Gravitropism: The LAZY way of intracellular hitchhiking.

Plant gravitropism has fascinated scientists for centuries. A new study provides a major mechanistic update of the so-called starch/statolith hypothesis, revealing how gravity perception is converted into a physiological response.

Understanding the role of starch sheath layer in graviception of Alternanthera philoxeroides: a biophysical and microscopical study.

Plants' ability to sense and respond to gravity is a unique and fundamental process. When a plant organ is tilted, it adjusts its growth orientation relative to gravity direction, which is achieved by a curvature of the organ. In higher, multicellular plants, it is thought that the relative directional change of gravity is detected by starch-filled organelles that occur inside specialized cells called statocytes, and this is followed by signal conversion from physical information to physiological information within the statocytes. The classic starch statolith hypothesis, i.e., the starch accumulating amyloplasts movement along the gravity vector within gravity-sensing cells (statocytes) is the probable trigger of subsequent intracellular signaling, is widely accepted. Acharya Jagadish Chandra Bose through his pioneering research had investigated whether the fundamental reaction of geocurvature is contractile or expansive and whether the geo-sensing cells are diffusedly distributed in the organ or are present in the form of a definite layer. In this backdrop, a microscopy based experimental study was undertaken to understand the distribution pattern of the gravisensing layer, along the length (node-node) of the model plant Alternanthera philoxeroides and to study the microrheological property of the mobile starch-filled statocytes following inclination-induced graviception in the stem of the model plant. The study indicated a prominent difference in the pattern of distribution of the gravisensing layer along the length of the model plant. The study also indicated that upon changing the orientation of the plant from vertical position to horizontal position there was a characteristic change in orientation of the mobile starch granules within the statocytes. In the present study for the analysis of the microscopic images of the stem tissue cross sections, a specialized and modified microscopic illumination setup was developed in the laboratory in order to enhance the resolution and contrast of the starch granules.

Motor imagery helps updating internal models during microgravity exposure.

Skilled movements result from a mixture of feedforward and feedback mechanisms conceptualized by internal models. These mechanisms subserve both motor execution and motor imagery. Current research suggests that imagery allows updating feedforward mechanisms, leading to better performance in familiar contexts. Does this still hold in radically new contexts? Here, we test this ability by asking participants to imagine swinging arm movements around shoulder in normal gravity condition and in microgravity in which studies showed that movements slow down. We timed several cycles of actual and imagined arm pendular movements in three groups of subjects during parabolic flight campaign. The first, control, group remained on the ground. The second group was exposed to microgravity but did not imagine movements inflight. The third group was exposed to microgravity and imagined movements inflight. All groups performed and imagined the movements before and after the flight. We predicted that a mere exposure to microgravity would induce changes in imagined movement duration. We found this held true for the group who imagined the movements, suggesting an update of internal representations of gravity. However, we did not find a similar effect in the group exposed to microgravity despite the fact that the participants lived the same gravitational variations as the first group. Overall, these results suggest that motor imagery contributes to update internal representations of the considered movement in unfamiliar environments, while a mere exposure proved to be insufficient.NEW & NOTEWORTHY Gravity strongly affects the way movements are performed. How internal models process this information to adapt behavior to novel contexts is still unknown. The microgravity environment itself does not provide enough information to optimally adjust the period of natural arm swinging movements to microgravity. However, motor imagery of the task while immersed in microgravity was sufficient to update internal models. These results show that actually executing a task is not necessary to update graviception.

Effects of motion paradigm on human perception of tilt and translation.

