The role of attractive and repellent scene memories in ant homing (<i>Myrmecia croslandi</i>)

Murray, Trevor G.; Kócsi, Zoltán; Dahmen, Hansjürgen; Narendra, Ajay; Moël, Florent Le; Wystrach, Antoine; Zeil, Jochen

doi:10.1242/jeb.210021

Cited by 39 publications

(60 citation statements)

References 67 publications

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“…Therefore, the current model makes the counter-intuitive prediction that a similar behaviour is expected when the ant is located exactly at the nest and when in unfamiliar surroundings. We recently verified this prediction with ants tethered on an air suspended treadmill [93].…”

Section: Predictions and Further Hypothesesmentioning

confidence: 68%

Opponent processes in visual memories: A model of attraction and repulsion in navigating insects’ mushroom bodies

Moël

Wystrach

2020

PLoS Comput Biol

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Solitary foraging insects display stunning navigational behaviours in visually complex natural environments. Current literature assumes that these insects are mostly driven by attractive visual memories, which are learnt when the insect's gaze is precisely oriented toward the goal direction, typically along its familiar route or towards its nest. That way, an insect could return home by simply moving in the direction that appears most familiar. Here we show using virtual reconstructions of natural environments that this principle suffers from fundamental drawbacks, notably, a given view of the world does not provide information about whether the agent should turn or not to reach its goal. We propose a simple model where the agent continuously compares its current view with both goal and anti-goal visual memories, which are treated as attractive and repulsive respectively. We show that this strategy effectively results in an opponent process, albeit not at the perceptual level-such as those proposed for colour vision or polarisation detection-but at the level of the environmental space. This opponent process results in a signal that strongly correlates with the angular error of the current body orientation so that a single view of the world now suffices to indicate whether the agent should turn or not. By incorporating this principle into a simple agent navigating in reconstructed natural environments, we show that it overcomes the usual shortcomings and produces a step-increase in navigation effectiveness and robustness. Our findings provide a functional explanation to recent behavioural observations in ants and why and how so-called aversive and appetitive memories must be combined. We propose a likely neural implementation based on insects' mushroom bodies' circuitry that produces behavioural and neural predictions contrasting with previous models.

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Section: Predictions and Further Hypothesesmentioning

confidence: 68%

Opponent processes in visual memories: A model of attraction and repulsion in navigating insects’ mushroom bodies

Moël

Wystrach

2020

PLoS Comput Biol

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“…Previous studies assumed that ants memorise views while facing the goal [20][21][22] and anti-goal [23][24][25] ) directions, and that they must consequently align their body in these same directions to recognise a learnt view as familiar [26][27][28] . On the contrary, our modelling effort suggests that ants should rather recognise views based on whether the route direction stands on their 'left or right' rather than 'in front or behind'.…”

Section: The Recognition Of Familiar Views Triggers Compensatory Leftmentioning

confidence: 99%

“…3, left panels) was based on the recognition of terrestrial rather than celestial cues. It however remains unclear whether the sun rotation had an impact on ants in unfamiliar terrain, as ants in this situation regularly alternate between left and right turns anyway 25 . Finally, to ensure that the observed effect on route was not due to an innate bias at this particular location, we repeated this experiment with ants tethered at the exact same route location and body orientation, but this time only with ants that were trained to an alternative straight route, which was aligned with the tethered direction of the trackball (Fig.…”

Section: Guidance Based On Memorised Views Involves the Celestial Commentioning

confidence: 99%

A lateralised design for the interaction of visual memories and heading representations in navigating ants

Wystrach¹,

Moël²,

Clément³

et al. 2020

Preprint

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The navigational skills of ants, bees and wasps represent one of the most baffling examples of the powers of minuscule brains. Insects store long-term memories of the visual scenes they experience, and they use compass cues to build a robust representation of directions. We know reasonably well how long-term memories are formed, in a brain area called the Mushroom Bodies (MB), as well as how heading representations are formed in another brain area called the Central Complex (CX). However, how such memories and heading representations interact to produce powerful navigational behaviours remains unclear. Here we combine behavioural experiments with computational modelling that is strictly based on connectomic data to provide a new perspective on how navigation might be orchestrated in these insects. Our results reveal a lateralised design, where signals about whether to turn left or right are segregated in the left and right hemispheres, respectively. Furthermore, we show that guidance is a two-stage process: the recognition of visual memories, presumably in the MBs, does not directly drive the motor command, but instead updates a desired heading, presumably in the CX, which in turn is used to control guidance using celestial compass information. Overall, this circuit enables ants to recognise views independently of their body orientation, and combines terrestrial and celestial cues in a way that produces exceptionally robust navigation.

