Obstacle stepping involves spinal anticipatory activity associated with quadrupedal limb coordination

Obstacle avoidance steps are associated with a facilitation of spinal reflexes in leg muscles. Here we have examined the involvement of both leg and arm muscles. Subjects walking with reduced vision on a treadmill were acoustically informed about an approaching obstacle and received feedback about task performance. Reflex responses evoked by tibial nerve stimulation were observed in all arm and leg muscles examined in this study. They were enhanced before the execution of obstacle avoidance compared with normal steps and showed an exponential adaptation in contralateral arm flexor muscles corresponding to the improvement of task performance. This enhancement was absent when the body was partially supported during the task. During the execution of obstacle steps, electromyographic activity in the arm muscles mimicked the preceding reflex behaviour with respect to enhancement and adaptation. Our results demonstrate an anticipatory quadrupedal limb coordination with an involvement of proximal arm muscles in the acquisition and performance of this precision locomotor task. This is presumably achieved by an up-regulated activity of coupled cervico-thoracal interneuronal circuits.     

Neuronal coordination of arm and leg movements during human locomotion

We aimed to study the neuronal coordination of lower and upper limb muscles. We therefore evaluated the effect of small leg displacements during gait on leg and arm muscle electromyographic (EMG) activity in walking humans. During walking on a split-belt treadmill (velocity 3.5 km/h), short accelerations or decelerations were randomly applied to the right belt during the mid or end stance phase. Alternatively, trains of electrical stimuli were delivered to the right distal tibial nerve. The EMG activity of the tibialis anterior (TA), gastrocnemius medialis (GM), deltoideus (Delt), triceps (Tric) and biceps brachii (Bic) of both sides was analysed. For comparison, impulses were also applied during standing and sitting. The displacements were followed by specific patterns of right leg and bilateral arm muscle EMG responses. Most arm muscle responses appeared with a short latency (65-80 ms) and were larger in Delt and Tric than in Bic. They were strongest when deceleration impulses were released during mid stance, associated with a right compensatory TA response. A similar response pattern in arm muscles was obtained following tibial nerve stimulation. The arm muscle responses were small or absent when stimuli were applied during standing or sitting. The arm muscle responses correlated more closely with the compensatory TA than with the compensatory GM responses. The amplitude of the responses in most arm muscles correlated closely with the background EMG activity of the respective arm muscle. The observations suggest the existence of a task-dependent, flexible neuronal coupling between lower and upper limb muscles. The stronger impact of leg flexors in this interlimb coordination indicates that the neuronal control of leg flexor and extensor muscles is differentially interconnected during locomotion. The results are compatible with the assumption that the proximal arm muscle responses are associated with the swinging of the arms during gait, as a residual function of quadrupedal locomotion.     

Quadrupedal coordination of bipedal gait: implications for movement disorders

During recent years, evidence has come up that bipedal locomotion is based on a quadrupedal limb coordination. A task-dependent neuronal coupling of upper and lower limbs allows one to involve the arms during gait but to uncouple this connection during voluntarily guided arm/hand movements. Hence, despite the evolution of a strong cortico-spinal control of hand/arm movements in humans, a quadrupedal limb coordination persists during locomotion. This has consequences for the limb coordination in movement disorders such as in Parkinson’s disease (PD) and after stroke. In patients suffering PD, the quadrupedal coordination of gait is basically preserved. The activation of upper limb muscles during locomotion is strong, similar as in age-matched healthy subjects although arm swing is reduced. This suggests a contribution of biomechanical constraints to immobility. In post-stroke subjects a close interactions between unaffected and affected sides with an impaired processing of afferent input takes place. An afferent volley applied to a leg nerve of the unaffected leg leads to a normal reflex activation of proximal arm muscles of both sides. In contrast, when the nerve of the affected leg was stimulated, neither on the affected nor in the unaffected arm muscles EMG responses appear. Muscle activation on the affected arm becomes normalized by influences of the unaffected side during locomotion. These observations have consequences for the rehabilitation of patients suffering movement disorders.     

The numbers and relative sizes of motor units estimated by computer.

