Sensorimotor Adaptation, Including SMS
Sensorimotor adaptation refers to the capacity of the central nervous system to gradually update motor control to compensate for changes in sensory inputs from the environment or for changes in mechanical characteristics of the body. One example is learning to accommodate to the refraction of light in water when reaching for objects viewed through a diving mask. In the microgravity environment, somatosensory and vestibular inputs are quite different than they are on Earth. The body is unloaded, resulting in greater movement per unit of force. Moreover, on Earth the otoliths of the vestibular system signal angle of orientation of the head relative to a gravitational vector, which is absent in space. There is a resulting reinterpretation of head tilt as a linear acceleration which leads to motor control and perceptual disruptions on return to Earth. It is perhaps not surprising then that crewmembers report a high incidence of space motion sickness due to sensory conflict. In addition, once individuals adapt movement control for the microgravity environment, these new control processes and strategies are maladaptive for Earth’s gravitational field. Therefore, there is a period of readaptation of sensorimotor control upon return to Earth which can last for days to weeks depending upon the preceding flight duration.
The topic of human spaceflight conjures images of crewmembers gracefully floating and somersaulting through a capsule. Most people do not stop to consider the substantial challenges that moving through this unique environment provide to the central nervous system. The motor commands that have efficiently and effectively moved the body throughout one’s lifetime in Earth’s gravitational environment are no longer appropriate and must be modified through sensorimotor adaptation.
The vestibular system, which contributes to the sense of balance, is a small structure found within the inner ear (Young 1984). One portion, the semicircular canals, detects angular acceleration of the head by fluid flowing within the canals. The other portion, the otoliths, signals angle of tilt of the head relative to gravity and linear acceleration of the head via movement of small calcium carbonate stones placed over hair cell receptors. In microgravity, the otoliths can only detect linear acceleration due to the absence of a gravitational reference vector. The central nervous system can adapt to this relatively quickly inflight over a period of a few days, but then sensorimotor control is maladaptive upon return to Earth (cf. Clement et al. 2005). The proprioceptive system also exhibits adaptive change in microgravity as well. Together the modified sensory signals result in difficulties with spatial orientation and a number of illusions including self or surround motion and difficulty with identifying a subjective vertical. Furthermore, crewmembers report a number of postural disturbances and illusions upon return from spaceflight, with readaptation from short-duration flights (i.e., shuttle) occurring within a number of days and from longer-duration flights (i.e., ISS) within weeks.
It is becoming increasingly clear that postflight performance disturbances do not simply arise from declines in muscle strength and cardiovascular fitness that occur in microgravity. In fact, current exercise protocols followed by astronauts on the ISS are quite effective at staving off these declines. Despite this, the crews still experience difficulties with eye-hand coordination, spatial and geographic orientation perception, mobility, and balance postflight and also have reduced dynamic visual acuity (cf. Paloski et al. 2008; Reschke et al. 2015; Bloomberg and Mulavara 2003). Dynamic visual acuity is particularly affected postflight, which is the ability to read while walking or undergoing some other displacement to the body such as in a moving vehicle. This seemingly simple behavior requires the coordinated orchestration of not only eye and head movements but also between the movements of body segments to keep the gaze focused on a target despite the vertical and lateral displacements induced by locomotion. Spaceflight causes a reorganization of this full-body gaze control system. Extensive research has revealed that body load-sensing somatosensory input centrally modulates vestibular input and can also adaptively modify vestibularly mediated head-movement control during locomotion. Spaceflight can thus cause a central adaptation of the converging vestibular system and the body load-sensing somatosensory system (Young et al. 1985). Additional postflight sensorimotor changes include alterations in jump-landing strategies and increased time to complete functional tasks.
