A built-in reaction to stimuli that is automatic and beyond a newborns control is called a

Tonic Neck Reflexes

The asymmetric reflex is elicited with the baby supine (Fig. 3.48). The examiner turns the baby’s head all the way to one side, holds that position for 10 seconds, and then turns the head to the other side. The baby responds by extending the arm and leg on that side and flexing the arm and leg on the other side. The position of the arm and leg are referred to as the “fencer’s position.” Absence of the reflex suggests a flaccid disorder or hypotonicity. The reflex should resolve by 4 to 6 months and persistence suggests hypertonicity or cerebral palsy. It may also be abnormal if it occurs every time the baby’s head is turned (seeFig. 3.48).

The symmetric tonic neck reflex is performed with the child held prone over the examiner’s knees. When the head and neck are extended, the arms extend and the lower extremities flex. Then the head and neck are flexed, the arms flex, and the lower extremities extend. The reflex does not appear until 5 to 8 months of age and usually goes away by 12 months of age (Fig. 3.49).

Parachute reflex: For this reflex the baby is held prone, then suddenly tilted downward and moved quickly toward the table or floor (Fig. 3.50). A positive response is to extend the arms and wrists as if to protect the head from a fall. In the sitting or standing position the reflex is elicited by tilting or pushing the child backward with enough force to push the child off balance. The positive response is a backward extension of both arms with the fingers extended and abducted and the weight born on the hands. The response does not depend on vision. The reflex should appear at approximately 6 months of age and remain throughout life. Absence of the reflex indicates significant neurologic dysfunction.

C Coordination of Head, Body, and Limbs

Limb movements are dependent on or covary with head position, as becomes evident in labyrinthine reflexes and symmetric and asymmetric tonic neck reflexes. These reflexes often interact with each other during movement production. For example, head dorsiflexion induces extension of the forelimbs and flexion of the hindlimbs, whereas the opposite effect occurs during ventriflexion (symmetric tonic neck reflex). The neck reflexes can be observed in the newborn but gradually disappear during the first months of life. However, some have argued that such reflexes do not fully disappear and may show up during the production of movements in sports events or other voluntary activities (Keele, 1981). Fukuda (1961) captured many skilled performers on film and found various patterns of limb coordination that are congruent with those found in the tonic neck reflexes. In addition, Hellebrandt, Houtz, Partridge, and Walters (1956) underscored the role of reflexes during the production of forceful events and demonstrated that patterns in accordance with these reflexes augment work output. It is thus reasonable to assume that some patterns of coordination are built into the organism and become subsequently integrated into voluntary activities. Coaches are aware of the important role of head position during skill acquisition. Instructions often relate to particular head movements (look at the floor during a handstand) in order to promote these built-in patterns of activity. Sometimes, these patterns are conducive to the new coordination form to be acquired; at other times, they may impose persistent errors in performance that need to be suppressed (Walter & Swinnen, Chapter 23, this volume). More will be said about the two faces of preexisting coordination modes later in this chapter.

In their chapter on head an body coordination, Berthoz and Pozzo argue that the head serves as an important frame of reference during multilimb coordination (Chapter 7). Depending on the type of activity to be executed, the head is stabilized intermittently under the control of gaze. This stabilization allows the head to serve as an inertial guidance platform for the control of multilimb movement. They infer this from the strong tendency of performers to stabilize the head with respect to the sagittal as well as the frontal plane. Head stabilization may simplify the transformations necessary to set up a coherent internal representation of external space. During various types of walking, head angular displacement in the sagittal plane remains within a small range when compared with the movements of the other limbs. When trunk movements are limited, the head is locked onto the trunk. During complex balancing tasks (standing on a narrow beam or on a semicircular platform), the head is again stabilized whereas the trunk is making the compensatory movements. A remarkable stabilization of the head in the frontal plane can also be observed during downhill skiing.