A fully automated system is described for estimating the numbers and relative sizes of functioning motor units in proximal and distal muscles of the arm and leg. In this system, a computer controls the motor nerve stimulation, and analyzes the potentials evoked from the muscles; a subprogram searches for instances of "alternation." In 33 healthy volunteers, aged 21 to 56 years, the median-innervated thenar muscles of one hand were tested 2 to 3 times; the mean motor unit estimate was 228 +/- 93 SD. For similar numbers of biceps brachii, extensor digitorum brevis, and vastus medialis muscles, the respective mean values were 113 +/- 40, 131 +/- 45, and 229 +/- 108 units. The reproducibility of the method was such that the overall coefficient of variation, for the normalized results from the 121 muscles studied, was 22%. The reliability of the automated method was doubled if 3 estimates, rather than one, were performed on each muscle. Comparisons of the results obtained by automated and "manual" methods indicated that the computer-derived values tended to be lower by approximately 33%.     

A case of brachial plexus neuropathy who presented with acute paralysis of the hand after sleep]

We report a 46-year-old woman who presented with acute paresis of the right hand and arm. She was well until when she noted a paresis and dysesthesia in her right hand in the morning. Neurological examination revealed weakness in the muscles which were supplied by lower cervical segments, with increased deep tendon reflexes in the right arm. Allen's test and Wright's test were positive. The nerve conduction studies disclosed a reduced CMAPs more severely by right median than ulnar nerve stimulation. The frequency and amplitude of the F waves was also reduced. Needle electromyogram showed a mild neurogenic pattern in the right hand muscles. Digital subtraction angiography revealed a tapering of the subclavian artery when the right arm was abducted. She underwent decompression surgery. A remarkable improvement of the symptoms was observed after surgery. Our patient suggests that brachial plexus neuropathy should be considered in the acute paresis of the hand after sleep, and that surgical procedure would lead to a successful outcome.     

The breathing hand: obstetric brachial plexopathy reinnervation from thoracic roots?

It has been found that in cases of obstetric brachial plexopathy, injured phrenic nerve or C3/4/5 roots may sprout into the adjacent injured upper and middle trunks of the brachial plexus. This aberrant regeneration produces co-contraction of the diaphragm and proximal upper limb muscles. This phenomenon, referred to as respiratory synkinesis or "the breathing arm", may not be limited to the upper cervical roots. We present two cases, identified through electromyographic investigations, of respiratory synkinesis selectively affecting intrinsic hand muscles, and propose that upper thoracic roots and their intercostal nerves may also produce respiratory synkinesis, resulting in a "breathing hand." This novel brand of synkinesis indicates that obstetric brachial plexus neuropathies can have quite proximal nerve injury in all trunks. The findings in our patients may not be entirely unique. The time required to develop distal muscle synkinesis and the subtle nature of our findings may suggest that with time and the assistance of EMG the breathing hand may be more common. When considering brachial plexus surgery, the significance of respiratory synkinesis should not be overlooked as its presence indicates injury at a root or proximal trunk level and may come from either nerves destined for the diaphragm or for the intercostal muscles.     

Diagnostic importance of somatosensory evoked potentials in the diagnosis of thoracic outlet syndrome

Somatosensory evoked potentials (SEPs) after stimulation of median and ulnar nerves were analyzed retrospectively in a group of 14 patients presenting with rudimentary cervical ribs or ill-healed clavicular fractures, where clinically the possibility of thoracic outlet syndrome was raised. In 5 patients who presented with pain in the arm and hypoesthesia along the ulnar border of the forearm without weakness and wasting in the muscles supplied by the lower trunk of the brachial plexus, the SEPs after both median and ulnar nerve stimulation were normal. In the second group of 9 patients there was weakness and wasting of the lower trunk-supplied muscles. All these patients were treated surgically by excision of abnormal tissues; all of them improved subjectively, and most of them improved strength in the previously affected muscles. SEPs in this group recorded preoperatively showed normal findings after median nerve stimulation, while the potentials after stimulation of ulnar nerve were always abnormal from the affected arm, being delayed, attenuated or even absent at Erb's point, cervical spinal cord and contralateral scalp. The results of this study, which were based on 314 investigations performed in patients with different lesions of the brachial plexus, suggest that abnormal ulnar nerve SEPs in the presence of normal median nerve SEPs are supportive means in the diagnosis of thoracic outlet syndrome, where nervous structures have been endangered. This is in accordance with the most recent reports in the literature.     

Modulations of interlimb and intralimb cutaneous reflexes during simultaneous arm and leg cycling in humans.

