Clin Neurophysiol. 2014 Aug;125(8):1682-8. doi: 10.1016/j.clinph.2013.12.102.

Deficits in startle-evoked arm movements increase with impairment following stroke.

 

Honeycutt CF1, Perreault EJ2
  • 1Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, IL, USA. Electronic address: claire.honeycutt@gmail.com.
  • 2Sensory Motor Performance Program, Rehabilitation Institute of Chicago, Chicago, IL, USA; Department of Biomedical Engineering, Northwestern University, Evanston, IL, USA; Department of Physical Medicine and Rehabilitation, Northwestern University, Chicago, IL, USA.

 

Abstract

OBJECTIVE: The startle reflex elicits involuntary release of planned movements (startReact). Following stroke, startReact flexion movements are intact but startReact extension movements are impaired by task-inappropriate flexor activity impeding arm extension. Our objective was to quantify deficits in startReact elbow extension movements, particularly how these deficits are influenced by impairment.

METHODS: Data were collected in 8 stroke survivors performing elbow extension following two non-startling acoustic stimuli representing “get ready” and “go”, respectively. Randomly, the “go” was replaced with a startling acoustic stimulus. We hypothesized that task-inappropriate flexor activity originates from unsuppressed classic startle reflex. We expected that increasing damage to the cortex (increasing impairment) would relate to increasing task-inappropriate flexor activity causing poor elbow extension movement and target acquisition.

RESULTS: Task-inappropriate flexor activity increased with impairment resulting in larger flexion deflections away from the subjects’ intended target corresponding to decreased target acquisition.

CONCLUSIONS: We conclude that the task-inappropriate flexor activity likely results from cortical or corticospinal damage leading to an unsuppressed or hypermetric classic startle reflex that interrupts startReact elbow extension.

SIGNIFICANCE: Given startReact’s functional role in compensation during environmental disturbances, our results may have important implications for our understanding deficits in stroke survivor’s response to unexpected environmental disturbances.

Copyright © 2013 International Federation of Clinical Neurophysiology.

KEYWORDS: Reaching; StartReact; Startle; Stroke

PMID: 24411525

 

Supplemental information

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 startReact response is a new technique that has recently been implicated as a potential tool to evaluate motor planning. In the presence of a motor plan, a startling acoustic stimulus triggers the involuntary release of planned movement, a phenomenon referred to as startReact. StartReact is distinct from the classic startle reflex, which occurs in the absence of a motor plan and results in brief, synchronous firing of muscles throughout the body. Instead, these startReact movements release planned muscle activation patterns that are quantitatively indistinguishable from those elicited voluntarily, except that they are released 30-40ms earlier. What makes startReact attractive is its neural substrates. StartReact is mediated by the brainstem (e.g. reticular formation, reticulospinal tract) (Davis et al. 1982; Davis and Gendelman 1977; Honeycutt et al. 2013; Rothwell 2006; Yeomans and Frankland 1996) which is spared following majority of strokes in contrast with the significant damage to volitional pathways (e.g. cortex, corticospinal tract). StartReact allows us to evaluate motor planning when elicited through alternative, more intact structures giving a clearer picture of how motor planning is impacted by stroke.

 

fig 1

Figure 1: Depicts voluntary (left) and startReact (right) movements for both unimpaired (top) and stroke (bottom) subjects. Onset latencies are marked with a solid bar to highlight dierences in responses between voluntary and startReact [1]. Impairments in stroke voluntary movements are highlighted: 1) delay in voluntary onset latency (blue arrow) and 2) agonist/antagonist ring delay (red arrow).

The central hypothesis of our work is that stroke survivors retain the capacity to plan more functional movements than they can release voluntarily. Our recent work strongly supports this hypothesis. When startReact is utilized to initiate movement in stroke survivors, movements are initiated as rapidly as in unimpaired individuals and muscle coordination patterns are not statistically different between stroke and unimpaired (Honeycutt and Perreault 2012) (Figure 1). In other words, when a stroke survivor’s movement plan is accessed through startReact, we find that their movements approach unimpaired individuals’ movement. This is particularly striking given the differences in voluntary movements of these two groups (e.g. Figure 1: blue and red arrows). We find similar results in startReact hand extension (Honeycutt et al. 2014) indicating that startReact is accessible across the entire limb. These results are provocative indicating that stroke survivors can plan more appropriate movements than they can release voluntarily.

The paper highlighted here shows that there are deficits associated with the startReact response following stroke but that these deficits are not related to improper planning. Specifically, task-inappropriate flexor activity interrupts startReact elbow extension in stroke subjects. However, this inappropriate activity diminishes over time while the task-appropriate activity in the agonist muscle remains steady. This adaptation suggests that the inappropriate activity is transient in nature and not related to the underlying movement plan. We hypothesize that this activity results from an unsuppressed or hypermetric classic startle response. This is supported by our evidence that the task-inappropriate activity increased with cortical impairment.

Our future work will utilize the startReact response to further explore the capacity of stroke survivors to plan movement with the goal of developing training interventions specifically designed to maximize stroke survivors’ residual planning ability.

 

References:

  1. Davis M, Gendelman DS, Tischler MD, and Gendelman PM. A primary acoustic startle circuit: lesion and stimulation studies. J Neurosci 2: 791-805, 1982.
  2. Davis M, and Gendelman PM. Plasticity of the acoustic startle response in the acutely decerebrate rat. Journal of comparative and physiological psychology 91: 549-563, 1977.
  3. Honeycutt CF, Kharouta M, and Perreault EJ. Evidence for reticulospinal contributions to coordinated finger movements in humans. J Neurophysiol 110: 1476-1483, 2013.
  4. Honeycutt CF, and Perreault EJ. Planning of Ballistic Movement following Stroke: Insights from the Startle Reflex. PLoS ONE 7: e43097, 2012.
  5. Honeycutt CF, Tresch UA, and Perreault EJ. Startling acoustic stimuli can evoke fast hand extension movements in stroke survivors. Clin Neurophysiol 2014.
  6. Rothwell JC. The startle reflex, voluntary movement, and the reticulospinal tract. Supplements to clinical neurophysiology 58: 223-231, 2006.
  7. Yeomans JS, and Frankland PW. REVIEWS Review article The acoustic startle reflex : neurons and connections. Brain Research Reviews 21: 301-314, 1996.

 

Honeycutt Head ShotContact:

Claire Honeycutt, PhD

Assistant Professor

Ira A Fulton Schools of Engineering

Arizona State University

501 E Tyler Mall, Room 334, PO Box 879709, Tempe, Arizona 85287-9709

480-965-8453 (P)

claire.honeycutt@asu.edu

http://faculty.engineering.asu.edu/honeycutt/

 

 

 

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