Primitive Reflexes

Primitive reflexes appear and disappear at specific times during development (Table 608.2), and their absence or persistence beyond those times signifies CNS dysfunction. Although many primitive reflexes have been described, the Moro, grasp, tonic neck, and parachute reflexes are the most clinically relevant. TheMoro reflex is elicited by supporting the infant in a semierect position and then allowing the infant's head to fall backward onto the examiner's hand. A normal response consists of symmetric extension and abduction of the fingers and upper extremities, followed by flexion of the upper extremities and an audible cry. An asymmetric response can signify a fractured clavicle, brachial plexus injury, or hemiparesis. Absence of the Moro reflex in a term newborn is ominous, suggesting significant dysfunction of the CNS. Thegrasp response is elicited by placing a finger in the open palm of each hand; by 37 wk of gestation, the reflex is strong enough that the examiner can lift the infant from the bed with gentle traction. Thetonic neck reflex is produced by manually rotating the infant's head to one side and observing for the characteristic fencing posture (extension of the arm on the side to which the face is rotated and flexion of the contralateral arm). An obligatory tonic neck response, in which the infant becomes stuck in the fencing posture, is always abnormal and implies a CNS disorder. Theparachute reflex, which occurs in slightly older infants, can be evoked by holding the infant's trunk and then suddenly lowering the infant as if he or she were falling. The arms will spontaneously extend to break the infant's fall, making this reflex a prerequisite to walking.

Fine Motor Development

It is in large part through motor acts that infants develop and express perception, emotion, and cognition. Between 2 and 3 months of age, the weakening of the obligatory asymmetric tonic neck reflex and expansion of accommodative abilities permit infants to look at their hands and touch one hand with the other. By furnishing simultaneous information to the senses of vision and touch, this mutual hand grasp provides a foundation for later visual motor skills. During the third month of life, as the world of close proximity comes into focus, infants begin swiping at objects with loosely fisted hands. At this stage, infants swipe with one hand only at objects in front of one shoulder or the other. By 6 months of age, they reach persistently toward objects in the midline, at first with both hands and then with one.

Between 3 and 6 months of age, the coordination of grasping and reaching gradually comes under visual guidance and voluntary control. During early reaching efforts, grasping may occur, but only after the hand has contacted the object. After 6 months of age, infants begin to shape their hands for grasping in the horizontal or vertical plane of the desired object immediately before touching it. By 9 months of age, shaping of the hand occurs before the object is reached. At 1 year old, children orient the hand in the appropriate plane when starting to reach for an object (Twitchell, 1965).

When the infant can reliably obtain an object, clumsy whole-hand grasping becomes progressively refined. At 4 months of age, the infant holds an object between fingers and palm; at 5 months of age, the thumb becomes involved. By 7 months of age, thumb and fingers can grasp and retain an object without resting on the palm at all. At this time, the infant uses a raking motion between the thumb and several fingers to scoop up small objects. By 9 months of age, the infant manipulates small objects with a neat pincer grasp, using thumb and forefinger perpendicular to the surface. Every nook and cranny is now accessible to the infant's exploration. During the second year of life, toddlers develop a palmar grasp and wrist supination that permits them to use tools such as spoons and pencils.

Diagnostic Decisions

Patients often present with descriptions of symptoms such as chest pain. Cues are scattered, like pieces of a jigsaw puzzle. Clinicians, as with all decision makers, often use mental shortcuts calledheuristics to organize cues and to turn an unstructured problem into a set of structured decisions.10,11 They are taught to collect the scattered cues of an unstructured clinical problem by using an organized history and physical examination.12-14 Clinicians are able to reason by analogy by comparing a patient's narrative to prototypic descriptions of diseases. When experts take a history, they use a process known as “early hypothesis generation” to develop a list of three to five possible diagnoses very early in the process.15 This enables the questioning to become more direct and the clinician to become more engaged in the fact-finding exercise.

After collecting, sorting, and organizing data, clinicians often use a problem list as a tool to list, group, and prioritize clinical findings. With additional information, aproblem statement can be defined more specifically. For example, “shortness of breath” may be an initial problem statement that is replaced by “acute systolic heart failure,” as further clinical information leads to a more refined problem statement that moves from symptom to diagnosis. Clinicians then use a differential diagnosis to expand the list of possibilities to avoid premature closure of the search for the true diagnosis. This step-by-step process enables the clinician to formulate a set of hypothetical diagnostic possibilities, which can then be tested using iterative hypothesis testing.Iterative hypothesis testing allows the clinician to narrow the list of possible diagnoses and hone in on the most plausible hypothesis.1-3

Understandingprobability is essential for clinical decision making.1-3,16 Probability can be estimated for outcomes that are measured as continuous or categorical variables.Fig. 3.1 shows how probability of an outcome or event is distributed across a range of possibilities. For example, a laboratory test might be measured in a population of patients resulting in a distribution where most patients are distributed to the middle of the range of possibilities and fewer scatter to the edges of the range, as shown in the probability density curve in the left panel ofFig. 3.1. The probability of categories or discrete variables can also be measured, as shown in the probability distribution graph in the right panel. If all the diagnostic possibilities are mutually exclusive and collectively exhaustive, the probability of all of the possibilities will add up to 1, as shown by the red cumulative probability curves inFig. 3.1. Understanding cumulative probability is important for understanding sensitivity and specificity, as discussed later.