OBJECTIVE: We investigated to what extent intralimb and interlimb cutaneous reflexes are altered while simultaneously performing arm and leg cycling (AL cycling) under different kinematic and postural conditions. METHODS: Eleven subjects performed AL cycling under conditions in which the arm and leg crank ipsilateral to the stimulation side were moved synchronously (in-phase cycling) or asynchronously (anti-phase cycling) while sitting or standing. Cutaneous reflexes following superficial radial or superficial peroneal nerve stimulation (2.0-2.5 times radiating threshold, 5 pulses at 333 Hz) were recorded at 4 different pedal positions from 12 muscles in the upper and lower limbs. Cutaneous reflexes with a peak latency of 80-120 ms were then analyzed. RESULTS: The magnitude of interlimb and intralimb cutaneous reflexes in the arm and leg muscles was significantly modulated depending on the crank position for the relevant limb (phase-dependent modulation). A significant correlation between the magnitude of the cutaneous reflex and background EMG was observed in the majority of muscles during static contraction, but not during AL cycling (task-dependent modulation). No significant difference was found in comparisons of the magnitude of intralimb and interlimb cutaneous reflexes obtained during in- and anti-phase AL cycling. Qualitatively, the same results were obtained during AL cycling while sitting or standing. In addition, the modulation of cutaneous reflexes in arm muscles was identical among in-phase, anti-phase and isolated arm cycling. Results were the same for leg muscles. CONCLUSIONS: Cutaneous reflexes in arm muscles are little influenced by rhythmic movement of the legs and vice versa during AL cycling. It is likely that neural components that control interlimb reflexes are loosely coupled during AL cycling while sitting or standing. SIGNIFICANCE: Our results provide a better understanding of the coordination between the upper and lower limbs during rhythmic movement.     

Obstacle avoidance locomotor tasks: adaptation, memory and skill transfer

The aim of this study was to explore the neural basis of adaptation, memory and skill transfer during human stepping over obstacles. Whilst walking on a treadmill, subjects had to perform uni- and bilateral obstacle steps. Acoustic feedback information about foot clearance was provided. Non-noxious electrical stimuli were applied to the right tibial nerve during the mid-stance phase of the right leg, i.e. 'prior' to the right or 'during' the left leg swing over the obstacle. The electromyogram (EMG) responses evoked by these stimuli in arm and leg muscles are known to reflect the neural coordination during normal and obstacle steps. The leading and trailing legs rapidly adapted foot clearance during obstacle steps with small further changes when the same obstacle condition was repeated. This adaptation was associated with a corresponding decrease in arm and leg muscle reflex EMG responses. Arm (but not leg) muscle EMG responses were greater when the stimulus was applied 'during' obstacle crossing by the left leg leading compared with stimulation 'prior' to right leg swing over the obstacle. A corresponding difference existed in arm muscle background EMG. The results indicate that, firstly, the somatosensory information gained by the performance and adaptation of uni- and bilateral obstacle stepping becomes transferred to the trailing leg in a context-specific manner. Secondly, EMG activity in arm and leg muscles parallels biomechanical adaptation of foot clearance. Thirdly, a consistently high EMG activity in the arm muscles during swing over the obstacle is required for equilibrium control. Thus, such a precision locomotor task is achieved by a context-specific, coordinated activation of arm and leg muscles for performance and equilibrium control that includes adaptation, memory and skill transfer.     

Cutaneous nerve stimulation and motoneuronal excitability. II: Evidence for non-segmental influences.

After stimulation of a sensory nerve, even distant motor nuclei undergo excitability changes which are evidenced by recovery curves. In all, two unequal peaks of facilitation can be identified. They appear when a given motor nucleus is tested after stimulation of various sensory nerves or when the same stimulation (of the sural nerve) is studied in various motor nuclei. The first facilitation is seen earlier in the masseter, then in the arm muscles and finally in lower limb muscles. The existence of a supraspinal centre activated by low threshold exteroceptive afferents and facilitating motor nuclei in a rostro-caudal sequence is postulated to account for certain features of the first and second peaks of facilitation.     