The effect of varying sinusoidal linear acceleration on perception of human motion was examined using 4 motion paradigms: off-vertical axis rotation, variable radius centrifugation, linear lateral translation, and rotation about an earth-horizontal axis. The motion profiles for each paradigm included 6 frequencies (0.01-0.6 Hz) and 5 tilt amplitudes (5°-20°). Subjects verbally reported the perceived angle of their whole-body tilt and the peak-to-peak translation of their head in space and used a joystick capable of recording 2-axis motion in the sagittal and transversal planes to indicate the phase between the perceived and actual motions. The amplitudes of perceived tilt and translation were expressed in terms of gain, i.e., the ratio of perceived tilt to equivalent tilt angle, and the ratio of perceived translation to equivalent linear displacement. Tilt perception gain decreased, whereas translation perception gain increased, with increasing frequency. During off-vertical axis rotation, the phase of tilt perception and of translation perception did not vary across stimulus frequencies. These motion paradigms elicited similar responses in roll tilt and interaural perception of translation, with differences likely due to the influence of naso-occipital linear accelerations and input to the semicircular canals that varied across motion paradigms.

Mechanosensation Mediates Long-Range Spatial Decision-Making in an Aneural Organism.

The unicellular protist Physarum polycephalum is an important emerging model for understanding how aneural organisms process information toward adaptive behavior. Here, it is revealed that Physarum can use mechanosensation to reliably make decisions about distant objects in its environment, preferentially growing in the direction of heavier, substrate-deforming, but chemically inert masses. This long-range sensing is abolished by gentle rhythmic mechanical disruption, changing substrate stiffness, or the addition of an inhibitor of mechanosensitive transient receptor potential channels. Additionally, it is demonstrated that Physarum does not respond to the absolute magnitude of strain. Computational modeling reveales that Physarum may perform this calculation by sensing the fraction of its perimeter that is distorted above a threshold substrate strain-a fundamentally novel method of mechanosensation. Using its body as both a distributed sensor array and computational substrate, this aneural organism leverages its unique morphology to make long-range decisions. Together, these data identify a surprising behavioral preference relying on biomechanical features and quantitatively characterize how the Physarum exploits physics to adaptively regulate its growth and shape.

Actual and Imagined Movements Reveal a Dual Role of the Insular Cortex for Motor Control.

Movements rely on a mixture of feedforward and feedback mechanisms. With experience, the brain builds internal representations of actions in different contexts. Many factors are taken into account in this process among which is the immutable presence of gravity. Any displacement of a massive body in the gravitational field generates forces and torques that must be predicted and compensated by appropriate motor commands. The insular cortex is a key brain area for graviception. However, no attempt has been made to address whether the same internal representation of gravity is shared between feedforward and feedback mechanisms. Here, participants either mentally simulated (only feedforward) or performed (feedforward and feedback) vertical movements of the hand. We found that the posterior part of the insular cortex was engaged when feedback was processed. The anterior insula, however, was activated only in mental simulation of the action. A psychophysical experiment demonstrates participants' ability to integrate the effects of gravity. Our results point toward a dual internal representation of gravity within the insula. We discuss the conceptual link between these two dualities.

Flying dreams stimulated by an immersive virtual reality task.

Despite a high prevalence and broad interest in flying dreams, these exceptional experiences remain infrequent. Our study aimed to (1) induce flying dreams using a custom-built virtual reality (VR) flying task, (2) examine their phenomenological correlates and (3) investigate their relations to participant state and trait factors. 137 participants underwent VR-flying followed by a morning nap. They also completed home dream journals for 5 days before and 10 days after the VR exposure. VR-flying successfully increased the reporting of flying dreams during the laboratory nap and on the following morning compared to both baseline frequencies and a control cohort. Flying dreams were also changed qualitatively, exhibiting higher levels of Lucid-control and emotional intensity, after VR exposure. Factors such as prior dream-flying experiences and level of VR sensory immersion modulated flying dream induction. Findings are consistent with a new vection-based explanation of dream-flying and may facilitate development of dream flight-induction technologies.

Spatial Updating Depends on Gravity.