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“…Therefore, the current model makes the counter-intuitive prediction that similar behaviour is expected when the ant is located exactly at the nest and when in unfamiliar surroundings. We recently verified this prediction with ants tethered on an air suspended treadmill (93).…”

Section: Predictions and Further Hypothesesmentioning

confidence: 76%

Opponent processes in visual memories: a model of attraction and repulsion in navigating insects’ mushroom bodies

Moel

Wystrach²

2019

Preprint

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19Solitary foraging insects display stunning navigational behaviours in visually complex natural 20 environments. Current literature assumes that these insects are mostly driven by attractive 21 visual memories, which are learnt when the insect's gaze is precisely oriented toward the goal 22 direction, typically along its familiar route or towards its nest. That way, an insect could return 23 105 106This principle can be directly applied to recapitulate idiosyncratic routes, given a set of visual 107 memories stored along them. Agent-based simulations have shown that the 'walking forward 108 in the most familiar direction' rule enables agents to recapitulate routes (8,24,29,38) in a way 109 that closely resembles what is observed in solitary foraging ants (18,39,40). These models are 110 further supported by the well-choreographed 'learning walks' displayed by ants -as well as 111 the equivalent 'learning flights' displayed by bees and wasps (41-45) -around their nest (or a 112 food source). During learning walks, ants appear to systematically pause while facing towards 113 the nest (or a food source), presumably to memorise 'correctly aligned' views from multiple 114 locations around the goal (12,14,(46)(47)(48). Given such a visual memory bank, models show 115 that the exact same principle used for route following is able to produce a search centred on 116 the goal location (24,27). There again, the models' emerging search patterns capture several 117 aspects of the ants' visually driven search (38,46,49,50). 119The greatest appeal of familiarity-based models is that the comparison of the current and 120 memorised view needs only to output one familiarity value. To get this familiarity value, there 121 is no need for finding correspondence between parts of the visual field and a direction in the 122 world. This contrasts with so called 'correspondence models' where features must be 123 extracted from panoramas, and matched locally. Familiarity-based models do not need 124 retinotopic mapping to be preserved at the comparison stage. This fits well the connectivity 125 of the insect Mushroom Bodies (51), where memories of visual scenes are likely encoded 126 (8,9). Indeed, in visually navigating insects, the visual input as perceived through their low-127 resolution eyes and processed by early optic neural relays (52-54), is then projected to more 128 than 100,000 Mushroom Body cells (Kenyon Cells: KCs) through an apparently random 129 pattern of connections, likely disrupting retinotopic organisation (55-57). Remarkably, given 130 the synaptic plasticity observed at the output of the MB during learning (58-60), the resulting 131 activity of the MB output neurons naturally provides a measure of familiarity of the current 132 sensory input (8,51). 133 A simplified model of the ant and bees circuitry shows that the Mushroom Bodies provides 134 enough 'memory space' for an agent to store the required visual information to recapitulate a 135 10 meter long-route in a naturalistic environment -here again, by simply...

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The role of attractive and repellent scene memories in ant homing (Myrmecia croslandi)

Cited by 39 publications

References 67 publications

Opponent processes in visual memories: A model of attraction and repulsion in navigating insects’ mushroom bodies

Opponent processes in visual memories: A model of attraction and repulsion in navigating insects’ mushroom bodies

A lateralised design for the interaction of visual memories and heading representations in navigating ants

Opponent processes in visual memories: a model of attraction and repulsion in navigating insects’ mushroom bodies

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