Adaptation of gait is important in daily life, stepping up a curb, avoiding a puddle, or maneuvering trough crowded streets is something we do on a daily basis. Stroke survivors have a high falls incidence (Hyndman et al., 2002; Jorgensen et al., 2002; Lamb et al., 2003; Smith et al., 2006; Yates et al., 2002), which indicates treatments and falls prevention may be effective in reducing falls. Current treatments seem to be effective in increasing gait speeds (Dickstein, 2008), however quality and/or robustness of gait, allowing people to be safe in ADL, is not really aimed on, or assessed. The need to gain a better understanding of how to provide effective interventions to improve gait adaptability is shown in the number of recent studies assessing the feasibility of target stepping to asses and train gait adaptability (Heeren et al., 2013; K. L. Hollands et al., 2016; K. L. Hollands et al., 2015; Timmermans et al., 2016; van Ooijen et al., 2015; van Ooijen et al., 2013).
Gait adaptability has shown to be feasible for testing and training gait (Heeren et al., 2013; K. L. Hollands et al., 2016; K. L. Hollands et al., 2015; Timmermans et al., 2016; van Ooijen et al., 2015; van Ooijen et al., 2013) however, the knowledge of the factors that
reduce the ability to adapt gait in stroke survivors are limited. Two features of target stepping performance in stroke survivors have been shown to be related with clinical measures of functional recovery after stroke. Firstly, the number of targets missed by the paretic limb is associated with the Fugl-Meyer score (which indicates motor recovery); secondly, speed of target stepping can be predicted using the Berg balance scale, (a measure for balance) (K. L. Hollands et al., 2016). Furthermore, stroke survivors have shown to have greater foot
placement error when narrowing gait while they have to maintain balance in comparison to when they are stabilized by crutches (Nonnekes et al., 2010). Target stepping therefore could be indicative of how impaired balance and motor recovery would affect gait and be a
valuable measure to assess safe gait in stroke survivors.
The factors that are likely to affect foot placement control in healthy young and older adults are likely to deteriorate more in stroke survivors. The direction of adaptation is
expected to be affected as stroke survivors prefer lengthening over shortening when avoiding an obstacle (Den Otter et al., 2005), and are less accurate stepping medially than laterally (Nonnekes et al., 2010). The fact that medial stepping is more challenging than lateral, and this difference is reduced when stroke survivors are stabilized with crutches, indicates
balance affects foot placement accuracy as well (Nonnekes et al., 2010). Also, the time stroke survivors got to avoid an obstacle showed to affect how successful stroke survivors were at obstacle avoidance (van Swigchem et al., 2013). And lastly, stroke survivors are known to have executive function deficits (Ballard et al., 2003; Zinn, Bosworth, Hoenig, &
Swartzwelder, 2007). Therefore, investigating how stroke survivors are affected in their foot placement control may provide insights for treatment and training.
2.6.1 How does the direction of adaptation affect foot placement in
stroke survivors?
Stroke survivors have difficulty adjusting foot placement, part of this difficulty could lie in the motor control of the limb. Two factors due to stroke affect the motor control directly. Firstly, the hemiparesis affects the descending activation from the motor cortex to the spinal tracts, resulting in the inability to voluntarily contract or relax muscles (Arene & Hidler, 2009). Secondly, tone, which is defined as the resistance against passive movement, which is often negligible, or totally absent, during the acute phase after stroke. In the chronic phase it either stays reduced or tone can increase. Both situations severely affect the coordination of a movement, both reduced or no tone and increased tone will limit the effectiveness of the
movement, if movement is even possible. Lastly, spasticity, where tone is a constant
resistance against passive movement in a hemiparesis, spasticity appears in stretch reflexes; the resistance is dependent on the stretch speed (Arene & Hidler, 2009). If and how spasticity affects gait is still unknown, as multiple studies have shown contradicting results, either saying spasticity is affecting (McLellan, 1977; Sahrmann & Norton, 1977) or not affecting (Ada, Vattanasilp, O'Dwyer, & Crosbie, 1998; Yelnick, I, & I, 1999) gait. Many factors may affect the motor control of the foot placement. All of these factors could singularly or in combination affect, by degrees of severity, how well the planned endpoint of the foot can be reached, which could not only considerably influence how safely the current step is made, but also impact on the base of support and balance for the upcoming steps. Therefore, it is
important to study the effect of stroke on foot placement accuracy in as well the paretic and non-paretic limb, as both limbs might be affected by different factors, which might induce different limitations.
