Biology subjects

Buehlmann, C.

Publications and source records attributed to Buehlmann, C..

8 recordsLinked to original sources

bioRxiv2021

Impact of central complex lesions on visual orientation in ants: Turning behaviour, but not the overall movement direction, is disrupted

Wood ants are excellent navigators using a combination of innate and learnt navigational strategies to travel between their nest and feeding sites. Visual navigation in ants has been studied extensively, however, we only know little about the underlying neural mechanisms. The central complex (CX) is located at the midline of the insect brain. It receives sensory input that allows an insect to keep track of the direction of sensory cues relative to its own orientation and to control movement. We show here direct evidence for the involvement of the central complex in the innate visual orientation response of freely moving wood ants. Lesions in the CX disrupted the control of turning in a lateralised manner, but had no effect on the overall heading direction, walking speed or path straightness.

animal behavior and cognition↗

bioRxiv2021

Innate visual attraction in wood ants is a hardwired behaviour seen across different motivational and ecological contexts

Ants are expert navigators combining innate and learnt navigational strategies. Whereas we know that the ants feeding state segregates visual navigational memories in ants navigating along a learnt route, it is an open question if the motivational state also affects the ants innate visual preferences. Wood ant foragers show an innate attraction to conspicuous visual cues. These foragers inhabit cluttered woodland habitat and feed on honeydew from aphids on trees, hence, the attraction to tree-like objects might be an ecologically relevant behavior that is tailored to the wood ants foraging ecology. Foragers from other ant species with different foraging ecologies show very different innate attractions. We investigated here the innate visual response of wood ant foragers with different motivational states, i.e., unfed or fed, as well as males that show no foraging activity. Our results show that ants from all three groups orient towards a prominent visual cue, i.e., this intrinsic visuomotor response is not context dependent, but a hardwired behavior seen across different motivational and ecological contexts.

animal behavior and cognition↗

bioRxiv2021

A unified mechanism to support innate and learned use of visual landmark guidance in insects

Insects can navigate efficiently in both novel and familiar environments, and this requires flexiblity in how they are guided by sensory cues. A prominent landmark, for example, can ellicit strong innate behaviours (attraction or menotaxis) but can also be used, after learning, as a specific directional cue as part of a navigation memory. However, the mechanisms that allow both pathways to co-exist, interact or override each other are largely unknown. Here we propose a model for the behavioural integration of innate and learned guidance based on the neuroanatomy of the central complex (CX), adapted to control landmark guided behaviours. We consider a reward signal provided either by an innate attraction to landmarks or a long-term visual memory in the mushroom bodies (MB) that modulates the formation of a local vector memory in the CX. Using an operant strategy for a simulated agent exploring a simple world containing a single visual cue, we show how the generated short-term memory can support both innate and learned steering behaviour. In addition, we show how this architecture is consistent with the observed effects of unilateral MB lesions in ants that cause a reversion to innate behaviour. We suggest the formation of a directional memory in the CX can be interpreted as transforming rewarding (positive or negative) sensory signals into a mapping of the environment that describes the geometrical attractiveness (or repulsion). We discuss how this scheme might represent an ideal way to combine multisensory information gathered during the exploration of an environment and support optimized cue integration. 1 Author summaryIn this paper, we modeled the neural pathway allowing insects to perform landmark guided behaviours using their internal compass. First, we observed the intrinsic property of the connectome, extracted from drosophila online database, between the internal compass neurons and the steering neurons to support an oriented behaviour towards a single landmark. Then, we proposed and evaluated an adaptation of the bees path integration neural circuit, to sustain flexible landmark guidance behaviours such as attraction or menotaxis. We showed the model ability to form a memory during the exploration of the local environment to support both innate or learned navigation behaviour using a single landmark in the environment. In addtion, we demonstrated the transformation of a simple goodness/badness signal, from innate or long-term memory pathways, into an oriented steering signal that could be applied to other sensory pathways. Furthermore, by reproducing lesion experiments in the mushroom bodies of wood ants we highlight the consistency of the model with biological observation. We then discuss the different emergent properties and the potential outcome that this local, and operant, memory supports.

animal behavior and cognition↗

bioRxiv2020

Transfer of orientation memories in untethered wood ants (Formica rufa) from walking in an arena to walking on a motion compensation treadmill

The scale of natural insect navigation during foraging makes it challenging to study, in a controlled way, the navigation processes that an insect brain can support. Virtual Reality and trackball setups have offered experimental control over visual environments while studying tethered insects, but potential limitations and confounds introduced by tethering motivates the development of alternative untethered solutions. In this paper we validate the use of a motion compensator (or treadmill) to study visually-driven behaviour of freely moving wood ants (Formica rufa). We show how this setup allows naturalistic walking behaviour and motivation over long timeframes. Furthermore, we show that ants are able to transfer associative and navigational memories from classical maze and arena contexts to our treadmill. Thus, we demonstrate the possibility to study navigational behaviour over ecologically relevant durations (and virtual distances) in precisely controlled environments, bridging the gap between natural and highly controlled laboratory experiments. 1 Summary statementWe have developed and validated a motion compensating treadmill for wood ants which opens new perspectives to study insect navigation behaviour in a fully controlled manner over ecologically relevant durations.

