Motor cognition in plants: from thought to real experiments.

Motor cognition involves the process of planning and executing goal-directed movements and recognizing, anticipating, and interpreting others' actions. Motor cognitive functions are generally associated with the presence of a brain and are ascribed only to humans and other animal species. A growing body of evidence suggests that aneural organisms, like climbing plants, exhibit behaviors driven by the intention to achieve goals, challenging our understanding of cognition. Here, we propose an inclusive perspective under motor cognition to explain climbing plants' behavior. We will first review our empirical research based on kinematical analysis to understand movement in pea plants. Then, we situate this empirical research within the current theoretical debate aimed at extending the principles of cognition to aneural organisms. A novel comparative perspective that considers the perception-action cycle, involving transforming perceived environmental elements into intended movement patterns, is provided.

Handedness in Animals and Plants.

Structural and functional asymmetries are traceable in every form of life, and some lateralities are homologous. Functionally speaking, the division of labour between the two halves of the brain is a basic characteristic of the nervous system that arose even before the appearance of vertebrates. The most well-known expression of this specialisation in humans is hand dominance, also known as handedness. Even if hand/limb/paw dominance is far more commonly associated with the presence of a nervous system, it is also observed in its own form in aneural organisms, such as plants. To date, little is known regarding the possible functional significance of this dominance in plants, and many questions remain open (among them, whether it reflects a generalised behavioural asymmetry). Here, we propose a comparative approach to the study of handedness, including plants, by taking advantage of the experimental models and paradigms already used to study laterality in humans and various animal species. By taking this approach, we aim to enrich our knowledge of the concept of handedness across natural kingdoms.

Artificial and biological supports are different for pea plants.

Previous studies on the kinematics of pea plants' ascent and attach behavior have demonstrated that the signature of their movement varies depending on the kind of support. So far, these studies have been confined to artificial supports (e.g. wooden sticks). Little is known regarding the conditions under which pea plants could rely on biological supports (e.g. neighboring plants) for climbing toward the light. In this study, we capitalize on the 3D kinematic analysis of movement to ascertain whether pea plants scale their kinematics differently depending on whether they aim for artificial or biological support. Results suggest that biological support determines a smoother and more accurate behavior than that elicited by the artificial one. These results shed light on pea plants' ability to detect and classify the properties of objects and implement a movement plan attuned to the very nature of the support. We contend that such differences depend on the augmented multisensory experience elicited by the biological support.

Ascent and Attachment in Pea Plants: A Matter of Iteration.

Pea plants (Pisum sativum L.) can perceive the presence of potential supports in the environment and flexibly adapt their behavior to clasp them. How pea plants control and perfect this behavior during growth remains unexplored. Here, we attempt to fill this gap by studying the movement of the apex and the tendrils at different leaves using three-dimensional (3D) kinematical analysis. We hypothesized that plants accumulate information and resources through the circumnutation movements of each leaf. Information generates the kinematical coordinates for the final launch towards the potential support. Results suggest that developing a functional approach to grasp movement may involve an interactive trial and error process based on continuous cross-talk across leaves. This internal communication provides evidence that plants adopt plastic responses in a way that optimally corresponds to support search scenarios.

'United we stand, divided we fall': intertwining as evidence of joint actions in pea plants.

In life, it is common for almost every kind of organism to interact with one another. In the human realm, such interactions are at the basis of joint actions, when two or more agents syntonize their actions to achieve a common goal. Shared intentionality is the theoretical construct referring to the suite of abilities that enable such coordinated and collaborative interactions. While shared intentionality has become an important concept in research on social cognition, there is controversy surrounding its evolutionary origins. An aspect still unexplored but promising to bring new insights into this open debate is the study of aneural organisms. To fill this gap, here we investigate whether climbing plants can act jointly to achieve a common goal, i.e. reaching the light. We examined Pisum Sativum plants growing intertwined when there is a need to climb but a potential support is not present in the environment. Three-dimensional kinematic analysis of their movement revealed a coordinated and complementary behaviour. They tend to coordinate their movement in time and space to achieve a joint climbing. By deliberately extending the context in which a joint action takes place, we pay tribute to the complex nature of this social phenomenon. The next challenge for the field of joint action is to generate a perspective that links coordination mechanisms to an evolutionary framework across taxa.

Evidence of motor intentions in plants: A kinematical study.

