A large-scale investigation of sensorimotor learning in schizophrenia and elderly participants was conducted. The current paper presents three of the learning tasks that were carried out in the two experimental groups and in healthy controls. A single aiming task (SAT) over repetitions measured improvement in motor acuity which has never been investigated in schizophrenia and elderly participants. In addition, explicit sequence learning remains unclear in both groups and was therefore investigated using the EPLT. The CVLT was administered as a measure of cognitive learning, to contrast cognitive learning and sensorimotor learning in these groups.

The large-scale investigation measured numerous sensorimotor subprocesses including explicit and implicit sequence learning and adaptation, motor acuity, tracking, applied tasks (specifically writing) and cognitive tasks. Results of the three new tasks will be discussed first. The present findings will then be discussed in light of all previous findings to map out specific deficiencies in sensorimotor learning in schizophrenia and to compare schizophrenia with aging on sensorimotor learning and performance.

New findings

Motor learning in the SAT involved improving acuity, i.e. increasing speed and accuracy of a rather simple movement that varied in direction, distance and target width. Results demonstrated improvement over sessions in all three groups (MT decreased in E: 24%, S: 22% and C: 16%). This improvement was even larger for the elderly and schizophrenia group but this could be attributed to their very high initial values. While the findings that individuals with schizophrenia would not have difficulties in learning in this task were expected, the hypothesis that elderly participants would be impaired in learning in this task was not confirmed.

Interestingly, differences between the groups were found while analysing the main primary movement (PM) and secondary movements separately. In all three groups, over sessions the main PM increased in speed and accuracy and there was a decrease in the number of secondary movements. However, controls reached the targets much faster and with a higher peak velocity in the main PM than both experimental groups. In addition, accuracy of the PM was much lower in the elderly group causing them to make more secondary movements than the schizophrenia group. When comparing conditions with equal Index of difficulty (ID), a linear increase of MT with task difficulty was nearly perfect, however the elderly deviated from this straight line with a longer MT when the target was small. In other words, although the elderly showed significant learning, they were less accurate than individuals with schizophrenia.

The cause of longer MT in the elderly may be the result of slower movement speed or it may be caused by less accurate movement precision. If muscle force is more variable (less precise) in the execution of a main movement, then the target will be missed more frequently and additional movements will be needed to correct the movement, resulting in prolonged MT. This is what seems to have been the case. This finding and its interpretation is in line with earlier research suggesting that reduced movement accuracy (Voelcker-Rehage 2008) and increased movement variability (Seidler et al. 2010) requiring multiple corrective movements (Ketcham et al. 2002) is the primary cause of age-related slowing. Whether this variability originates from the planning stage of the movement or from the way these plans are transmitted by the peripheral nervous systems or executed by the muscles cannot be deducted from our data. It was observed that many elderly participants were frequently surprised and annoyed by their inaccuracy. It stimulated extra effortful attention focused on making the corrective secondary submovements as fast as possible. This attempt at compensation and the resulting cortical overactivation patterns in aging has been reviewed by Hill et al. (2020) and more recently demonstrated by Van Ruitenbeek et al. (2022).

In the EPLT participants had to learn a sequence of twelve movements. This pattern had to be discovered by trial and error. Individuals with schizophrenia were not impaired but the elderly learned this sequence slower than controls.  Unexpectedly, the rate of learning in the elderly group was much lower than that of the schizophrenia group. The high frequency of target errors made by elderly participants, even in the third session suggests that they were less successful in the storage or retrieval of the target positions.

