To successfully conduct the neurological assessment, the clinician must understand what he or she is looking for. To do so, the clinician does not have to venture too far into the field of neurophysiology in which many lively debates occur in light of recent advances. Rather, a minimal background in the maturation and pathophysiology of muscle tone will allow the clinician to interpret his or her observations during the assessment. The clinician must also understand the importance of the cranial assessment, as cranial sutures and head circumference reflect both the increase in volume due to maturation and negative aspects associated with underlying brain damage. In this perspective, we propose a step by step approach, starting with a brief explanation of the neurophysiological mechanisms in motor activity followed by a functional analysis of motor pathways, all while accounting for maturation.
Medullar level: monosynaptic arc reflex
A motor unit refers to the α motoneuron located in the anterior horn of the spine and all the motor fibers it innervates. Muscle spindles are included in each motor unit, consisting of specialized fibers sensitive to muscle length. These intrafusal fibers are contained in a capsule and send information to the α motoneuron via afferences when the muscle stretches. The spindles sensitivity to stretch is regulated by γ motoneurons of the anterior horn that receive and send information to the spindles and thus maintain the effectiveness of the system according to the spindle’s preset length.
The whole set, including the spindle afferences, the α motoneuron and its efferent neuron towards the muscle, constitutes the monosynaptic reflex arc. The activation of this system by stretching the spindle causes myotatic reflex or stretch reflex.
When agonists contract, interneurons neighbouring the concerned α motoneuron send information towards α motoneurons of antagonist muscles that will then relax. This is the reciprocal inhibition phenomenon, which is essential to efficient movement.
To complete this rather reductionist description, we must add:
- The fact that there is, in addition to spindles, other mechanoreceptors attached to tendons (sending afferent fibers, always polysynaptic). All mechanoreceptors provide proprioceptive information that will ensure control of posture and movement.
- The fact that the response will vary according to the speed of stretching: if stretching is slow, spindles send a flight of afferences to the spinal cord, but the signal is asynchronous and intermittent. Spindles adapt quickly to their new length and resume there basic activity. If stretching is fast and instantaneous, all spindles (a few hundred) simultaneously send a strong and synchronous signal to the spine. This strong afference stimulates the α motoneuron from the anterior horn and muscle fibers. The result of this stimulation is a muscle contraction, clearly visible to the clinician.
- The fact that the density of muscle spindles is not uniform: it is rather high in postural muscles, such as the triceps surae.
Central control over the monosynaptic arc
Brain structures and descending motor pathways
In the absence of supraspinal control, the myotatic reflex caused by each sudden muscle stretch makes rapid movement impossible (active or passive). Therefore, the clinician must have a solid understanding of how the brain controls spinal activity to allow rapid movement. Supraspinal control has two levels:
- Brainstem and cerebellum level (also known as lower brain, the most archaic) generates subcorticospinal pathways including tracts from the tectum, tracts from the upper reticular formation upper (brain stem) and lower (bulbar), and tracts from the vestibular nuclei. All these tracts do not terminate directly at the α motoneuron in the anterior horn but at the interneurons. The lower system receives visual afferences through the tectospinal tract and vestibular afferences through the vestibulospinal tract. Finally, the cerebellum is connected to the lower system: it receives information from the spinal level and cortical level and transmits its messages through its connections with the brainstem. Together, all of these lower brain structures play a key role in the automatic control of posture and movement.
- Hemispheric level (also known as upper brain) generates corticospinal pathways. Axons of motor neurons in frontal areas 4 and 6 terminate directly on the α motoneurons of the anterior horn. The majority of fibers cross the midline at the bulbar pyramids, the corticospinal cross tract. A small portion, consisting in the direct corticospinal tract, is linked to the body axis. Finally, the corticobulbar tract reaches the cranial nerves.
The upper system also includes basal ganglia (caudate nucleus, putamen and globus pallidus) as well as the thalamus, the sensory relay. The basal ganglia receive information from most cortical areas and transmit it to the cortex after relay in the thalamus. This loop, called motor loop, plays a major role in the control of voluntary movements. Corticospinal downward paths go through a narrowed area in the posterior arch of the internal capsule; this area is particularly sensitive to hypoxia-ischemia.
Activation and inhibition in the CNS
Spinal activity is constantly monitored by the lower brain, while the upper brain is monitored by facilitating or inhibiting stimulations on the α motoneuron of the anterior horn. The hemispheric level moderates the excitatory activity of the underlying formations, especially the upper reticular formation and vestibular nuclei. This permanent control over the spinal cord, and consequently the monosynaptic reflex arc, modulates postural control and enables smooth and precise movements.