To test a diagnostic hypothesis, we useconditional probability, which is the probability that something will happen, on the condition that something else happened. Conditional probability can tell us the probability of a diagnosis, on the condition of some new information, such as a positive test result. Bayesian reasoning enables us to form a probability estimate and revise that estimate based on new information using conditional probability. For example, a clinician might ask, What is the probability of coronary artery disease in my patient, given a positive stress echocardiogram? What is the probability of pulmonary embolus, given a negative D-dimer test? What is the probability of an acute coronary syndrome, given an abnormal troponin test? The post-test probability depends on a prior estimate of the probability for that particular patient, combined with the strength of the test result. Probability theory helps us understand the question and calculate the answer.

Bayesian reasoning requires both a prior estimate of probability and an estimate of the strength of a test result. Prior estimates can come from experience or published data on the prevalence of a disease. A classic paper by Diamond and Forrester,17 for example, provides estimates of the prevalence of coronary artery disease in patients depending on age, gender, and symptom features. This type of observational research can be used to provide us with the prior probabilities needed for bayesian reasoning.

INFANT AND TODDLER

The accurate identification of infants and toddlers with cerebral palsy depends on repeating examinations at different ages and evaluating the quality of movement patterns, in addition to assessing motor milestones and completing the traditional neurological examination. Important movement patterns include primitive reflexes, such as the asymmetrical tonic neck reflex, the tonic labyrinthine reflex-supine, and the neonatal positive support reflex, which disappear with maturation; and automatic reactions, such as truncal equilibrium responses and parachute responses that appear with increasing age. In addition, it is important to observe the motor patterns used to roll, come to sit, and pull to stand. A number of screening tests incorporate some or most of these items: the Alberta Infant Motor Scale,43,44 the Chandler Movement Assessment of Infants Screening Test,45 the Infant Motor Screen,46 the Milani Comparetti Motor Development Screening Test,47 and the Primitive Reflex Profile.48 Screening tests provide a structure for making accurate observations and can assist with referral decisions.

Other authors have emphasized making careful observations of the generalized movements of very young infants to improve the identification of cerebral palsy.49,50 This approach is based on the work of Heinz Prechtl and involves scoring the video recording of the movement of infants from a few weeks to several months of age. The age for fidgety movements (2 to 4 months) is reported to be the best age for making predictions.50 As with other methods, however, prediction of developmental outcomes are best made on the basis of a longitudinal series of assessments.50

A number of infants continue to present diagnostic challenges. Some preterm infants appear to have spasticity in their legs and a spastic diplegia pattern of cerebral palsy; however, these signs resolve after a year of age. In one study, only 118 of 229 children with a diagnosis of cerebral palsy at 1 year of age still had the diagnosis at 7 years.51 This pattern of development is called transient dystonia. A few infants with mild diplegia, hemiplegia, or extrapyramidal cerebral palsy may be “missed” when examined in the first year. Athetosis and ataxia may not develop until after a year of age. Finally, a few infants present with the signs of cerebral palsy but subsequently are shown to have a progressive disorder. All these issues underline the importance of repeating examinations at different ages.

Neonatal Reflexes

One way to develop an account of the development of walking is to note that several characteristic behaviors or, as they are classically called, “reflexes,” come into play during walking. Some of these behaviors appear in infancy but not in later life (Easton, 1972). The disappearance of these behaviors signal neurological changes that allow for more mature forms of motor behavior.

Consider some of the reflexes exhibited by infants (Figure 5.14). One is the startle reflex, which is triggered by unexpected noise or changes in bodily position, particularly changes in body position that create a sensation of falling. The baby’s arms and legs move symmetrically, first outward, then upward, then inward. The hands open and clench, as do the legs.

Another infantile reflex, the tonic neck reflex, is an asymmetrical pose adopted by newborns up to about 16 weeks of age. The baby’s head and arm extend to one side. On the opposite side, the arm and leg flex. The functional significance of the tonic neck reflex has been widely discussed. One hypothesis is that it enables the infant to observe its own hand, thereby facilitating the development of hand-eye coordination. Although the tonic neck reflex disappears during development, it may remain available later in life (see Figure 5.15), providing a built-in pattern that can be called upon as necessary (Easton, 1972).

