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Frente. Neurociência., 20 de janeiro de 2022 Sec. Neuropróteses Volume 15 - 2021 | https://doi.org/10.3389/fnins.2021.
Direcionando a
Integração Sensorial e
Motora para a
Recuperação do
Movimento Após Lesão
no SNC
Departments of Neurology and Orthopedics, Columbia University, New York, NY, United States
Resumo
O sistema nervoso central (SNC) integra informações sensoriais e motoras para adquirir movimentos habilidosos, conhecidos como integração sensório-motora (SMI). A interação recíproca dos sistemas sensorial e motor é pré-requisito para aprender e realizar movimentos
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Direcionando
a
Integração
Sensorial
e Motora
para a
Recuperação
do
Movimento
Após
Lesão no
SNC
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Ahmet S. Asan
James R. McIntosh
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habilidosos. Lesão em vários nós da rede sensorimotora causa comprometimento na execução do movimento e no aprendizado. Métodos de estimulação foram desenvolvidos para recrutar diretamente o sistema sensorimotor e modular redes neurais para restaurar o movimento após uma lesão no SNC. A Parte 1 revisa os principais processos e interações anatômicas responsáveis pela SMI na saúde. A Parte 2 detalha os efeitos da lesão em locais críticos para LMI, incluindo a medula espinhal, cerebelo e córtex cerebral. Por fim, a Parte 3 revisa a aplicação da plasticidade dependente da atividade de maneiras que visam especificamente a integração dos sistemas sensoriais e motores. Compreender cada um desses componentes é necessário para avançar em estratégias que visem a SMI e melhorar a reabilitação em humanos após lesões.
Parte 1: Integração Sensorimotora na Saúde
Integração Sensorimotora
O movimento habilidoso requer atividade neural coordenada dos sistemas sensorial e motor. Sua coativação temporizada é usada para convergir entradas sensoriais e motoras nos centros de integração sensorimotora (SMI) e visa promover a plasticidade em sua interseção. A integração sensoriomotora é o processo de incorporar sensações sobre o próprio corpo e o ambiente externo para moldar o movimento (Wolpert et al., ). Esse processo ocorre em várias áreas do sistema nervoso, incluindo a medula espinhal, tálamo, gânglios basais, cerebelo e várias áreas do córtex cerebral (
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Parte 1: Integra Sensor na Saúde
Parte 2: Perturb da Integra Sensor por Lesão ou Doenç
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Some of the important SMI centers and their connections mentioned in Part 1: (1) the sensorimotor cortex, (2) cerebellum, (3) posterior parietal cortex, (4) basal ganglia, (5) spinal cord, and (6) brainstem. Sensory information travels to the spinal cord via sensory afferents and then is relayed to the sensory centers in the cortex, thalamus, and cerebellum through the dorsal medial lemniscus (shown in red) and spinocerebellar pathway (shown in dark green), respectively. We have chosen not to show the spinothalamic pathway since it has not yet been shown to be crucial to SMI. The cerebellum constantly receives somatosensory information and integrates these senses with an efference copy of motor commands relayed through pontine nuclei located in the brain stem (shown with black arrows) to estimate the sensory consequences of movements. In turn, it provides feedback to the cortical areas through the thalamus. The motor cortex has loops with different cortical areas including basal ganglia, PPC, cerebellum, and brainstem. Information provided by these loops is used to shape the final motor command and the output is sent to the spinal cord. Descending cortical information synapses either directly with lower motor neurons or spinal i t Th t t t
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interneurons. The motor output travels through the ventral root of the spinal cord to muscles to generate movement.
We conceive of therapies directed at SMI as belonging to two main groups. The first is the coordinated activity of sensory and motor systems. Timed engagement of these systems through either endogenous activity (e.g., movement) or exogenous activity (induced by sensory or electrical stimulation) is a consistent theme of therapies targeting SMI. The second type of therapy targets where the two systems meet so that SMI is altered because of altering the gain of the integration site. Rather than altering multiple inputs to a site, these interventions change the state of the single site where integration occurs ( ).
Figure 2
Shows the organization in Part 2 and describes the different strategies of stimulation targeting SMI.
Relearning of Sensorimotor
Functions
Recovery of movement after injury or disease can involve similar processes to motor learning in health. One main difference to relearning after injury is that the circuits available for recovery are limited. A central strategy for
Figure 2
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unsupervised, and reinforcement learning (Doya, ). Different brain regions such as the cerebellum, basal ganglia, and cerebral cortex are specialized to use certain kinds of computation and learning (Doya, , ; Raymond and Medina, ). We will also discuss some of these mechanisms in more detail under relevant sections.