Investigations of postural control under varying conditions of vision, proprioception, and vestibular inputs have further elucidated sensorimotor adaptation to spaceflight. Crewmembers were tested on their ability to maintain balance control while standing on a platform under varying conditions of balance challenge and sensory inputs: (1) eyes open and stable surface, (2) eyes closed and stable surface, (3) eyes open with visual surround sway referenced (e.g., as the participant sways forward so does the surrounding display, eliminating visual flow cues of motion), (4) eyes open with support surface sway referenced (e.g., as the participant sways forward the support surface tilts forward, eliminating ankle proprioceptive cues of motion), (5) eyes closed with support surface sway referenced, and (6) eyes open with both visual surround and support surface sway referenced. Interestingly, these tests have revealed that postflight deficits are largest in the conditions relying more heavily on vestibular inputs (reviewed in Clément et al. 2005). Modifying the test to have crewmembers make pitch head movements under condition 6 makes it particularly sensitive to postflight postural impairments. While these declines in sensorimotor coordination and posture control dissipate as one readapts to Earth’s gravitational field over days and weeks, they are considered a risk for remote space exploration as they would impede emergency egress and exploration activities for several days until the crew adapts to the new gravitational environment of Mars or some other body.
In addition to effects on whole-body locomotion and posture control, microgravity also impedes manual control and reaching movements, actions which are relied upon for functional and operational performance (Paloski et al. 2008). For example, studies have shown that the ability to simultaneously perform a manual control task and a cognitive task is decreased during spaceflight. It has been suggested that both stress and scarcity of resources required for sensorimotor adaptation may be responsible for these deficits during spaceflight. Critically, these declines do not show recovery inflight even after a period of 6 months, elevating the potential risk of errors for mission critical performance. Another factor affecting the ability of crewmembers to visually fixate on targets during head movements is disruption of the vestibulo-ocular reflex (Reschke et al. 2015). This reflex response results in eye movements in the direction opposing head movements, allowing one to maintain gaze steady on a target. The vestibulo-ocular reflex experiences inflight adaptive recalibration leading to gaze instability when crewmembers are returning to Earth’s gravitational field after a period in space.
Ground-based experiments of the sensorimotor adaptation process have identified two underlying components: one is a cognitive strategic process that results in faster behavior changes, and the other is a slower, more gradual, adaptive recalibration (cf. Seidler et al. 2013). While the latter occurs more slowly, the acquired adaptive state is persistent, resulting in prolonged readaptation such as observed with return from spaceflight. The initial trigger for adaptation is a mismatch between the expected sensory consequences of a movement and the actual outcome. Imagine reaching for a target while wearing prism lenses which shift the visual world to one side; one will reach to the side of a target when first pointing. Across trials, individuals can adapt to the new relationship between visual inputs and motor outputs, progressively reducing reach errors. Once the lenses are removed, after effects of the adaptation are observed as one reaches to the other side of the target for the first several trials, automatically using the new updated state. Importantly, after spaceflight these same adaptive motor control processes are exhibited, which may be leveraged for the design of countermeasures to realize faster readaptation to Earth’s gravitational environment.
Large individual differences are observed in the rate of adaptation, both in ground-based experiments of sensorimotor adaptation and in measures of postflight postural recovery curves. Predictors of adaptability have been identified in ground-based experiments, including spatial working memory capacity, visual dependence, and genotype for genetic polymorphisms that play a role in dopaminergic processing (Seidler et al. 2015). This raises the intriguing possibility that one may be able to predict in advance which individuals adapt more slowly to the sensory conflict of spaceflight; they could then be provided with additional sensorimotor adaptability training prior to flight. This remains an open area of research.
We still do not have a full understanding of the neurocognitive mechanisms underlying sensorimotor adaptation. Continued work in this domain has importance not only for being able to mitigate the untoward effects of spaceflight; numerous health conditions alter sensory inputs and require the central nervous system to adapt to noisy, unreliable signals including the peripheral neuropathy that can accompany diabetes and vestibular impairments that occur with aging, Meniere’s disease, inner ear infections, and other causes.