Relevance of this simplistic dichotomy for clinicians
- The lower system acts preferentially upon the antigravitic tone, including the extensor muscles of the axis and of the lower limbs, the flex tone of the upper and lower limbs, and primary reflexes.
- The upper system moderates the activity of the lower brain, therefore modulating antigravitic tone, relaxation of the flexor tone in limbs, and primary reflexes. This modulation acts on the quality of both gross and fine voluntary movements.
Some examples of clinical application
Based on these rudimentary concepts, the clinician can interpret the response of a tendon reflex, like the patellar reflex : the hammer hit on the patellar tendon causes a rapid and brief stretch of the quadricep muscle. The response is an abrupt contraction that moves the leg forward. It is a myotatic reflex caused by a muscle stretch. When supraspinal control is intact, the muscle contraction is brief and γ servocontrol allows the leg to return to the resting position. We will later address the excessive response when upper control is altered.
The clinician can also understand what muscle tone is : In the waking state, a muscle is never completely at rest. Thus, muscle tone said to be at rest is actually the result of a minimal contraction related to the state of mild excitation. Only during REM sleep, after curarisation or section of the posterior root this resting tone is suppressed, thus showing it depends on both peripheral and central influences. It is in this state of rest that passive muscle tone is explored. Slow passive segmental stretching by the assessor does not stimulate the spindles; it assesses the extensibility of the musculoligamentous system. The result of each maneuver is expressed either by an angle between two limb segments (the popliteal angle, for example), or in relation to an anatomical landmark (the elbow from the midline in the scarf sign maneuver, for example), or by the amplitude of a curve (in the trunk, for example). The rapid stretching maneuver allows the clinician to search for a possible dysfunctioning when the central control of the monosynaptic reflex arc is altered. In the case of a central originating pathology, spinal control is a priori normal; it is rather a supraspinal control dysfunctioning we are looking for.
- a brief one (section 2 in figure), called phasic, in which the resistance to stretch will release (the sequence “resistance release” resembles the closure of a pocket-knife).
- The other (section 3 in figure), more prolonged, called tonic, in which the resistance to stretching persists, thus preventing any quick passive mobilization, meaning that the segmental movement can only be continued slowly.
In both cases, the observed anomaly is speed-dependent and therefore qualified as spastic. Central control maturation Organization of motor pathways: maturation and function, interactions with other pathways
“Upper brain” and “lower brain” have different maturation regarding precocity, speed, and upward or downward direction. All of these features, joined with the functional specificity of the two systems is summarized in the illustration of postural tone during fetal life until the second year.
Maturation of the lower system (represented by letter A) shows how the righting reaction in the upright position develops in a caudo-cephalic manner between 28 and 40 weeks, due to the ascending maturation of corresponding bundles. Later on, from 32 weeks, maturation of the upper system (represented by letter B) will modulate the postural responses in a downward manner, allowing successively head control, sitting, then standing position, or in other words, acquisition of motor skills. From the age of approximately 3 months, the primary reflexes (under lower brain control) will be integrated through maturation of the higher system, meaning that they will essentially disappear for the clinician.
The following figure shows in parallel the evolution of passive muscle tone (assessed on posture and segmental extensibility in limbs) and active muscle tone in standing position. During the last weeks of fetal life (zone 1), flexor muscles tone first appears in the lower limbs, then a strong quadriflexion takes place around term, at 40 weeks, as shown in Zone 2 of the figure. In the first year of life (shown in area 3 of the figure), the passive tone is released from the top down under the influence of the higher brain, beginning at the upper limbs and then the lower limbs.
It may be noted that:
- The frog-like posture (upper limbs extended, lower limbs bent) is physiological during two periods, at 34 weeks in zone 1 and around 3-4 months postpartum in zone 3.
- The essential motor acquisitions of standing and walking (average 13 months) coincide with the period of maximum physiological hypotonia (8-15 months). Thus the evaluation can only be interpreted in regard to the age of the child. The gap between early maturation of the lower system and the late maturation of the upper one explains semiotics: unspecific at first then becoming more specific with the maturation of the upper system.
- Regarding the body axis tone, the clinician understands, due to the staggered maturation of both systems, that the predominance of the physiological antigravitic tone until the term is no longer in the early postnatal months: the predominance of extensor muscle tone therefore becomes one of the earliest signs of upper brain damage.