- Sensorimotor Integration in the Cortex
The cortical contribution to SMI is tuned by its connections to subcortical structures such as the thalamus and to areas within the cortex. After receiving peripheral somatosensory inputs, the thalamus relays that information primarily to layer 4 (L4) of the somatosensory cortex (S1) and also L of the primary motor cortex (M1) (Yamawaki et al., ; Barbas and García-Cabezas, ). The neurons in this layer have an excitatory projection within the hemisphere to L2-3 in the M1 and S1 (Yamawaki et al., ). Information flows between primary sensory and motor cortices largely through horizontal connections in L2–
- The axonal connection from sensory cortex onto neurons within motor cortex in this layer is the site for plasticity and sensorimotor integration (Kaneko et al., , ) and also essential for acquiring skilled movement (Papale and Hooks, ).
Sensory feedback enables skilled sensorimotor behavior, but the relatively long time needed for the feedback to reach sensorimotor centers can make adjustments slow (Miall and Wolpert, ). Use of an efferent phenocopy likely speeds the adjustment of the movement from forward model centers and is necessary for some skilled movement (Azim et al., ). The same motor command used to perform a
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movement is also delivered to the sensorimotor system such as the PPC and cerebellum, and the sensory feedback is interpreted in relationship to this plan (Wolpert et al., ). This model suggests that the CNS predicts the sensory consequences of motor movement and uses it to decrease the movement error, known as feedforward control. In this context, practice becomes crucial since it optimizes the internal mechanisms when the prediction and the sensory feedback do not overlap (error detection). That also means that sensory feedback updates the forward model in order to modify the motor plan, and this assists in generating a faster and more accurate movement. Learning in the CNS also improves motor performance and reduces the need for correction. Information processed in the cerebellum and cortex seems to play an essential role in this model.
- Cerebellum
The cerebellum is critical for feedforward control (Wolpert et al., ). It is thought to receive the efferent copy of the motor command through the cortico-ponto-cerebellar pathway and somatosensory information through the spinocerebellar tract. It also receives vestibular (Ango and Dos Reis, ) and visual information (Glickstein, ). This sensory and motor integration in the cerebellum is important for various sensorimotor tasks including coordination and postural control. Incoming sensory and motor information updates the cerebellum about the motor plan and the current state of the body. So, a prediction for the sensory consequence of the movement is made and feedback to cortical regions involved in the motor plan is made through the cerebello-thalamic-
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result also supports the role of the cerebellum for error reduction during motor learning. The spinocerebellar tract carries somatosensory information to the cerebellum, and impairment in this pathway also dramatically affects SMI and impairs skilled movement, balance, and posture (MacKinnon, ).
- Posterior Parietal Cortex
The PPC plays a pivotal role in creating an internal model of the outside world (Blakemore and Sirigu, ; McNamee and Wolpert, ). It receives and integrates the different sensory modalities from the somatosensory, visual, and auditory systems to generate the representation of the current state of the body and its environment. It contributes to several sensorimotor functions such as motor planning, visually guided locomotion, and eye movement (Konen and Kastner, ; Marigold and Drew, ). Previously, the direct connection of the PPC with M1 was in question. However, studies on non- human primates showed the presence of reciprocal connections between PPC and M1 and the premotor cortex (Fang et al., ). These findings are also supported by recent human studies in which paired PPC and M stimulation was applied and optimum latency was measured for altering the cortically evoked MEPs. The strongest facilitation was observed at 2–4 ms (Koch et al., , ; Karabanov et al., ). The short ISI indicates a monosynaptic connection between PPC and M1.
Posterior parietal cortex is heavily involved during the early phases of sensorimotor behavior. In the Karabanov et al. study, participants performed a sensorimotor task while cortical activity was recorded with EEG. They showed that interaction between
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M1 and PPC increased during the early phases of training and decreased in the late phases (Karabanov et al., ). Similar to the cerebellum, it is thought that the PPC receives the efference copy of the motor command and integrates this with the sensory information, and provides feedback to the motor cortex (Blakemore and Sirigu, ; Koch et al., ; Cui, ). The main differences between the cerebellum and PPC are the phase of motor learning during which they participate and the role in execution. Posterior parietal cortex appears to be more engaged in the early stages of sensorimotor learning and is also thought to be more involved in movement planning and goal selection (Mulliken et al., ; Aflalo et al., ). The cerebellum, on the other hand, participates more in late phases, and it contributes to the rapid prediction of the sensory consequences of movement (Blakemore and Sirigu, ; Hull, ).