"How" an action is performed is not solely determined by biomechanical constraints, but it depends on the agent's intention, that is, "why" the action is performed. Recent findings suggest that intentions can be specified at a tangible and quantifiable level in the kinematics of movements; that is, different motor intentions translate into different kinematic patterns. In the present study, we used 3D kinematical analysis to investigate whether the organization of climbing plants' approach-to-grasp action is sensitive to the kind of intention driving their movement toward potential support, namely individual or social. For the individual condition, a plant in isolation acted upon the support. For the social condition, two plants were located in the same pot opposite to each other with a support in the middle. Results indicate differences in kinematics depending on the context within which the plant is acting. In the presence of neighbors, climbing plants are able to modify their behaviors to maximize their long-term gains, including the grasping of a potential support. Overall, these data suggest that the organization of climbing plants' kinematics is sensitive to the "intention" driving their movement toward a potential support. To discuss this phenomenon, we capitalize on the concept of motor intentionality in plants and on available theories concerned to motor cognition. We suggest how they could be revisited to explain the intentionality component inherent in plant life and other brainless organisms. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Decision-Making Underlying Support-Searching in Pea Plants.

Finding a suitable support is a key process in the life history of climbing plants. Those that find a suitable support have greater performance and fitness than those that remain prostrate. Numerous studies on climbing plant behavior have elucidated the mechanistic details of support-searching and attachment. Far fewer studies have addressed the ecological significance of support-searching behavior and the factors that affect it. Among these, the diameter of supports influences their suitability. When the support diameter increases beyond some point, climbing plants are unable to maintain tensional forces and therefore lose attachment to the trellis. Here, we further investigate this issue by placing pea plants (Pisum sativum L.) in the situation of choosing between supports of different diameters while their movement was recorded by means of a three-dimensional motion analysis system. The results indicate that the way pea plants move can vary depending on whether they are presented with one or two potential supports. Furthermore, when presented with a choice between thin and thick supports, the plants showed a distinct preference for the former than the latter. The present findings shed further light on how climbing plants make decisions regarding support-searching and provide evidence that plants adopt one of several alternative plastic responses in a way that optimally corresponds to environmental scenarios.

Classifying Circumnutation in Pea Plants via Supervised Machine Learning.

Climbing plants require an external support to grow vertically and enhance light acquisition. Climbers that find a suitable support demonstrate greater performance and fitness than those that remain prostrate. Support search is characterized by oscillatory movements (i.e., circumnutation), in which plants rotate around a central axis during their growth. Numerous studies have elucidated the mechanistic details of circumnutation, but how this phenomenon is controlled during support searching remains unclear. To fill this gap, here we tested whether simulation-based machine learning methods can capture differences in movement patterns nested in actual kinematical data. We compared machine learning classifiers with the aim of generating models that learn to discriminate between circumnutation patterns related to the presence/absence of a support in the environment. Results indicate that there is a difference in the pattern of circumnutation, depending on the presence of a support, that can be learned and classified rather accurately. We also identify distinctive kinematic features at the level of the junction underneath the tendrils that seems to be a superior indicator for discerning the presence/absence of the support by the plant. Overall, machine learning approaches appear to be powerful tools for understanding the movement of plants.

Kinematic Evidence of Root-to-Shoot Signaling for the Coding of Support Thickness in Pea Plants.

Plants such as climbers characterized by stems or tendrils need to find a potential support (e.g., pole, stick, other plants or trees) to reach greater light exposure. Since the time when Darwin carried out research on climbing plants, several studies on plants' searching and attachment behaviors have demonstrated their unique ability to process some features of a support to modulate their movements accordingly. Nevertheless, the strategies underlying this ability have yet to be uncovered. The present research tries to fill this gap by investigating how the interaction between above- (i.e., stems, tendrils, …) and below-ground (i.e., the root system) plant organs influences the kinematics of their approach-to-grasp movements. Using three-dimensional (3D) kinematic analysis, we characterized the movements of pea plants (Pisum sativum L.) as they leaned towards supports whose below- and above-ground parts were characterized by different thicknesses (i.e., thin below- thick above-ground, or the opposite). As a control condition, the plants were placed next to supports with the same thickness below and above ground (i.e., either entirely thin or thick). The results suggest that the information regarding below- and above-ground parts of a support appears to be integrated and modulates the reach-to-grasp behavior of the plant. Information about the support conveyed by the root system seems to be particularly important to achieve the end-goal of movement.

Cracking the code: a comparative approach to plant communication.

The linguistic behavior of humans is usually considered the point of reference for studying the origin and evolution of language. As commonly defined, language is a form of communication between human beings; many have argued that it is unique to humans as there is no apparent equivalent for it in non-human organisms. How language is used as a means of communication is examined in this essay from a biological perspective positing that it is effectively and meaningfully used by non-human organisms and, more specifically, by plants. We set out to draw parallels between some aspects characterizing human language and the chemical communication that occurs between plants. The essay examines the similarities in ways of communicating linked to three properties of language: its combinatorial structure, meaning-making activities and the existence of dialects. In accordance with the findings of researchers who have demonstrated that plants do indeed communicate with one another and with organisms in their environment, the essay concludes with the appeal for an interdisciplinary approach conceptualizing a broader ecological definition of language and a constructive dialogue between the biological sciences and the humanities.

