Claire F. Honeycutt

Electromyographic Responses From the Hindlimb Muscles of the Decerebrate Cat to Horizontal Support Surface Perturbations

The sensory and neural mechanisms underlying postural control have received much attention in recent decades but remain poorly understood. Our objectives were 1) to establish the decerebrate cat as an appropriate model for further research into the sensory mechanisms of postural control and 2) to observe what elements of the postural response can be generated by the brain stem and spinal cord. Ten animals were decerebrated using a modified premammillary technique, which consists of a premammillary decerebration that is modified with a vertical transection near the subthalamic nucleus to eliminate spontaneous locomotion. Horizontal support surface perturbations were applied to all four limbs and electromyographic recordings were collected from 14 muscles of the right hindlimb. Muscle activation was quantified with tuning curves, which compared increases and decreases in muscle activity to background and graphed the difference against perturbation direction. Parallels were drawn between these tuning curves, which were further quantified with a principal direction and breadth (range of directions of muscle activation), and data collected by other researchers from the intact animal. We found a strong similarity in the direction and breadth of the tuning curves generated in the decerebrate and intact cat. These results support our hypothesis that directionally specific tuning of muscles in response to support surface perturbations does not require the cortex, further indicating a strong role for the brain stem and spinal cord circuits in mediating directionally appropriate muscle activation patterns.

Evidence for reticulospinal contributions to coordinated finger movements in humans

The reticulospinal tract was recently shown to have synaptic connections to the intrinsic muscles of the fingers in nonhuman primates, indicating it may contribute to hand function long thought to be controlled exclusively through corticospinal pathways. Our objective was to obtain evidence supporting the hypothesis that these same anatomical connections exist in humans. startReact, an involuntary release of a planned movement via the startle reflex, provides a noninvasive means to examine the reticulospinal tract in humans. We found that startReact was triggered during coordinated grasp but not individuated finger movements. This result suggests that the reticulospinal tract does have connections to the intrinsic muscles of the fingers in humans but its functional role is limited to coordinated movement of the whole hand. These results do not diminish the well-established role of corticospinal pathways in the control of hand movement. Indeed, they cement the significance of corticospinal pathways in individuated finger movement control. Still, these results point to an updated and expanded view of distal hand control where reticulospinal and corticospinal pathways work in parallel to generate a large repertoire of diverse, coordinated movement in the hand. Finally, the presence of reticulospinal pathways to the muscles of the hand makes this pathway an attractive therapeutic target for clinical populations where the corticospinal tract is absent or injured.

Planning of ballistic movement following stroke: insights from the startle reflex.

Following stroke, reaching movements are slow, segmented, and variable. It is unclear if these deficits result from a poorly constructed movement plan or an inability to voluntarily execute an appropriate plan. The acoustic startle reflex provides a means to initiate a motor plan involuntarily. In the presence of a movement plan, startling acoustic stimulus triggers non-voluntary early execution of planned movement, a phenomenon known as the startReact response. In unimpaired individuals, the startReact response is identical to a voluntarily initiated movement, except that it is elicited 30–40 ms. As the startReact response is thought to be mediated by brainstem pathways, we hypothesized that the startReact response is intact in stroke subjects. If startReact is intact, it may be possible to elicit more task-appropriate patterns of muscle activation than can be elicited voluntarily. We found that startReact responses were intact following stroke. Responses were initiated as rapidly as those in unimpaired subjects, and with muscle coordination patterns resembling those seen during unimpaired volitional movements. Results were striking for elbow flexion movements, which demonstrated no significant differences between the startReact responses elicited in our stroke and unimpaired subject groups. The results during planned extension movements were less straightforward for stroke subjects, since the startReact response exhibited task inappropriate activity in the flexors. This inappropriate activity diminished over time. This adaptation suggests that the inappropriate activity was transient in nature and not related to the underlying movement plan. We hypothesize that the task-inappropriate flexor activity during extension results from an inability to suppress the classic startle reflex, which primarily influences flexor muscles and adapts rapidly with successive stimuli. These results indicate that stroke subjects are capable of planning ballistic elbow movements, and that when these planned movements are involuntarily executed they can be as rapid and appropriate as those in unimpaired individuals.

The decerebrate cat generates the essential features of the force constraint strategy.