As we move through an environment the positions of surrounding objects relative to our body constantly change. Maintaining orientation requires spatial updating, the continuous monitoring of self-motion cues to update external locations. This ability critically depends on the integration of visual, proprioceptive, kinesthetic, and vestibular information. During weightlessness gravity no longer acts as an essential reference, creating a discrepancy between vestibular, visual and sensorimotor signals. Here, we explore the effects of repeated bouts of microgravity and hypergravity on spatial updating performance during parabolic flight. Ten healthy participants (four women, six men) took part in a parabolic flight campaign that comprised a total of 31 parabolas. Each parabola created about 20-25 s of 0 g, preceded and followed by about 20 s of hypergravity (1.8 g). Participants performed a visual-spatial updating task in seated position during 15 parabolas. The task included two updating conditions simulating virtual forward movements of different lengths (short and long), and a static condition with no movement that served as a control condition. Two trials were performed during each phase of the parabola, i.e., at 1 g before the start of the parabola, at 1.8 g during the acceleration phase of the parabola, and during 0 g. Our data demonstrate that 0 g and 1.8 g impaired pointing performance for long updating trials as indicated by increased variability of pointing errors compared to 1 g. In contrast, we found no support for any changes for short updating and static conditions, suggesting that a certain degree of task complexity is required to affect pointing errors. These findings are important for operational requirements during spaceflight because spatial updating is pivotal for navigation when vision is poor or unreliable and objects go out of sight, for example during extravehicular activities in space or the exploration of unfamiliar environments. Future studies should compare the effects on spatial updating during seated and free-floating conditions, and determine at which g-threshold decrements in spatial updating performance emerge.

The gravitational imprint on sensorimotor planning and control.

Humans excel at learning complex tasks, and elite performers such as musicians or athletes develop motor skills that defy biomechanical constraints. All actions require the movement of massive bodies. Of particular interest in the process of sensorimotor learning and control is the impact of gravitational forces on the body. Indeed, efficient control and accurate internal representations of the body configuration in space depend on our ability to feel and anticipate the action of gravity. Here we review studies on perception and sensorimotor control in both normal and altered gravity. Behavioral and modeling studies together suggested that the nervous system develops efficient strategies to take advantage of gravitational forces across a wide variety of tasks. However, when the body was exposed to altered gravity, the rate and amount of adaptation exhibited substantial variation from one experiment to another and sometimes led to partial adjustment only. Overall, these results support the hypothesis that the brain uses a multimodal and flexible representation of the effect of gravity on our body and movements. Future work is necessary to better characterize the nature of this internal representation and the extent to which it can adapt to novel contexts.

Characteristics and Prevalence of Gravitational Insecurity in Children with Sensory Processing Dysfunction.

BACKGROUND: Children with sensory processing challenges often demonstrate a specific vestibular dysfunction characterized by an irrational fear of movement experiences referred to as gravitational insecurity. PROCEDURES/OUTCOMES: This descriptive, exploratory study of existing de-identified data examined characteristics and prevalence of symptoms indicative of gravitational insecurity and the relationship among gravitational insecurity, gender, age, and other types of sensory-motor problems in 689 children, aged 4-12 years, with Sensory Processing Disorder (SPD) and related parent-reported co-morbid diagnoses of Attention Deficit-Hyperactivity Disorder, Anxiety Disorder, Learning Disabilities and Autism Spectrum Disorder. Gravitational insecurity was identified by the sum of eight items on a parent-report clinical questionnaire of sensory processing and motor skills in children. RESULTS/CONCLUSIONS: The number and patterns of gravitational insecurity symptoms were not significantly different across age, gender or comorbid diagnoses. Prevalence of symptoms of gravitational insecurity in a clinical population of children with SPD was 15 - 21%. Cluster analysis found two groups with and without gravitational insecurity. In the gravitational insecurity group all eight items examined occurred "sometimes/often" and four or more symptoms were reported by individuals in this group. IMPLICATIONS: Gravitational insecurity is an important vestibular-based dysfunction to identify and treat in children with SPD. Future studies should examine the relationship between these symptoms and objective measures of gravitational insecurity.

Role of somatosensory and/or vestibular sensory information in subjective postural vertical in healthy adults.