Understanding the lesional levels according to anatomophysiological data
Theoretical expectations in the neuromotor chapter are summarized according to the injury level
- Abnormal response to rapid stretch
- Clonus, meaning repeated contractions in response to an on-going stretch
- Hypertonia, meaning limited extensibility based on normal values for age
- Sharp deep tendon reflexes, polycinetic, diffused
An injury to the lower system leads, depending on the lesional level, either to rigidity (ongoing resistance to passive stretch, stiffness not speed dependent), or global hypotonia.
Abnormal movements grouped under the term dyskinesia reflect impairment of the basal ganglia and are most often associated with either spasticity or rigidity. Dystonia is often added to spasticity, due to the lack of inhibition in the spinal system. If reciprocal inhibition is altered, the co-contraction of agonists and antagonists parasite voluntary movement. Muscle weakness is always associated, with varying degrees, to the disorders mentioned above. For example, weakness is often more troublesome than spasticity itself in walking. Although rarely mentioned in early childhood because it is difficult to measure, it remains consistent with the use of the term cerebral palsy to refer to all motor disorders of central origin in young children. Finally, musculotendinous shortenings and secondary deformities due to tone disorders make it more difficult to detect spasticity and dystonia. The facts are actually more complex because of the immaturity of the brain during HI insult.
Two main conditions may be described:
- HI encephalopathy of the newborn at term
Lesions take place in the cortex and/or the white hemispheric matter, basal ganglia. The lesions are most often visible with conventional MRI; associated cognitive and sensory impairments, and even epilepsy, are frequent.
- The premature newborn encephalopathy
In premature infants, the lesions are mainly located in the periventricular white matter, due to elective sensitivity to hypoxia of immature oligodendrocytes. As mentioned previously, the posterior arm of the internal capsule is particularly vulnerable, explaining the classic condition of the premature infant with spastic diplegia almost always associated with impaired visual function. The typical image is that of a dilatation of the lateral ventricles secondary to atrophy of the periventricular white matter. However, the lesions are often more diffused: they affect as well the cortex, basal ganglia, thalamus and cerebellum. Finally, the more extreme prematurity (ELBV) is, the more disrupted the future child development will be. This disorganization is difficult to pinpoint with the neurological assessment during the first years of life. More complex imaging techniques are necessary to aid in their identification. Clinically, this disorganization will gradually be revealed in different areas of brain function.
In conclusion, pediatricians feel easily lost amongst those complex issues. Conflicts between specialists, the absence of consensus on definitions and the lack of an animal model lead to an uncomfortable clinical approach. These pathophysiological bases have been simplified to the extreme in order to increase the confidence of each clinician in their own diagnostic skills.
Consequences of CNS lesions on cranial growth
Cranial growth in the fetus and young child depends on two factors: the “active” growth (genetically programmed, which explains the relevance of measuring the head circumference of both parents) but also the “passive” growth, which allows the cranial vault to follow the tremendous expansion of the cerebral hemispheres. This passive growth, made possible by the architecture of the skull which consists of separated parts linked by membranous sutures, allows us to comprehend why the cephalic growth measure and palpation of sutures have neurological meaning.
All together the skull bones form a box that protects the CNS. Only the bones forming the cranial vault are palpable: the frontal bone (F) in front, the occipital bone (O) behind, the parietal (P) and temporal (T) bones laterally; the sphenoid and ethmoid, forming the anterior and middle base of the skull. Head circumference (HC) reflects brain growth. It is obtained by measuring the largest occipitofrontal circumference and then comparing the value obtained with measurement values from other children of the same age and gender on a growth curve. We add to this measure the clinical evaluation of cranial sutures. It is important to remember that the bones of the skull are not yet tightly fixed to one another in the neonate or young infant.
In the newborn, the edges of the bones are nearly straight, and membranous spaces are easily perceived with a finger. Most sutures will become indented, such as the sagittal suture between the two parietal bones, the coronal suture between the parietal and frontal bones, and the metopic suture between the left and right sides of the frontal bone. The suture between the parietal and temporal bones (seen above the ear) is called “squamous” because it is not indented but bevelled.
Sutures ossify progressively and very slowly until about 3 years, in the following order: first metopic, then sagittal, coronal, lambdoid and finally squamous. Until then, and especially during the perinatal period, the mobility of the skull bones is such that the distention of sutures allows an increase of skull volume in cases of intracranial hyper-pressure, and is easily perceived with a finger as a membranous space between two flat bones.
The identification of these distension and overlapping phenomena enriches the simple measurement of head circumference and palpation of fontanels.