One possible explanation for the observed difficulties in learning this task is that elderly participants might have approached this task wrongly. Despite clear instructions to put the learning of the pattern first, they may have focused too much on speed, a strategy adapted from previous tasks (such as in the SAT, among others), thus taking insufficient time between trials to consciously store the features of the positions of successive targets. This explanation would predict that the time between target movements, i.e. the RT for the next target, should be smaller in the elderly group than in the schizophrenia group. However the reverse was found. Another possible explanation emphasizes that elderly individuals require extra attention to correct their frequent movement inaccuracies. This might lower their capacity for conscious coding and storage of discovered targets while they were moving. If their goal was to find the right target quickly by trial and error and to rely on automatic storage, not spending much attention and time to store the specific features of the found target, then the high RT can be explained by trying to find in memory a location of the next target which was not properly stored earlier. In support of this explanation are many studies, reviewed by Seidler et al. (2010), that have reported deficits in older adults simultaneously performing cognitive and motor tasks.

Results of the Verbal Learning Task (CVLT) demonstrated that both the elderly and schizophrenia group performed less well than the control group as expected. However, in contrast to results of the EPLT, elderly participants performed significantly better on this cognitive task than those with schizophrenia. In the CVLT all attention could be focused on one type of information, while the EPLT required additional attention to movement execution. The CVLT was not administered under time pressure, and the 16 items that had to be remembered had easy (word) codes, while the twelve target positions in the EPLT required elaborate spatial coding (e.g. ‘go one step from here diagonally down to the left’). The EPLT could therefore be categorised as a complex learning task, which is in line with previous suggestions that motor learning diminishes in old age as tasks become more complex (King et al. 2013; Bootsma et al. 2021; Van Ruitenbeek et al. 2022).

Together, these new findings of two very diverse motor learning tasks and one cognitive learning task demonstrate quite different patterns of results among the groups. Specifically, elderly individuals were less accurate in the SAT and learned less in the EPLT, while individuals with schizophrenia performed worse on cognitive learning.

Results of the current tasks in light of previous findings

Table 5 provides a comprehensive summary of all tasks conducted with their results. This summary, based on the data presented in Table 4, shows that individuals with schizophrenia and elderly individuals demonstrated significant sensorimotor learning in all categories of motor learning except in the over-learned task of writing digits. These learning results were obtained despite marked psychomotor slowing in schizophrenia and the elderly, as found in SDST writing, in the SAT and on baseline trials of the implicit sequence learning tasks and adaptation tasks.

Table 5 Summary of findings

From Table 5 it is also clear that the two experimental groups showed different patterns of results. Equal learning was found in all three groups when learning instructions were not explicit, as in improving acuity (SAT), implicit motor sequence learning and in cognitive learning of SDST symbol-digit pairs. The schizophrenia group learned better than the elderly in explicit sequence learning and in tracking, while the elderly group scored higher than the schizophrenia group on adaptation tasks and verbal learning. These patterns will be discussed below.

Motor learning in the elderly

Elderly participants demonstrated intact motor learning on simple tasks, such as the SAT. This is supported by intact motor learning on the random blocks of the IPLT (Cornelis et al. 2016). These tasks were simple in that only one short, fast, straight movement was required towards a clearly visible target. However, on tracking tasks in which a moving target had to be closely followed, the elderly group showed significantly less learning compared to both controls and to the schizophrenia group (De Picker et al. 2014). Additionally, results from the current tasks demonstrated that explicit learning of a target sequence was more difficult for the elderly. These combined results are in line with the conclusion drawn in an often cited review by Voelcker-Rehage (2008), that in more complex tasks and with increased difficulty level, age-related learning differences become more pronounced. Furthermore, older adults rely more on visual control. This could explain why in this study elderly individuals were hardly effected by an unexpectedly altered (rotated or shortened) visual feedback of their movements on adaptation tasks (Cornelis et al. 2022). Online correction, driven by visual feedback, has become part of their normal habit.

‘Complexity’ or ‘difficulty’ of a task can be increased in different ways. Firstly, by increasing extra demands on corrective motor control, as when target size or trajectory path (Bootsma et al. 2021) become smaller or when the target is moving. Secondly, complexity increases when explicit cognitive processes needed for planning or execution of a movement sequence ask for more elaborate processing, as when sequences are longer or when the spatial coding of the targets is more complex. An account of why ‘complexity’ results in less motor learning is given in Seidler’s “Supply and demand” framework (Seidler et al. 2010; Seidler and Carson 2017). In this framework, deficits in motor performance in old age such as increased variability of movement and slowing of movement, are caused by a dysfunction of the central and peripheral nervous systems as well as the neuromuscular system. This motor deficit, meaning less supply of motor control, then requires higher demands on cognitive brain processes needed for motor control, and this in turn reduces the capacity for cognitive learning of target sequences.