The body's subjective postural vertical (SPV) has been thought to be affected by somatosensory information. How the SPV is perceived based on what types of somatosensory information has not been determined experimentally by manipulating somatosensory conditions. We investigated the effects of disturbing the somatosensory information from a seat pad and/or vestibular sensory information on the SPV in 15 healthy adults. Their SPV values were measured under four conditions (control, somatosensory, vestibular, and somatosensory + vestibular) in random order. The average and absolute SPV values were measured. In the somatosensory condition, a foam rubber pad was placed on the seating surface and the subject's SPV was measured. In the vestibular condition, the SPV was measured during galvanic vestibular stimulation (GVS). The somatosensory + vestibular condition was used to measure the SPV during combined somatosensory and vestibular stimulation. The mean SPV value was significantly increased in the somatosensory + vestibular condition compared to the other three conditions. The absolute value of SPV was significantly increased in the somatosensory and somatosensory + vestibular conditions compared to the control and vestibular conditions. There was no significant difference in the average or absolute SPV values in the vestibular condition compared to the other conditions. There was no significant difference between SPV errors when somatosensory information was disturbed or when somatosensory + vestibular information was disturbed. When the somatosensory information from the seat was disturbed, the SPV error increased, and it also shifted under the influence of the vestibular sensory information modulation. These results indicate that somatosensory information from the seat plays an important role in SPV in healthy adults.

Free Energy Principle in Human Postural Control System: Skin Stretch Feedback Reduces the Entropy.

Human upright standing involves an integration of multiple sensory inputs such as vision, vestibular and somatosensory systems. It has been known that sensory deficits worsen the standing balance. However, how the modulation of sensory information contributes to postural stabilization still remains an open question for researchers. The purpose of this work was to formulate the human standing postural control system in the framework of the free-energy principle, and to investigate the efficacy of the skin stretch feedback in enhancing the human standing balance. Previously, we have shown that sensory augmentation by skin stretch feedback at the fingertip could modulate the standing balance of the people with simulated sensory deficits. In this study, subjects underwent ten 30-second trials of quiet standing balance with and without skin stretch feedback. Visual and vestibular sensory deficits were simulated by having each subject close their eyes and tilt their head back. We found that sensory augmentation by velocity-based skin stretch feedback at the fingertip reduced the entropy of the standing postural sway of the people with simulated sensory deficits. This result aligns with the framework of the free energy principle which states that a self-organizing biological system at its equilibrium state tries to minimize its free energy either by updating the internal state or by correcting body movement with appropriate actions. The velocity-based skin stretch feedback at the fingertip may increase the signal-to-noise ratio of the sensory signals, which in turn enhances the accuracy of the internal states in the central nervous system. With more accurate internal states, the human postural control system can further adjust the standing posture to minimize the entropy, and thus the free energy.

The people behind the papers - Qiang Zhu, Marçal Gallemí and Eva Benková.

The apical hook is a transient structure that functions to protect the vulnerable apical meristem from damage when the seedling penetrates the soil. Although some of the molecular players regulating its development have been identified, many aspects have remained opaque, including how an early auxin asymmetry in the hypocotyl is established. A paper in Development now provides a link between hormone signalling and the gravitropic response of the seedling's growing root in apical hook development. We caught up with co-first authors Qiang Zhu and Marçal Gallemí and their supervisor Eva Benková, Professor at the Institute of Science and Technology Austria in Klosterneuberg, to find out more about the project.

Root gravity response module guides differential growth determining both root bending and apical hook formation in Arabidopsis.

The apical hook is a transiently formed structure that plays a protective role when the germinating seedling penetrates through the soil towards the surface. Crucial for proper bending is the local auxin maxima, which defines the concave (inner) side of the hook curvature. As no sign of asymmetric auxin distribution has been reported in embryonic hypocotyls prior to hook formation, the question of how auxin asymmetry is established in the early phases of seedling germination remains largely unanswered. Here, we analyzed the auxin distribution and expression of PIN auxin efflux carriers from early phases of germination, and show that bending of the root in response to gravity is the crucial initial cue that governs the hypocotyl bending required for apical hook formation. Importantly, polar auxin transport machinery is established gradually after germination starts as a result of tight root-hypocotyl interaction and a proper balance between abscisic acid and gibberellins.This article has an associated 'The people behind the papers' interview.