2.6.1.1 Anterior-posterior direction of adaptation in stroke survivors
From studies in healthy young and older adults we know that lengthening steps can be achieved with more accuracy than shortening steps (Hoogkamer et al., 2015), which implies shortening is harder either due to the forward momentum during walking, a shorter time to react, or the smaller base of support. In stroke survivors, no studies have investigated anterio- posterior stepping adjustments to targets; from obstacle avoidance studies it is known
however that stroke survivors are less successful at avoiding an obstacle during treadmill walking than their healthy counterparts (van Swigchem et al., 2013), and that they are more successful at using a lengthening strategy, which they use more often and with longer time to adapt, than their healthy counterparts (Den Otter et al., 2005; van Swigchem et al., 2013). This increased success and preference for the lengthening strategy in obstacle avoidance suggests that stroke survivors may be more successful in lengthening steps than shortening steps, similar to young and older adults. In addition, it might even be that the control to shorten a step is more limited in stroke survivors, slowing down the forward momentum in single stance requires foot-ankle strategies that require high forces (MacKinnon & Winter, 1993), which only leaves them with the option to lengthen when avoiding an obstacle. 2.6.1.2 Medial-lateral adaptation
As poor balance has shown to be a limiting factor in target stepping among stroke survivors (Nonnekes et al., 2010), it is likely that narrowing gait, which reduces the base of support,
will affect gait. However, no studies have investigated step narrowing and widening during walking in stroke survivors. Nonnekes et al. (2010) showed that step narrowing from standing makes stroke survivors’ foot placement less accurate than when widening. When support for balance (i.e. crutches) was allowed, the narrowing steps would be as accurate as the widening steps (Nonnekes et al., 2010). Stepping accuracy can be affected by a paretic leg in both the stance and step phase. During stance phase on the paretic leg weakness limits balance and drive in the targeting direction, affecting foot placement of the non-paretic limb. During Swing phase motor control affects the aim of the paretic leg. While no differences in error in foot placement or success have been found between paretic and non-paretic legs (Den Otter et al., 2005; Nonnekes et al., 2010; van Swigchem et al., 2013), Said et al. (2008), investigated balance during obstacle avoidances and did find a difference between paretic and non-paretic obstacle negotiation. A greater separation between CoP and centre of mass (CoM) during paretic stance compared to non-paretic stance. The separation between centre of pressure and CoM reflects an aspect of balance, as the CoM has to stay within the base of support to maintain stability. However, this balance deficit in stroke survivors does not seem to affect the success of obstacle avoidance and target stepping, it indicates underlying mechanisms for the overall declined success in stroke survivors is different for the paretic than the non-paretic limb. The increase in separation between CoM and centre of pressure during paretic stance and the decrease of stepping error when support for balance is offered supports a theory that weakness in the affected limb causes balance problems.
Besides the deficit of balance in stroke survivors, van Swigchem et al. (2013) proposed that motor control impairments, as reduced and delayed electromyogram responses, may underlie the diminished adaptability during walking. When motor control of the paretic leg affects targeting, a greater foot placement error on the paretic side would be expected. Accordingly, a study investigating over-ground target stepping found a greater time taken to walk over (and hit) stepping stones correlated with poorer balance scores (K. L. Hollands et al., 2016). In turn poor balance scores have been associated with high risk of falling, showing, albeit indirectly, that control of foot placement/adaptability of walking may be related to falls risk. The correlation between the success of stepping to targets on the paretic side and motor function corroborates evidence from previous studies (Den Otter et al., 2005; Nonnekes et al., 2010) which found that impairments in the control of paretic limb foot placement may be a limiting factor in gait adaptations, which will affect adaptations in the anterio-posterior direction as much as in the medio-lateral direction. Therefore, it is understood that balance
and motor control affect the medial stepping adjustments, although which of these represents the greater fall risk during walking is yet unknown.
2.6.2 When do stroke survivors need to see the target to respond
accurately?
It is known that young healthy adults become less successful in target stepping with a shorter available response distance or time to adjust the foot placement (Hoogkamer et al., 2015). However, in stroke survivors no studies to identify the time required to step to a target have been performed. Obstacle avoidance studies have shown that stroke survivors become less successful in avoiding the obstacle when they have less time to do so (Den Otter et al., 2005; van Swigchem et al., 2013). In tests with a short (150-300ms) available response time, a step- shortening strategy was preferred, but stroke survivors often failed to sufficiently shorten their step, resulting in hitting the obstacle (van Swigchem et al., 2013). One of the factors that could underlie this deficit is delayed and reduced muscle activations resulting in slower limb acceleration compared to healthy older adults (Nonnekes et al., 2010; van Swigchem et al., 2013). Both paretic and non-paretic sides are affected when adjusting foot placement, the cause however it is yet unclear whether the underlying cause is the same. Considering that young healthy adults are less successful in target stepping with a shorter available response distance/time, and stroke survivors hit more obstacles when they have less time to respond, it is likely that stroke survivors will have difficulty with target stepping under time pressure.
2.6.3 The role of the executive function lobe in target stepping in
stroke survivors
Impaired executive function is common following stroke; in acute stroke 50% suffers from cognitive impairments, especially in left cortical strokes where declined executive function is found to be present in 60-70%, is present 8-10 days after stroke (G. M. S. Nys et al., 2007; Zinn et al., 2007). These executive dysfunctions have also been found three months after stroke (Vataja et al., 2003). Executive function has been associated with the functional recovery post stroke (Hayes, Donnellan, & Stokes, 2013; Lesniak, Bak, Czepiel, Seniow, & Czlonkowska, 2008; G. M. Nys et al., 2005), Hayes et al. (2013), suggesting that stroke survivors might be more reliant on executive function abilities during less complicated tasks then healthy counter parts, which could affect the available executive function in walking in busy environments or performing double tasks. This difficulty in performing double tasks has
been shown in reduced success rates of stepping tasks during obstacle avoidance (van Ooijen et al., 2015), decline in remembering a shopping list while walking (Hyndman, Ashburn, Yardley, & Stack, 2006), and a decline in walking parameters while turning during a cognitive dual-task subsequently subtracting threes from hundred (K. L. Hollands et al., 2014). In addition, stroke survivors with increased functional disability tend to stop walking when talking (Hyndman & Ashburn, 2004). This increased load of the cognitive function in stroke survivors and in other neurological diseases like Parkinson’s Disease, multiple sclerosis and Alzheimer’s Disease, could be the reason they fall more often (Segev- Jacubovski et al., 2011), and are less able to adjust foot placement.