- Basal Ganglia
The basal ganglia processes sensory and motor inputs from the cortex and shapes motor output. It receives somatotopically organized inputs from the motor cortex, premotor cortex, supplementary motor area, primary somatosensory cortex, and superior parietal lobule (Lanciego et al., ). After processing information from these multiple sources, it modulates the activity of the thalamus that in turn projects to the cortex. It does not receive direct sensory information from the periphery. The basal ganglia processes the signals through two different pathways: direct and indirect. At rest, it has an inhibitory tone in the thalamus (Fischer, ). The direct pathway removes the inhibition on the thalamus, and increases the motor cortex activity. The output of the
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reward but also prediction of the future reward, a critical component of reinforcement learning (Tanaka et al., ). This learning mechanism in the basal ganglia allows action selection by assessing capacity for reward.
- Spinal Cord
The spinal cord is the termination of motor output and the initial entry point for somatosensation, and it serves as a critical node of SMI. The spinal cord receives input from pyramidal neurons in layer 5 located in the premotor cortex, primary motor cortex, and primary and secondary somatosensory cortices directly via corticospinal tract (CST), and indirectly through brain stem projections. These descending motor pathways project onto the alpha motor neurons either directly or indirectly through premotor interneurons in the intermediate zone of the spinal cord. In humans, inputs from the somatosensory cortex project extensively onto the interneurons located in dorsal and lateral regions of the spinal cord while primary motor cortex inputs project more ventrally.
Interneurons integrate descending motor commands and segmental somatosensory information. As an example of how the spinal cord can accomplish complex movement, spinalized animals without any brain to spinal cord connections can walk and even recover from a stumble, all with spinal circuits alone (central pattern generators) (Whelan, ; Côté et al., ). This mechanism allows the spinal cord to contribute to generating rhythmic movement patterns such as walking and swimming (Marder and Bucher, ). Central pattern generators do not require sensory information for generating movement; however, sensory feedback is necessary to fine-tune motor output. In addition to coordinating movement,
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interneurons modulate reflexes and somatosensation. The incoming sensory afferents are presynaptically inhibited by interneurons whose activity is also controlled by descending cortical inputs (Flanders, ). This mechanism is named primary afferent polarization (PAD). This procedure occurs in the cord in a very selective manner to filter the sensory inputs (Eguibar et al., , ) and is shown to be a crucial mechanism for voluntary movement (Hultborn et al., ; Seki et al., ).
Spinal cord circuitry also plays a vital role in controlling respiratory muscles (Monteau and Hilaire, ; Gad et al., ) and is involved in haemodynamic stability (Squair et al., ). Further understanding of this circuitry is also important in developing stimulation where targeting SMI might also play a significant role in modulating these activities.
- Brainstem-Motor Pathways
Descending motor control is exerted both directly via the corticospinal system as well as indirectly through cortex to brainstem to spinal cord connections. As one of the important descending pathways located in the brainstem, the rubrospinal tract originates within the midbrain and contributes to SMI at the spinal level (Moreno-López et al., ). It arises from the red nucleus and receives inputs from different brain areas including cortex, via cortico-rubral tract, and the cerebellum (Wyart and Knafo, ). Rubrospinal inputs converge with CST in the spinal segmental level at interneurons and propriospinal neurons which are also receiving cutaneous and muscle afferents (Olivares-Moreno et al., ). The rubrospinal tract works in parallel with CST and is important for skilled movement. It plays a critical role
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to the environment to plan a movement. That motor plan is used to predict the sensory consequences, and updated with sensory feedback. Sensory-motor integration is a process that is disseminated across centers classically considered motor centers, such as the motor cortex and the ventral spinal cord, and sensory centers, such as the sensory cortex and sensory thalamus. Sensory-motor integration also involves several feedback loops involving the basal ganglia, cerebellum, and others. Knowledge of the nervous system circuits that enable skilled movement through SMI can be used to predict the consequence of injury (Part 2) and also guides application of interventions to strengthen SMI and improve function (Part 3).