Behavioral and molecular markers of death in Drosophila melanogaster.

Fly movement was tracked through 3-dimensional (3D) space as the fly died, using either reflected visible light, reflected infrared (IR) light, or fly GFP fluorescence. Behaviors measured included centrophobism, negative geotaxis, velocity, and total activity. In addition, frequency of directional heading changes (FDHC) was calculated as a measure of erratic movement. Nine middle-aged flies were tracked as they died during normal aging, and fifteen young flies were tracked as they died from dehydration/starvation stress. Episodes of increased FDHC were observed 0-8 h prior to death for the majority of the flies. FDHC was also increased with age in flies with neuronal expression of a human Abeta42 protein fragment associated with Alzheimer's disease. Finally, green autofluorescence appeared in the eye and body immediately prior to and coincident with death, and fluorescence of GFP targeted to the retina increased immediately prior to and coincident with death. The results suggest the potential utility of FDHC, green autofluorescence, and retinal GFP as markers of neuronal malfunction and imminent death.

Time course of the subjective visual vertical during sustained optokinetic and galvanic vestibular stimulation.

The brain is thought to use rotation cues from both the vestibular and optokinetic system to disambiguate the gravito-inertial force, as measured by the otoliths, into components of linear acceleration and gravity direction relative to the head. Hence, when the head is stationary and upright, an erroneous percept of tilt arises during optokinetic roll stimulation (OKS) or when an artificial canal-like signal is delivered by means of galvanic vestibular stimulation (GVS). It is still unknown how this percept is affected by the combined presence of both cues or how it develops over time. Here, we measured the time course of the subjective visual vertical (SVV), as a proxy of perceived head tilt, in human participants (n = 16) exposed to constant-current GVS (1 and 2 mA, cathodal and anodal) and constant-velocity OKS (30°/s clockwise and counterclockwise) or their combination. In each trial, participants continuously adjusted the orientation of a visual line, which drifted randomly, to Earth vertical. We found that both GVS and OKS evoke an exponential time course of the SVV. These time courses have different amplitudes and different time constants, 4 and 7 s respectively, and combine linearly when the two stimulations are presented together. We discuss these results in the framework of observer theory and Bayesian state estimation.NEW & NOTEWORTHY While it is known that both roll optokinetic stimuli and galvanic vestibular stimulation affect the percept of vertical, how their effects combine and develop over time is still unclear. Here we show that both effects combined linearly but are characterized by different time constants, which we discuss from a probabilistic perspective.

Computational neurology of gravity perception involving semicircular canal dysfunction in unilateral vestibular lesions.

Unilateral peripheral vestibular lesions not only lead to vertigo, nystagmus and imbalance, but also to a bias in the perception of verticality, which can be measured as tilt of the subjective visual vertical (SVV). Previously, this tilt has been assumed to be caused by a residual otolith bias, for example, because unequal numbers of active haircells on both sides of the utricular striola might result in an imbalance of the firing rates of central otolith neurons. Here we propose that a tilt of the subjective visual vertical might as well be caused by a vertical semicircular canal bias in the roll axis after unilateral peripheral lesions. The canal bias, acting similar to angular velocity stimuli, influences the SVV via the central gravity estimator, which under normal circumstances resolves a perceptual tilt-translation ambiguity. To illustrate our hypothesis, we compare model predictions to data on SVV measurements in patients with unilateral vestibular lesions while being tilted or being rotated eccentrically. We further embed the model of peripheral processing in a neural network that implements the idiotropic bias and represents the direction of gravity as population code in a three dimensional spherical topography.

Angular vestibuloocular reflex responses in Otop1 mice. I. Otolith sensor input is essential for gravity context-specific adaptation.