Cats actively respond to horizontal perturbations of the supporting surface according to the force constraint strategy. In this strategy, the force responses fall into two groups oriented in either rostral and medial directions or caudal and lateral directions, rather than in strict opposition to the direction of perturbation. When the distance between forelimbs and hindlimbs is decreased, the responses are less constrained and directed more in line with the perturbation. We have recently shown that electromyographic responses from limb muscles of the decerebrate cat resemble those obtained in the intact animal. Our objectives here were to determine whether the decerebrate cat preparation would also exhibit the force constraint strategy and whether that strategy would exhibit the characteristic dependence on limb position on the strategy. Horizontal support surface perturbations were delivered and three-dimensional exerted forces were recorded from all four limbs. Clustered force responses were generated by all four limbs and were found to be statistically indistinguishable between animals decerebrated using two different levels of transection. The directionality of the force responses was preserved throughout successive time epochs during the perturbations. In addition, the clustering of force responses increased with distance between forelimbs and hindlimbs. These results indicate that the force constraint strategy used by terrestrial animals to maintain stability can be generated without the assistance of the cerebral cortices and without prior training. This suggests an important role for the lower brain stem and spinal cord in generating an appropriate strategy to maintain stability.

Bilateral impairments in task-dependent modulation of the long-latency stretch reflex following stroke

OBJECTIVE Modulation of the long-latency reflex (LLR) is important for sensorimotor control during interaction with different mechanical loads. Transcortical pathways usually contribute to LLR modulation, but the integrity of pathways projecting to the paretic and non-paretic arms of stroke survivors is compromised. We hypothesize that disruption of transcortical reflex pathways reduces the capacity for stroke survivors to appropriately regulate the LLR bilaterally. METHODS Elbow perturbations were applied to the paretic and non-paretic arms of persons with stroke, and the dominant arm of age-matched controls as subjects interacted with Stiff or Compliant environments rendered by a linear actuator. Reflexes were quantified using surface electromyograms, recorded from biceps. RESULTS LLR amplitude was significantly larger during interaction with the Compliant load compared to the Stiff load in controls. However, there was no significant change in LLR amplitude for the paretic or non-paretic arm of stroke survivors. CONCLUSION Modulation of the LLR is altered in the paretic and non-paretic arms after stroke. SIGNIFICANCE Our results are indicative of bilateral sensorimotor impairments following stroke. The inability to regulate the LLR may contribute to bilateral deficits in tasks that require precise control of limb mechanics and stability.

Muscle spindle responses to horizontal support surface perturbation in the anesthetized cat: insights into the role of autogenic feedback in whole body postural control

Intact cats and humans respond to support surface perturbations with broadly tuned, directionally sensitive muscle activation. These muscle responses are further sensitive to initial stance widths (distance between feet) and perturbation velocity. The sensory origins driving these responses are not known, and conflicting hypotheses are prevalent in the literature. We hypothesize that the direction-, stance-width-, and velocity-sensitive muscle response during support surface perturbations is driven largely by rapid autogenic proprioceptive pathways. The primary objective of this study was to obtain direct evidence for our hypothesis by establishing that muscle spindle receptors in the intact limb can provide appropriate information to drive the muscle response to whole body postural perturbations. Our second objective was to determine if spindle recordings from the intact limb generate the heightened sensitivity to small perturbations that has been reported in isolated muscle experiments. Maintenance of this heightened sensitivity would indicate that muscle spindles are highly proficient at detecting even small disturbances, suggesting they can provide efficient feedback about changing postural conditions. We performed intraaxonal recordings from muscle spindles in anesthetized cats during horizontal, hindlimb perturbations. We indeed found that muscle spindle afferents in the intact limb generate broadly tuned but directionally sensitive activation patterns. These afferents were also sensitive to initial stance widths and perturbation velocities. Finally, we found that afferents in the intact limb have heightened sensitivity to small perturbations. We conclude that muscle spindle afferents provide an array of important information about biomechanics and perturbation characteristics highlighting their potential importance in generating appropriate muscular response during a postural disturbance.