Motor learning in schizophrenia

Individuals with schizophrenia also demonstrated intact motor learning on simple tasks, such as the SAT as well as in the random blocks of the IPLT (Cornelis et al. 2022). In addition, on three implicit learning tasks (SAT, IPLT and SDST matching) individuals with schizophrenia learned as well as controls. When explicit, conscious-cognitive processing was called for, as in the EPLT, the rate of learning in the schizophrenia group was not significantly reduced compared with controls. This is in contrast with the reduced performance in the CVLT, a cognitive learning task, where individuals with schizophrenia performed worse than both controls and the elderly, highlighting their cognitive difficulties. Manifestations of a cognitive deficit interfering with motor learning tasks were observed in the implicit sequence learning task, in which subjective sequence awareness arose significantly less (Cornelis et al. 2016). Therefore, it can be suggested that individuals with schizophrenia are impaired on sensorimotor learning paradigms in which explicit cognitive processes play a role.

However, in addition to the sometimes minor effects of deficient explicit cognitive processing on learning in schizophrenia, their slower adaptation in the three adaptation tasks (see Fig. 8, Table 4) is more remarkable. They might have detected the perturbation of the movement feedback later (as argued in Cornelis et al. 2022), but on later adaptation trials they still lagged far behind the elderly and the controls in adjusting their movements to the altered sensory feedback. Even more revealing was their behaviour on post-adaptation trials, specifically in the gain adaptation and the VRT, which showed that they had not rebuild or changed an automatised forward model for movements in the altered situation, a model which needed to be corrected when normal feedback was again restored. Visuomotor adaptation is now generally viewed as the combined action of explicit learning driven by the detection of a performance error and implicit learning of a forward model driven by prediction error (Heuer and Hegele 2011). The significant different behaviour on post-adaptation trials of the schizophrenia group compared with controls and the elderly, suggests that this implicit sensorimotor adaptation in schizophrenia is also impaired. The implications of difficulties in motor adaptation in schizophrenia may suggest a general disability to adapt to changes in any situation. A suggestion of further research is evident.

Cognitive and motor influences on sensorimotor slowing in schizophrenia

It is important to understand the nature of slow motor performance demonstrated in schizophrenia (see Table 5) and highlight that a diminished speed of cognitive processes related to actions in schizophrenia must play an important role. At a low level of cognitive processing, sensory processing (both auditory and visual) has been demonstrated to be dysfunctional in schizophrenia and found to contribute to higher-order cognitive dysfunction (Dong et al. 2023). Sensory discrimination has also been found to be significantly lower in individuals with schizophrenia (Koshiyama et al. 2021). In addition, higher order perceptual processes have been demonstrated to be deficient in schizophrenia using various drawing (copying) tasks (Jogems-Kosterman et al. 2001; Morrens et al. 2008; Grootens et al. 2009; Bervoets et al. 2014; Janssens et al. 2018). Copying rests on cognitive processes such as recognition, coding, storage in working memory and subsequent retrieval of the figure that has to be drawn. It also requires the use of executive processes to plan the optimal movement sequence. In addition, slowing in schizophrenia may arise from difficulties in monitoring the movement. It is therefore quite plausible that individuals with schizophrenia were less accurate or later to detect deviations from their planned movement. In addition, they might have been slower in making necessary movement adjustments. Monitoring and quick correction require intensive focused attention and sufficient arousal, which also might have been suboptimal in the schizophrenia group.

