

et al. 2022

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The notion that a neuron transmits the same set of neurotransmitters at all of its post-synaptic connections, typically known as Dale's law, is well supported throughout the majority of the brain and is assumed in almost all theoretical studies investigating the mechanisms for computation in neuronal networks. Dale's law has numerous functional implications in fundamental sensory processing and decision-making tasks, and it plays a key role in the current understanding of the structure-function relationship in the brain. However, since exceptions to Dale's law have been discovered for certain neurons and because other biological systems with complex network structure incorporate individual units that send both positive and negative feedback signals, we investigate the functional implications of network model dynamics that violate Dale's law by allowing each neuron to send out both excitatory and inhibitory signals to its neighbors. We show how balanced network dynamics, in which large excitatory and inhibitory inputs are dynamically adjusted such that input fluctuations produce irregular firing events, are theoretically preserved for a single population of neurons violating Dale's law. We further leverage this single-population network model in the context of two competing pools of neurons to demonstrate that effective decision-making dynamics are also produced, agreeing with experimental observations from honeybee dynamics in selecting a food source and artificial neural networks trained in optimal selection. Through direct comparison with the classical two-population balanced neuronal network, we argue that the one-population network demonstrates more robust balanced activity for systems with less computational units, such as honeybee colonies, whereas the two-population network exhibits a more rapid response to temporal variations in network inputs, as required by the brain. We expect this study will shed light on the role of neurons violating Dale's law found in experiment as well as shared design principles across biological systems that perform complex computations.

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Hive minded: like neurons, honey bees collectively integrate negative feedback to regulate decisions

Cited by 12 publications

References 56 publications

Static environments with limited resources select for multiple foraging strategies rather than conformity

Static environments with limited resources select for multiple foraging strategies rather than conformity

Negative feedback may suppress variation to improve collective foraging performance

Functional Implications of Dale's Law in Balanced Neuronal Network Dynamics and Decision Making

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