The role of the otoliths in mammals in the angular vestibuloocular reflex (VOR) has been difficult to determine because there is no surgical technique that can reliably ablate them without damaging the semicircular canals. The Otopetrin1 (Otop1) mouse lacks functioning otoliths because of failure to develop otoconia but seems to have otherwise normal peripheral anatomy and neural circuitry. By using these animals we sought to determine the role of the otoliths in angular VOR baseline function and adaptation. In six Otop1 mice and six control littermates we measured baseline ocular countertilt about the three primary axes in head coordinates; baseline horizontal (rotation about an Earth-vertical axis parallel to the dorsal-ventral axis) and vertical (rotation about an Earth-vertical axis parallel to the interaural axis) sinusoidal (0.2-10 Hz, 20-100°/s) VOR gain (= eye/head velocity); and the horizontal and vertical VOR after gain-increase (1.5×) and gain-decrease (0.5×) adaptation training. Countertilt responses were significantly reduced in Otop1 mice. Baseline horizontal and vertical VOR gains were similar between mouse types, and so was horizontal VOR adaptation. For control mice, vertical VOR adaptation was evident when the testing context, left ear down (LED) or right ear down (RED), was the same as the training context (LED or RED). For Otop1 mice, VOR adaptation was evident regardless of context. Our results suggest that the otolith translational signal does not contribute to the baseline angular VOR, probably because the mouse VOR is highly compensatory, and does not alter the magnitude of adaptation. However, we show that the otoliths are important for gravity context-specific angular VOR adaptation. NEW & NOTEWORTHY This is the first study examining the role of the otoliths (defined here as the utricle and saccule) in adaptation of the angular vestibuloocular reflex (VOR) in an animal model in which the otoliths are reliably inactivated and the semicircular canals preserved. We show that they do not contribute to adaptation of the normal angular VOR. However, the otoliths provide the main cue for gravity context-specific VOR adaptation.

Test-retest reliability of and age-related changes in the subjective postural vertical on the diagonal plane in healthy subjects.

The subjective postural vertical (SPV) reflects gravity perception when the eyes are closed. Changes in the SPV on both the frontal and sagittal planes occur in response to neurological disorders and aging; however, these changes on the diagonal plane are unclear. Here we examined test-retest reliability (n=16) of and age-related changes (n=38) in the SPV on the diagonal plane. Subjects sat on an electrical vertical board (EVB), which was used to measure the SPV on the diagonal plane. An experimenter controlled and moved the EVB seat at a constant speed on the diagonal plane and measured the seat's tilt using a digital inclinometer when subjects verbally reported that they had reached a true vertical position. Measurement was performed for eight trials, and the mean (tilt direction) and standard deviation (variability) were calculated. To determine test-retest reliability, the same experimenter repeatedly measured the SPV 1 week later. To assess age-related changes, tilt direction and variability were compared between the young (n=20) and elderly (n=18) groups. Test-retest reliability on the right and left diagonal planes was 0.61 or more. Moreover, tilt direction on the right diagonal plane - but not on the left diagonal plane - indicated a significant diagonally backward deviation in the elderly group compared with that in the young group. Variability was significantly higher in the elderly group on both planes. SPV measurement on the diagonal plane was indicated, and age-related changes were identified. Thus, future studies should assess the potential clinical applications of SPV in neurological disorders.

Gravity estimation and verticality perception.

Gravity is a defining force that governs the evolution of mechanical forms, shapes and anchors our perception of the environment, and imposes fundamental constraints on our interactions with the world. Within the animal kingdom, humans are relatively unique in having evolved a vertical, bipedal posture. Although a vertical posture confers numerous benefits, it also renders us less stable than quadrupeds, increasing susceptibility to falls. The ability to accurately and precisely estimate our orientation relative to gravity is therefore of utmost importance. Here we review sensory information and computational processes underlying gravity estimation and verticality perception. Central to gravity estimation and verticality perception is multisensory cue combination, which serves to improve the precision of perception and resolve ambiguities in sensory representations by combining information from across the visual, vestibular, and somatosensory systems. We additionally review experimental paradigms for evaluating verticality perception, and discuss how particular disorders affect the perception of upright. Together, the work reviewed here highlights the critical role of multisensory cue combination in gravity estimation, verticality perception, and creating stable gravity-centered representations of our environment.