animal behavior and cognition↗

bioRxiv2020

Mushroom bodies are required for accurate visual navigation in ants

Visual navigation in ants has long been a focus of experimental study [1-3], but only recently have explicit hypotheses about the underlying neural circuitry been proposed [4]. Indirect evidence suggests the mushroom bodies (MB), a known site of olfactory learning [5-10], may also be the substrate for visual memory in navigation tasks [11-14]. Computational modelling shows that MB neural architecture could support this function [15, 16], though there is no direct evidence that ants require MBs for visual navigation. Here we show that lesions of MB calyces impair ants visual navigation to a remembered food location whilst leaving their innate responses to visual cues unaffected. Ants are innately attracted to a large visual cue but we trained them to locate a food source at a specific angle to this visual cue. Subsequent bilateral or unilateral lesioning (through procaine hydrochloride injection) of the MB calyces, caused ants to revert to their innate cue attraction whilst control (saline) injected ants still approached the feeder. The ants path straightness and walking speed were unaffected by lesions. Reversion towards the cue direction occurred irrespective of whether it was ipsi-or contralateral to the lesion site, showing this is not due simply to an induced motor bias. Monocular occlusion did not diminish ants ability to locate the feeder, suggesting the lesion is not merely interrupting visual input to the calyx. The demonstrated dissociation between innate and learnt visual responses provides direct evidence for a specific role of the MB in navigational memory.

animal behavior and cognition↗

bioRxiv2020

Multimodal Influences on Learning Walks in Desert Ants (Cataglyphis fortis)

Ants are excellent navigators taking into account multimodal sensory information as they move through the world. To be able to accurately localise the nest at the end of a foraging journey, visual cues, wind direction and also olfactory cues need to be learnt. Learning walks are performed at the start of an ants foraging career or when the appearance of the nest surrounding has changed. We investigated here whether the structure of such learning walks in the desert ant Cataglyphis fortis takes into account wind direction in conjunction with the learning of new visual information. Ants learnt to travel back and forth between their nest and a feeder, and we then introduced a black cylinder near their nest to induce learning walks in regular foragers. By doing this across days with different prevailing wind directions, we were able to probe how ants balance the influence of different sensory modalities. We found that (i) the ants outwards headings are influenced by the direction of the wind with their routes deflected in such a way that they will arrive downwind of their nest when homing, (ii) a novel object along the route induces learning walks in experienced ants and (iii) the structure of learning walks is shaped by the wind direction rather than the position of the visual cue.

animal behavior and cognition↗

bioRxiv2019

Dynamic multimodal interactions in navigating wood ants: What do path details tell us about cue integration?

Ants are expert navigators using multiple cues from multiple sensory modalities to navigate successfully. Here, we present the results of systematic studies of multimodal cue use in navigating wood ants, Formica rufa. Ants learnt to navigate to a feeder that was defined by an olfactory cue, visual cue and airflow presented together. When ants learnt to find a feeder that was placed in the centre of the visual cue, well-trained ants were not anymore able to accurately approach the feeder when either the olfactory or visual cue were removed in tests. This confirms that some form of cue binding has taken place. However, in a visually simpler task with the feeder located at the edge of the visual cue, ants still approached the feeder accurately when individual cue components were removed. Hence, cue binding is flexible and depends on the navigational context. In general, cues act additively in determining the ants paths accuracy, i.e. the use of multiple cues increased navigation performance. Moreover, across different training conditions, we saw different motor patterns in response to different sensory cues. For instance, ants had more sinuous paths with more turns when they followed an odour plume but did not have any visual cues. Having visual information with the odour enhanced performance and therefore positively impacted on plume following. Interestingly, paths characteristics of ants from the two multimodal groups with a different visual task were different, suggesting that the observed flexibility in cue binding may be a result of the ants movement characteristics. Summary statementWe investigated the impact of multimodal information on navigating ants. Ants showed flexible response to multimodal information depending on the sensori-motor contingencies of the navigation task.

animal behavior and cognition↗

bioRxiv2019

Avoiding pitfalls: Trace conditioning and rapid aversive learning during route navigation in desert ants

The ability of bees and ants to learn long visually guided routes in complex environments is perhaps one of the most spectacular pieces of evidence for the impressive power of their small brains. While flying bees can visit flowers in an optimised sequence over kilometres, walking ants can precisely recapitulate routes of up to a hundred metres in complex environments. It is clear that route following depends largely on learnt visual information and we have good idea how views can guide individuals along them, however little is known about the mechanisms that control route learning and development. Here we show that ants in natural environments can actively learn a route detour to avoid a pit trap and that this depends on a process analogous to aversive trace conditioning. Views experienced before falling into the trap become associated with the ensuing negative outcome and thus trigger salutary turns on the subsequent trip. This drives the ants to orient away from the goal direction and avoid the trap. If the pit is avoided, the novel views experienced during the detour become positively reinforced and the new route crystallises. We discuss how such an interplay between appetitive and aversive memories might be implemented in insect neural circuitry.

animal behavior and cognition↗