In a recent review on psychomotor slowing in schizophrenia, Osborne et al. (2020) made a distinction between cognitive (prefix “psycho”) and motor execution (root word “motor”) aspects of psychomotor slowing. Motor aspects were defined as processes implicated in the initiation, coordination, and execution of movements. Many studies have demonstrated that individuals with schizophrenia have impaired cognitive processes involved in response selection and motor preparation, however findings of impaired motor execution are less consistent (Osborne et al. (2020, p 6)). Following this, the SAT and the baseline stages of IPLT, EPLT and VRT are a step towards investigating ‘pure’ motor execution aspects of sensorimotor slowing as these tasks require minimal cognitive processes. The present study therefore provides strong evidence for ‘motor’ slowing in schizophrenia (evident with very large effect sizes, see Table 4). This evidence is consistent with previously reviewed slow movements in the line-copying task (Jogems-Kosterman et al. 2001; Morrens et al. 2008; Docx et al. 2012, 2013; Janssens et al. 2018).

Although the SAT has the least cognitive components compared with other tasks, this task still required some implicit planning involving the choice for the optimal posture of arm, hand and fingers. Similarly, drawing a single line follows several implicit planning rules or so-called graphic production rules about the best way to start and to connect lines (Thomassen et al. 1991). When drawing a series of lines that gradually tilt from vertical to horizontal, somewhere half way in that series most people change their movement direction from top-down to left–right. Individuals with recent-onset schizophrenia made this shift much less frequently or much later than healthy controls (Grootens et al. 2009). In addition, when individuals with schizophrenia were instructed to begin drawing at a point that conflicted with the preference predicted by graphic production rules, more time was needed to initiate the drawing (Jogems-Kosterman et al. 2006; Grootens et al. 2009). Together these results show that implicit planning of very simple movements is also affected in schizophrenia.

Implicit planning of a movement, such as selection and positioning of our limbs is done without awareness of the choices or the forces that are involved. Yet it is based on ‘knowledge’, and the fact that a strong learning effect was demonstrated over sessions in these tasks suggests that this ‘knowledge’ can be increased. Therefore, it is hard to draw a line between ‘psycho’ and ‘motor’ in action research, on a scale between pure motor execution and higher order cognitive processes (Rosenbaum 2017; Rosenbaum and Feghhi 2019).

Implications of findings in schizophrenia

As argued before, a large array of different cognitive processes are closely related to sensorimotor slowing and diminished motor learning in schizophrenia. It has been proposed that the neural underpinnings of these processes comprise of parieto-frontal networks, the supplementary motor area (SMA) and pre-supplementary motor area (pre-SMA), important for planning movement sequences (Osborne et al. 2020). This view has been broadened to include effects of biochemical modulation, specifically taking into account affective changes interacting with psychomotor mechanisms leading to abnormalities (Northoff et al. 2021). In this view, the interaction between ‘psycho’ and ‘motor’ is highlighted, and a strict division of motor function from affective and cognitive function is rejected.

Difficulties in sensorimotor adaptation in schizophrenia provide evidence for the connection between these different functions on a neurobiological level. Sensorimotor adaptation relies heavily on cerebellar activity (Seidler et al. 2010; Izawa et al. 2012; Krakauer et al. 2019). An influential integrative theory of schizophrenia, already proposed by Andreasen et al. (1998), posits a cognitive dysmetria model in which a disruption to the cortico-cerebellar-thalamic-cortical circuit underlies a broad set of sensorimotor and cognitive dysfunction. In this circuit, the cerebellum plays a primary coordinative role and one way to test this theory is to examine if adaptation in schizophrenia is diminished (Cornelis et al. 2022). More recently also Mittal et al. (2021) stressed the importance of the role of the cerebellum and the CTCC circuits in psychomotor activity, which is in line with neuroimaging studies demonstrating CTCC dysfunction relating to sensorimotor abnormalities in schizophrenia (Hirjak et al 2021a). Importantly, evidence for ‘motor’ slowing found in the present study (see Table 4, Table 5 and the paragraph below), together with evidence of impaired implicit sensorimotor adaptation, strongly support CTCC dysfunction in schizophrenia.