Disruption of cutaneous feedback alters magnitude but not direction of muscle responses to postural perturbations in the decerebrate cat

Quadrupeds and bipeds respond to horizontal perturbations of the support surface with muscular responses that are broadly tuned and directionally sensitive. Since the discovery of this directional sensitivity, interest has turned toward the critical sensory systems necessary to generate these responses. We hypothesize that cutaneous feedback affects the magnitude of muscle responses to postural perturbation but has little effect on the directionality of the muscle response. We developed a modified premammillary decerebrate cat preparation to evaluate the sensory mechanisms driving this directionally sensitive muscle activation in response to support surface perturbation. This preparation allows us the flexibility to isolate the proprioceptive (cutaneous and muscle receptors) system from other sensory influences. We found that loss of cutaneous feedback leads to a significant loss in background activity causing a smaller muscular response to horizontal perturbations. However, the directional properties of the muscular responses remained intact.

Startle evoked movement is delayed in older adults: implications for brainstem processing in the elderly

Little attention has been given to how age affects the neural processing of movement within the brainstem. Since the brainstem plays a critical role in motor control throughout the whole body, having a clear understanding of deficits in brainstem function could provide important insights into movement deficits in older adults. A unique property of the startle reflex is its ability to involuntarily elicit planned movements, a phenomenon referred to as startReact. The noninvasive startReact response has previously been used to probe both brainstem utilization and motor planning. Our objective was to evaluate deficits in startReact hand extension movements in older adults. We hypothesized that startReact hand extension will be intact but delayed. Electromyography was recorded from the sternocleidomastoid (SCM) muscle to detect startle and the extensor digitorum communis (EDC) to quantify movement onset in both young (24 ± 1) and older adults (70 ± 11). Subjects were exposed to a startling loud sound when prepared to extend their hand. Trials were split into those where a startle did (SCM+) and did not (SCM−) occur. We found that startReact was intact but delayed in older adults. SCM+ onset latencies were faster than SCM− trials in both the populations, however, SCM+ onset latencies were slower in older adults compared to young (Δ = 8 msec). We conclude that the observed age‐related delay in the startReact response most likely arises from central processing delays within the brainstem.

The mechanical actions of muscles predict the direction of muscle activation during postural perturbations in the cat hindlimb

Humans and cats respond to balance challenges, delivered via horizontal support surface perturbations, with directionally selective muscle recruitment and constrained ground reaction forces. It has been suggested that this postural strategy arises from an interaction of limb biomechanics and proprioceptive networks in the spinal cord. A critical experimental validation of this hypothesis is to test the prediction that the principal directions of muscular activation oppose the directions responding muscles exert their forces on the environment. Therefore, our objective was to quantify the endpoint forces of a diverse set of cat hindlimb muscles and compare them with the directionally sensitive muscle activation patterns generated in the intact and decerebrate cat. We hypothesized that muscles are activated based on their mechanical advantage. Our primary expectation was that the principal direction of muscle activation during postural perturbations will be directed oppositely (180°) from the muscle endpoint ground reaction force. We found that muscle activation during postural perturbations was indeed directed oppositely to the endpoint reaction forces of that muscle. These observations indicate that muscle recruitment during balance challenges is driven, at least in part, by limb architecture. This suggests that sensory sources that provide feedback about the mechanical environment of the limb are likely important to appropriate and effective responses during balance challenges. Finally, we extended the analysis to three dimensions and different stance widths, laying the groundwork for a more comprehensive study of postural regulation than was possible with measurements confined to the horizontal plane and a single stance configuration.

Startling Acoustic Stimuli Elicit Rapid Hand Extension Following Stroke

Loud startling acoustic stimuli can involuntarily elicit planned movements faster than is possible voluntarily. This phenomenon, known as startReact, is thought to be mediated through brainstem pathways. The startReact can be elicited in stroke survivors with a cortical lesion. This has been demonstrated for elbow motions, thought to have significant input from brainstem pathways. This study sought to determine if the startReact can also be elicited for hand movements following stroke, even though these are driven predominantly by the motor cortex.Data were collected from 8 stroke survivors performing rapid hand extension movements. StartReact responses could be elicited in 7 of 8 subjects. Across all subjects, the startling acoustic stimuli were able to decrease movement times substantially (∆ 57ms; p ≈ 0) when indicators of startle were detected. However, these responses were elicited less frequently than previous reports for startReact at the elbow. Nevertheless, the intact startReact response suggests that the integrity and actions of the pathways mediating this response should be considered when rehabilitating the hand following stroke.