Sowing the seeds of intentionality: Motor intentions in plants.

Motor intention/intentionality has been investigated from a wide variety of perspectives: some researchers have, for example, been focusing on the purely physical and mechanical aspects underlying the control of action, while others have been concentrating on subjective intentionality. Basically, all approaches ranging from the neuroscientific to phenomenological-inspired ones have been used to investigate motor intentions. The current study set out to examine motor intentions in connection to plant behavior utilizing the final goal of plant action as the definition of its motor intention. Taking a wide-angle approach, the first part of the review is dedicated to examining philosophical and psychological studies on motor intentions. Recent data demonstrating that plant behavior does indeed seem goal-directed will then be reviewed as we ponder the possibility of purposeful or intentional plant responses to stimuli and stress conditions in their environment. The article will draw to a close as we examine current theories attempting to explain plants' overt behavior and corresponding covert representations.

The coding of object thickness in plants: When roots matter.

Tendrils are clasping structures used by climbing plants to anchor and support their vines that coil around suitable hosts to achieve the greatest exposure to sunlight. Although recent evidence suggests that climbing plants are able to sense the presence of a potential stimulus in the environment and to plan the tendrils' movements depending on properties such as its thickness, the mechanisms underlying thickness sensing in climbing plants have yet to be uncovered. The current research set out to use three-dimensional kinematical analysis to investigate if and in what way the root system contributed to thickness sensing. Experiment 1 was designed to confirm that the movement of the tendrils of pea plants (Pisum sativum L.) is planned and controlled on the basis of stimulus thickness when the stimulus is inserted into the substrate. Experiment 2 was designed to investigate what happens when the stimulus is lifted to the ground so as to impede the root system from sensing it. The results confirmed that tendrils' kinematics depend on thickness when the stimulus is available to the root system but not when it is unavailable to it. These findings suggest that the root system plays a pivotal role in sensing the presence and the thickness of a stimulus and that the information perceived affects the planning and the execution of the climbing plants' reach-to-grasp movements. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Can Plants Move Like Animals? A Three-Dimensional Stereovision Analysis of Movement in Plants.

In this article we adapt a methodology customarily used to investigate movement in animals to study the movement of plants. The targeted movement is circumnutation, a helical organ movement widespread among plants. It is variable due to a different magnitude of the trajectory (amplitude) exhibited by the organ tip, duration of one cycle (period), circular, elliptical, pendulum-like or irregular shape and the clockwise and counterclockwise direction of rotation. The acquisition setup consists of two cameras used to obtain a stereoscopic vision for each plant. Cameras switch to infrared recording mode for low light level conditions, allowing continuous motion acquisition during the night. A dedicated software enables semi-automatic tracking of key points of the plant and reconstructs the 3D trajectory of each point along the whole movement. Three-dimensional trajectories for different points undergo a specific processing to compute those features suitable to describe circumnutation (e.g., maximum speed, circumnutation center, circumnutation length, etc.). By applying our method to the approach-to-grasp movement exhibited by climbing plants (Pisum sativum L.) it appears clear that the plants scale movement kinematics according to the features of the support in ways that are adaptive, flexible, anticipatory and goal-directed, reminiscent of how animals would act.

On-line control of movement in plants.

At first glance, plants seem relatively immobile and, unlike animals, unable to interact with the surroundings or escape stressful environments. But, although markedly different from those of animals, movement pervades all aspects of plant behaviour. Here, we focused our investigation on the approaching movement of climbing plants, that is the movement they perform to reach-to-climb a support. In particular, we examined whether climbing plants evolved a motor accuracy mechanism as to improve the precision of their movement and how this eventually differs from animal species. For this purpose, by means of three-dimensional kinematical analysis, we investigated whether climbing plants have the ability to correct online their movement by means of secondary submovements, and if their frequency production is influenced by the difficulty of the task. Results showed, not only that plants correct their movement in flight, but also that they strategically increase the production of secondary submovements when the task requires more precision, exactly as humans do. These findings support the hypothesis that the movement of plants is far cry from being a simple cause-effect mechanism, but rather is appropriately planned, controlled and eventually corrected.

Speed-accuracy trade-off in plants.

Speed-accuracy trade-off (SAT) is the tendency for decision speed to covary with decision accuracy. SAT is an inescapable property of aimed movements being present in a wide range of species, from insects to primates. An aspect that remains unsolved is whether SAT extends to plants' movement. Here, we tested this possibility by examining the swaying in circles of the tips of shoots exhibited by climbing plants (Pisum sativum L.) as they approach to grasp a potential support. In particular, by means of three-dimensional kinematical analysis, we investigated whether climbing plants scale movement velocity as a function of the difficulty to coil a support. Results showed that plants are able to process the properties of the support before contact and, similarly to animal species, strategically modulate movement velocity according to task difficulty.