In addition, psychomotor slowing is not an unitary phenomenon, but consists of a wide range of distinct sub-processes of specific cognitive and motor deficiencies with possible different patterns across individual patients. This has important implications for future research. Clearly making a distinction between ‘psycho’ and ‘motor’ components is not only difficult but is also simplifying and masking the variety of possible delays in sensorimotor learning and performance. On the other hand, while it is valuable to stress the interconnectedness of cognitive and motor processes (Northoff et al. 2021), treating psychomotor slowing in schizophrenia, depression and Parkinson’s disease as a uniform dimension could detract from the ultimate goal to find the underlying causes of the motor abnormalities in these illnesses, which are probably highly different. Therefore, as a supplement to the extensive research on cognitive impairments in schizophrenia, which has led to the identification of separable cognitive factors in schizophrenia (Nuechterlein et al. 2004), future research should be conducted in the motor domain (in a RDoC perspective) focusing on distinct sub-processes contributing to psychomotor slowing in schizophrenia.

In the present study it was demonstrated that rates of learning in various motor learning categories differed highly between schizophrenia and elderly. One of the aims of this investigation was to compare supposed declines in categories of motor learning in schizophrenia with expected decreases in the elderly. This was motivated by recent research of Kirkpatrick et al. (2008) and Kirkpatrick and Kennedy (2018), supporting the theory that schizophrenia might be a neurodegenerative disorder with genetic, functional-organic and neuroanatomical features of accelerated aging sharing similarities with elderly individuals. However, results of the present study demonstrating different patterns of decline in motor speed and motor learning in schizophrenia patients and the elderly do not support this hypothesis.

Findings of this study have clinical implications as well. Daily functioning relies heavily on the quality of a range of cognitive abilities and motor skills. Both individuals with schizophrenia and their therapists must realise that not only do cognitive deficits have negative influences on functional outcome but also declining psychomotor skills play a role as well, specifically on motor skills. While psychomotor slowing and learning of sensorimotor tasks in schizophrenia is more pronounced as cognitive demands increase, their difficulties are not restricted to complex, cognitively charged motor skills. Difficulties also manifest in very simple motor tasks, which may provide valuable information for daily functioning in work and home situations. In addition, variability found amongst patients suggests that psychomotor slowing may not be an obstacle for all patients and suggests the use of testing motor skills to understand their limitations and to advise on employment opportunities. The finding that significant motor learning is possible might be of value for therapeutic programs in which motor skills are trained (i.e. sport, music or other leisure activities). It is also important in training to take into account their difficulties with adaptation to changing sensory conditions.

Limitations

A few strengths and limitations of this large scale investigation should be mentioned. Its strength lies in the design of the investigation in which multiple motor learning tasks were studied on the same set of participants and over repeated sessions. This might have created a limitation in that only individuals who were able to complete the tasks in all three one hour sessions were included in the study. As such, the motor learning and performance capabilities demonstrated in this study might be higher than what would be expected in schizophrenia and at old age respectively. However, the mean and range of scores on the negative symptoms scale of the patients in the present study were comparable to a large heterogenous sample of patients with schizophrenia (Van Erp et al. 2014), suggesting that results of the current study may be reflective of general schizophrenia. A second limitation concerns the fact that all patients with schizophrenia in the current study were taking (more than) one antipsychotic at the time of testing. The effect of antipsychotics on motor learning has still to be investigated.

It is possible that movement slowing in schizophrenia could be the result of sedentary lifestyles as opposed to neurological factors. Studies using actigraphy on patients with schizophrenia (Pieters et al. 2021), showed that low physical activity and sedentary behaviour of many of these patients is associated with movement disorders, in particular slowing evident in parkinsonism. However, the patients in the current study were out-patients and the elderly made a rather active impression on the evaluation clinician. More research is needed to determine whether psychomotor slowing leads to sedentary behaviour or whether an inactive life style results in observed psychomotor slowing.