Part 2: Disruption of Sensorimotor Integration by Injury or Disease
Lesion studies have taught us about the roles of the cortex in SMI. As one good example of this, Wolpert et al. studied a patient with a lesion in the superior parietal lobe (Wolpert et al., ). This patient showed impairment in detecting constant tactile and proprioceptive stimuli without visual information (tactile fading), even though she had intact proprioceptive and tactile systems. To investigate the motor consequences of tactile fading, the patient was asked to maintain a precision grip. Without visual feedback, she failed to generate a constant grip force which declined to near zero for about 15 s. The results of this study shed light on the role of PPC in SMI and demonstrated new evidence of its importance in storing inner representations of the body's state. In
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this part, we will briefly go over studies that assess how an injury or lesion in the sensorimotor centers, in particular the sensorimotor cortex, spinal cord, and cerebellum, affect sensorimotor behavior.
Injury in the Sensorimotor Cortex
Lesions in either primary or sensory cortices impair motor learning. Animal studies on cats (Sakamoto et al., ), monkeys (Pavlides et al., ; Liu and Rouiller, ), and rats (Kawai et al., ) showed that lesion in either one of these regions prevents the acquisition of skilled behavior and impairs sensorimotor learning. However, learned motor movements are not significantly affected by the injury of either the motor or somatosensory cortex (Pavlides et al., ; Kawai et al., ). These findings agree with others by showing the involvement of subcortical regions in motor learning and motor control (Jueptner et al., ; Errante and Fogassi, ). The basal ganglia (Foerde and Shohamy, ) and cerebellum (De Zeeuw and Ten Brinke, ) in particular are likely the locus of movement memory.
Middle cerebral artery stroke damages sensory and motor cortices and, therefore, results in movement impairment (Walcott et al., ; Bolognini et al., ; Edwards et al., ). Most stroke patients show difficulty with tactile sensation, proprioception, and stereognosis (Winward et al., ; Connell et al., ). Considering the necessity of sensory information for performing a successful sensorimotor task, deficits in the sensory system directly cause sensorimotor dysfunctions such as disruption in postural control (Dietz, ), impairment in temporal (Gentilucci et al., ), and spatial (Gordon et al., ) movement
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after SCI (Adams and Hicks, ; Nielsen et al., ; Holtz et al., ). Attenuation of the spinal inhibitory mechanism, hyperexcitability of motoneurons, and lack of supraspinal input in the cord are some of the main reasons causing these dysfunctions.
Cerebellar Degeneration
Cerebellar degeneration occurs due to the deterioration of the cerebellar neurons, and this increases progressively in many of the common cerebellar diseases. This degeneration could result from either genetic (Paulson, ) or non-genetic causes (Sullivan et al., ). Lesions in other CNS areas such as spinal cord can also impair the cerebellar circuitry due to loss of critical inputs (Visavadiya and Springer, ; Lei and Perez, ). As a result, cerebellar patients manifest uncoordinated movement along with deficits in motor adaptation/learning such as visuomotor learning and adaptations in walking and reaching (Schlerf et al., ; Martino et al., ).
Diseases affecting cerebellar processing also alter its influence on other CNS regions. Ming Kuei Lu et al. showed that repetitive paired cerebellum and motor cortex stimulation causes lasting changes in motor cortex excitability (Lu et al., ). However, this modulatory effect dissipated in patients with Parkinson's disease and spinocerebellar ataxia (Lu et al., ). Cerebellar-cortex inhibition was also abrogated in those patients. Similarly, others showed that activity in the cerebellum modulates the plasticity in the brain induced by paired motor cortex-peripheral nerve stimulation (Hamada et al., ; Popa et al., ). This facilitatory effect is disrupted in patients with cerebellar degeneration (Dubbioso et al., ). As another approach, repetitive
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stimulation of peripheral nerves also adjusts motor cortex excitability (Kaelin-Lang et al., ; Luft et al., ). It has been postulated that sensory inputs directly act in the motor cortex to generate this effect. However, this observed effect disappears in rats with removal of the controlling half of the cerebellum (Nordeyn et al., ; Taib et al., ). This highlights that cerebellar processing of sensory information is essential for this form of cortical plasticity (Luft et al., ).
Summary
Central nervous system injury and disease perturbs sensorimotor integration through disruption of nodes of the network or by their disconnection. The type of movement disturbance ranges from loss of fine control to paralysis, depending on the location and severity. The pattern of injury also helps to determine the substrate to target for therapy (Part 3). In many cases, this will be the node of the network that was disrupted. However, other therapies target intact circuits that are intended to take over the functions of the injured ones.
Part 3: Targeting SMI for the Recovery of Movement After Injury
In the Introduction, we described two main approaches to targeting SMI for recovery of movement: timed activity of sensory and motor systems, and strengthening the sites where integration occurs ( ). In this section, we describe interventions that target SMI, either explicitly or implicitly. In these descriptions, we try to identify the biological processes involved. For
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