Hereditary neuropathy with liability to pressure palsy: the electrophysiology fits the name

BACKGROUND: Studies of patients with hereditary neuropathy with liability to pressure palsies (HNPP) have shown accentuated distal slowing along with nonuniform conduction abnormalities at segments liable to compression, suggesting a distal myelinopathy as an underlying pathophysiological mechanism. METHODS: We evaluated 12 patients with HNPP by standard nerve conduction studies and by conduction to more proximal muscles in the arm and leg. Three CMT1A patients and six healthy subjects also were evaluated as controls. RESULTS: Median and peroneal motor nerves in all HNPP patients showed prolonged distal motor latencies (DML) (mean +/- SE, 5.9 +/- 0.41 and 8.63 +/- 0.58 milliseconds), but the ulnar and tibial DML were minimally prolonged or normal (mean +/- SE, 3.87 +/- 0.16 and 5.66 +/- 0.24 milliseconds). DML to forearm flexor (median and ulnar nerves) or anterior tibial muscles (peroneal nerve) were also normal. CONCLUSION: Accentuated distal slowing is found primarily in median and peroneal nerve segments liable to pressure palsies or repetitive trauma. However, the ulnar and tibial nerves, which are less liable to compression, have minimal changes. In addition, distal latencies to more proximal muscles in the arm and leg do not have distal slowing. These findings do not support a distal myelinopathy as a determinant of the conduction abnormalities in HNPP.     

Normal median nerve proximal latency in carpal tunnel syndrome: a clue to coexisting Martin-Gruber anastomosis.

Five of 65 patients referred for electrodiagnosis because of clinical evidence of carpal tunnel syndrome were found to have near normal latency on proximal stimulation of the median nerve, although the distal motor latency was prolonged. In one patient, the proximal latency was actually shorter than the distal latency. The failure of the proximal latency to be prolonged in proportion to the distal latency results in a spuriously high apparent conduction velocity in the forearm segment of the nerve. This value may even exceed the conduction velocity of the corresponding nerve segment in the unaffected arm. Stimulation studies on the ulnar nerve reveal that this disparity is the result of some of the median nerve fibres destined for the thenar muscles taking an aberrant course through the ulnar nerve and thus escaping compression at the wrist. A median-ulnar communication in the forearm, the 'Martin-Gruber' anastomosis, may occur in up to 15% of the population. The presence of the Martin-Gruber anastomosis in patients with carpal tunnel syndrome results in a partial or total sparing of thenar muscles from denervation and the paradoxical recording of normal proximal latencies in the median nerve when the distal latency is prolonged.     

Central motor reorganization after anastomosis of the musculocutaneous and intercostal nerves following cervical root avulsion

In 4 patients with a complete upper limb palsy due to traumatic cervical root avulsion, surgical anastomosis of intercostal to musculocutaneous nerves was performed to restore function in the biceps brachii muscle. Four to 6 months after the operation, motor unit discharges were recorded from the biceps muscle on the operated side during deep breathing and by cortical magnetic stimulation. The motor unit discharges became independent from respirations gradually over 1 to 2 years. The latencies of the motor potentials evoked by cortical and thoracic root magnetic stimulation decreased gradually over 2 to 3 years. Motor cortex mapping of the reinnervated biceps muscle showed a gradual change over 4 to 33 months from the area of the intercostal muscles to that of the arm area, which was more lateral on the motor cortex. These findings suggest that reorganization of the motor cortex to arm flexor muscles occurs following peripheral nerve anastomosis.     

Denervation and reinnervation in congenital brachial palsy.

Motor unit number estimation (MUNE) was shown to be useful in assessing the neurophysiological status of 18 subjects with congenital brachial palsy. This was especially so since conventional M-wave measurements may give misleading impressions as to the extent of motor axon regeneration. In most subjects the involvement of sensory nerve fibers indicated that the traumatic lesions included postganglionic segments of the fibers, with or without preganglionic damage. In a minority the lesions were purely preganglionic. Digital sensory nerve involvement was more in a mediolateral direction, consistent with greater damage to the uppermost elements in the brachial plexus. In 5 individuals, MUNE and sensory testing showed that there had been trauma to the supposedly unaffected arm. Discrepancies between sensory and motor results suggested that reinnervation of the biceps brachii muscle was greater than that of the intrinsic muscles of the hand. In one subject examined serially, reinnervation of the hand muscles was detected by 10 months and continued in the hypothenar muscles for the next 6 years.     