Space Motion Sickness
The vestibular system not only has sensorimotor functions but also plays a role in autonomic regulation (cf. Balaban 1999). A relatively high proportion of crewmembers experience space motion sickness, with some estimates at 75% incidence. Motion sickness is one of the most significant operational challenges experienced by spaceflight crews during the initial transition periods from Earth’s 1G to microgravity (Ortega and Harm 2008). Motion sickness appeared and was most consistently reported during human spaceflight missions with larger crew compartments during the Apollo space program in which crewmembers could be free-floating. The severity of space motion sickness stems from the “sopite syndrome” long after the more familiar features of nausea and pallor have abated; it includes chronic drowsiness, fatigue, mood, and personality changes and lack of initiative (Lackner and DiZio 2006). Based on a comprehensive literature review, Lackner and DiZio (2006) concluded that space motion sickness is not, in fact, a separable diagnosis but is rather an instance of what many experience as motion sickness under a variety of environments. Space motion sickness symptoms are evident within the first few minutes after insertion into weightlessness; recovery occurs within 96 h, but symptoms can reoccur up to 14 days into flight (Ortega and Harm 2008). Development of motion sickness symptoms during the early hours after insertion into microgravity has affected the schedule of mission critical operational activities; for example, extravehicular activity is typically delayed until day 3. Thirty-five to 60% of US and Russian crewmembers have had space motion sickness, with a higher incidence in first-time versus more experienced shuttle fliers. Motion sickness symptoms also occur upon return to Earth 1G, at the same levels of prevalence in the US and Russian space programs: 27% after short-duration missions and 92% in long-duration missions. Here, the symptom severity correlates with time spent in microgravity (Ortega and Harm 2008), similar to what is observed with sensorimotor adaptation.
The etiology and neural mechanisms of motion sickness remain unclear (Oman 1988; Oman and Cullen 2014). The vestibular system plays a critical role in space motion sickness because its incidence has been associated with active head movements (Oman 1990), and motion sickness is either absent or ameliorated after loss of vestibular function (Money 1970). Visual orientation illusions that astronauts feel throughout their missions also play a role in the etiology of space motion sickness (reviewed in Oman 1988). Thus a combination of both head movement vestibular stimulation and visual reorientation episodes can cause space motion sickness-related nausogenic effects once symptom threshold has been reached.
A currently accepted mechanism of space motion sickness is the sensory conflict hypothesis, recently reviewed and elaborated upon by Oman and Cullen (2014). This hypothesis, at its roots, depends upon the same mismatch of actual and predicted sensory consequences of action that was described above as contributing to spaceflight sensorimotor adaptation. Substantial evidence supports the idea of reafference suppression during self-generated motion. That is, when motor commands are generated to produce a movement, an efferent copy is created and used to estimate the sensory consequences of movement. This allows for comparison of reafferent signals (sensory information resulting from movement) with the desired state, leading to error detection when a mismatch occurs. Reafferent suppression allows individuals to perform movements without interference from incoming sensory signals when a movement is proceeding as desired. When the body is moved passively, for example, when one is standing on a ship, an efferent copy is not created, and reafferent suppression does not occur. The incoming sensory information is important for stabilizing the body, but the resulting sensory conflicts that occur can also lead to motion sickness.
Recent evidence supports a role for vestibular processing neurons in the brainstem leading to motion sickness (reviewed in Oman and Cullen 2014). These neurons have been characterized with compelling evidence for reafference cancelation as the “vestibular only” (VO) neurons in the vestibular nuclei. These VO neurons respond to yaw rotation stimulation of the semicircular canals and also to tilt and translation stimulation. Cullen and her colleagues have shown that the cancelation of the afferent component created by self-generated movement in the response of the VO neuron is not simply a gating response by a motor command neuron but is an actual subtractive cancelation by a central nervous system predicted signal. In new gravitational environments, especially in microgravity when the central nervous system is updating its internal models of sensorimotor predictions, larger error signals would be generated exceeding the threshold of emetic centers and resulting in motion sickness symptoms. A deeper understanding of the neurophysiological mechanisms of motion sickness may lead to new treatments, both for crewmembers and for those on Earth that experience similar symptoms.
Microgravity has clear effects on our sensory systems and multisensory integration, perhaps not surprising given that we have evolved to move in Earth’s gravitational environment. The central nervous system is highly plastic, allowing crewmembers to adapt their motor control to microgravity within a period of several days. This process can be difficult, however, and functionality is disrupted during this transition period. Upon return to Earth, crewmembers must consequently readapt their movements for this environment, a process that interferes with rapid and accurate sensorimotor behaviors for days to weeks. As outlined in this series, a number of features of spaceflight in addition to microgravity affect the central nervous system, including radiation exposure and sleep loss. The interactive effects of the multicomponent spaceflight environment on neurocognitive and sensorimotor functions remain to be studied.
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