Sensory afferent inhibition within and between limbs in humans

ObjectiveTo examine the distribution and inter-limb interaction of short-latency afferent inhibition (SAI) in the arm and leg.MethodsMotor evoked potentials (MEPs) in distal and proximal arm, shoulder and leg muscles induced with ranscranial magnetic stimulation (TMS) were conditioned by painless electrical stimuli applied to the index finger (D2) and great toe (T1) at interstimulus intervals (ISIs) of 15, 25–35, 80 ms (D2) and 35, 45, 55, 65 and 100 ms (T1) in 27 healthy human subjects. TMS was delivered over primary motor cortex (M1) arm and leg areas. Electrical stimulus intensities were varied between 1 and 3 times the sensory perception thresholds. We also tested effects of posterior cutaneous brachial nerve (PCBN) stimulation on MEPs in arm muscles at ISIs of 18 and 28 ms.ResultsD2 but not PCBN electrical conditioning reduced MEP amplitudes in upper limb muscles at ISIs of 25 and 35 ms. SAI was more pronounced in distal as compared to proximal arm muscles. Also, SAI following D2 stimulation increased with higher conditioning intensities. D2 stimulation did not change lower limb muscles MEPs. In ontrast, T1 stimulation did not induce SAI in any muscles but caused MEP facilitation in a foot muscle at an ISI of 55 ms and in upper limb muscles at ISIs of 35 and 55 ms. Short interval intracortical inhibition (SICI) and intracortical facilitation (ICF) were not affected by electrical T1 conditioning.ConclusionD2 stimulation causes segmental SAI in upper limb muscles with a distal to proximal attenuation without affecting leg muscles. In contrast, toe stimulation facilitates motor output both in foot and upper arm muscles.SignificanceOur data suggest that cutaneo-motor pathways in arms and legs are functionally organized in a different way with cutaneo-motor interactions induced by toe stimulation probably relayed at a thalamic level. Abnormal cutaneo-motor interactions following electrical toe stimulation may serve as an electrophysiological marker of thalamic dysfunction, e.g. in neurodegenerative diseases.     

Postural adjustments associated with rapid voluntary arm movements 1. Electromyographic data.

Normal subjects made bilaterally symmetric rapid elbow flexions or extensions ("focal movement") while free standing or when supported by being strapped to a firm wall behind them (different "postural set"). In some trials a load opposed the movement two thirds of the way into its course. Electromyographic activity in leg and trunk muscles ("associated postural adjustments") demonstrated specific patterns for each type of movement. Activity in these muscles began prior to activity in the arm muscles and demonstrated a distal-to-proximal order of activation. The EMG patterns were characterised by alternating activity in the antagonist pairs similar to the triphasic pattern seen in the arm muscles. When the movement type was changed change of the pattern of the postural muscles occurred over several trials. It is concluded that the associated postural adjustments are pre-programmed motor activity linked to the focal movement, specific for the focal movement including anticipated events and the postural set.     

Multiple oscillators are causing parkinsonian and essential tremor.

The tremors of Parkinson's disease (PD) and essential tremor (ET) are traditionally considered to depend on a central oscillator producing rhythmic activation of the motoneurones of all extremities. To test this hypothesis, we have compared electromyographic tremor activity in different muscles of the affected limbs using cross spectral analysis, including coherence and phase. Surface electromyographic recordings from both arms, legs, and the neck were analyzed in 22 patients with PD and 28 patients with ET. Volume conduction between neighboring muscles producing artificial "coherence" has been found to be an important methodologic problem. We have developed a mathematical test to exclude data that could distort the results. According to this test, 10% or 25% of muscle combinations from the same limb had to be excluded from further analysis in PD or ET, respectively. In both, patients with PD and ET, we found a considerable number of muscle combinations oscillating at virtually the same frequency (delta frequency <0.4 Hz) without showing a significant coherence. Thus, the frequency difference between different muscles is not sufficient to measure the correlation between two muscles. Significant coherencies between muscles within the same arm or leg were found in 70% or 90% of patients with PD or ET, respectively, whereas only one patient with PD and not a single patient with ET showed significant coherencies between muscles from different limbs. The phase between coherent muscles of the same arm of patients with PD showed a preference of either a reciprocal alternating pattern for antagonistic muscles in forearm flexor and upper arm extensor as opposed to a co-contraction pattern between the hand flexors and the triceps brachii. In patients with ET such clear differences were lacking. We conclude that multiple oscillators are responsible for the tremor in different extremities of patients with PD and ET. Differences between PD and ET concerning the phase relation within the arm may either be related to the topography within the basal ganglia or to differently involved-spinal pathways.     

Functional recovery in primates with brachial plexus injury after spinal cord implantation of avulsed ventral roots.

Intraspinal replantation of avulsed spinal nerve roots as a surgical treatment for motor deficits after severe brachial plexus injury was investigated in primates. Under general anaesthesia hemi-laminectomy was performed in cynomolgus monkeys (Macaca fascicularis). Ventral roots within the brachial plexus were then avulsed by traction and subsequently implanted into the ventrolateral aspect of the spinal cord. No dysfunction in the long fibre tracts was seen following surgery. Postoperatively there was a flaccid paralysis of the arm on the lesioned side. Severe atrophy developed within 5-7 weeks in the muscles supplied by the avulsed roots and EMG revealed denervation activity. Two to three months after surgery there were EMG signs of reinnervation, which were shortly followed by evidence of clinical recovery. A gradual improvement in the function of the affected arm occurred and the animals' motor behaviour normalised. One year after surgery there was a full range of motion in the arm, but the EMG activity in the reinnervated muscles at maximal force was reduced. Tracing of regenerated motor neurons with horseradish peroxidase (HRP) injected into the biceps muscle revealed retrogradely labelled motor neurons confined to the ipsilateral ventral horn. It was concluded that intraspinal replantation of avulsed ventral roots in primates significantly promotes motor recovery in the muscles supplied by the lesioned spinal cord segments.     

Motor reflex responses elicited by cutaneous stimulation in the regenerating nerve of man: Axon reflex or ephaptic response?

In 57 of 60 nerves (29 median and 31 ulnar) sutured at the wrist, forearm and arm, we recorded motor responses in thenar or hypothenar muscles by electrical stimulation of the corresponding fingers. Recordings were made at different times during the process of regeneration, ranging from 3 months up to 11 years. The responses showed a constant shape and latency to every stimulation (simple or repetitive). The latency was shorter the more distal the level of injury and the greater the elapsed time from the reinnervation. The point of "reflexion" of the responses is at or very near the line of nerve suture. The electrophysiological behavior of the responses fits well with either the criterion of axon reflex or ephaptic response. We discuss both possibilities and conclude that it is not possible, with the electrophysiological technique that we used, to distinguish between an axon reflex and an ephaptic response.     

Vascular and electromyographic responses evoked in forearm muscle by isometric contraction of the contralateral forearm

There is controversy over whether isometric contraction of the forearm evokes vasoconstriction or vasodilatation in the muscles of the contralateral forearm. In the present study we have investigated in normal man, the effects of isometric contraction of one arm at 75, 50 and 25% maximum voluntary contraction (MVC) on arterial pressure, heart rate, blood flow and vascular resistance of the contralateral forearm and on electromyographic (EMG) activity recorded from that same arm with sensitive, surface electrodes.When EMG activity was not being recorded from the resting arm, isometric contraction of the contralateral arm for 2 min evoked increases in arterial pressure and heart rate whose magnitudes were graded with % MVC and an increase in forearm blood flow and a decrease in forearm vascular resistance at 75, 50 and 25% MVC, indicating vasodilatation. Further experiments in which EMG activity was recorded from the resting arm demonstrated that the decrease in forearm vascular resistance evoked by 75% MVC was associated with a substantial increase in EMG activity of the extensor and flexor muscles of that arm. By contrast, when forearm contraction was performed at 75% MVC whilst subjects viewed the EMG activity in the resting arm on an oscilloscope and kept EMG activity minimal, vascular resistance increased in that arm, indicating vasoconstriction. Further, when subjects performed contraction at 25% MVC whilst showing minimal EMG activity in the contralateral arm, vascular resistance in that same arm increased (from 78 ± 16 to 124 ± 29 mmHg/ml/min/100 ml tissue). These results are discussed in relation to those of previous studies. We propose, that in normal man, isometric contraction of the forearm evokes primary vasoconstriction in the muscles of the contralateral forearm, but that this response may be overcome by muscle vasodilatation occurring secondary to unintended muscle contraction or as part of the alerting response to acute stress.