The righting reflex occurs when the infant is pulled up to a sitting position. When the righting reflex is exhibited, the infant attempts to keep its head erect. The head may flop forward or back due to poor coordination or weakness.

When pressure is applied to the palm of the baby’s hand or foot, the fingers or toes curl up as if to grab the object. Because this grasp reflex is seen in the feet as well as the hands, it may be a throwback to a time when our pre-human ancestors dwelled in trees.

The Babinski reflex is another involuntary response to stimulation of the bottom of the feet. Named for the neurologist who first described it, the foot pulls up, the toes fan out, and the big toe is raised. The Babinski reflex disappears during normal development. Its presence in older children or adults is generally taken as a sign of neurological damage.

The crawling reflex occurs in babies who have not yet learned to walk. As its name implies, this reflex is an alternating pattern of extensions and flexions of the arms and legs, performed with the belly on the ground.

The so-called swimming reflex is essentially the same as the crawling reflex, except that it occurs in water. An additional reflex is called upon when a baby is placed in water. If the baby’s face happens to be momentarily submerged, the baby rarely chokes or aspirates water. This implies that babies can inhibit their breathing. Other, more sophisticated, means of coordinating breathing and movement have also been documented (Bramble & Carrier, 1983).

Another reflex seen in babies has already been mentioned, the stepping reflex. The stepping reflex is present in newborns but usually disappears by around 4 weeks of age, only to reappear at 8 months to 1 year. The reasons for the disappearance and reappearance of stepping in infants have been debated. The debate is informative and is reviewed below.

B Strategies for Reaching at 2 to 5 Months of Age: Unilateral, Bilateral, Unilateral Again

Although mature reaching for small objects is mostly unimanual, spontaneous strategies preceding this mature stage fluctuate between unilaterality and bilaterality. There are a few studies concerning bilateral coordination during the first weeks of life. The now classic White, Castle, and Held (1964) study where infants were observed in a supine position and were provided with an object at a reaching distance either at the midline or at a lateral position, shows that between 2 and 3 months of age, response to object presentation consists of unilateral hand raising, and is more likely to occur if the object is presented on the side of the commonly viewed hand, which is the hand extended in the favored tonic neck reflex position (White, et al., 1964). As the asymmetrical tonic neck reflex declines and posture becomes more symmetrical at around 3 months of age, unilateral arm approaches decrease in favor of bilateral patterns, such as hands clasping to the midline. Bilateral arm activity in response to object presentation becomes more frequent up to 4 1/2 months but as the object begins to be crudely grasped at about 4 months, unilateral responses reappear, to predominate at 5 months in what White et al. term “top level reaching” (see Table I). This consists in a rapid lifting of one hand toward the object. Top level reaching is visually controlled although visual control over the hands fades.

This U-shaped development of bimanual responses to object presentation (which rises between 2 and 3 months of age, and then decreases after 4 months of age), is also observed for mouthing a tactually presented object (Rochat, 1992). After placing an object in either the left or the right hand of 2- to 5-month-old infants, Rochat analyzed the pattern used by the infants to transport the object to the mouth. He found this pattern to be unimanual at 2 months, bimanual at 3 months (and also at 4 months for one of the two experiments reported), and to become primarily one-handed again at 5 months. Such fluctuations between unilaterality and bilaterality of reaching were first observed by Gesell and Ames (Gesell & Ames, 1947; Ames, 1949).

Reaching requires control of the upper limb (arm, hand), which is the last part of the effector chain also involving postural adjustments. Consequently, the use of a strategy (uni- vs. bimanual) must be affected by the postural adjustments the infant can or has to make. This can be observed during development or by changing the postural conditions of testing, as will be seen in the next section.

Vestibular Responses in Neonates

At present, direct evidence that vestibular organs do function in neonates comes from research about vestibular-ocular responses and primitive reflexes such as the Moro reflex. For example, Eviatar and Eviatar (1978) have recorded pre- and post-rotatory nystagnus, induced by body rotation, in 75% of neonates and in only 25% of premature infants. Ocular doll’s eye reflex in response to vestibular stimulation during body tilting or head rotation also induces compensatory horizontal smooth eye movements as soon as birth. Different studies have focused on the effect of vestibular-postural stimulation on the visual system (see Jouen & Bloch, 1981, for a review). Placing newborns in an upright position increases the duration of fixation on visual targets and induces an improved horizontal smooth pursuit (Frederickson & Brown, 1975; Gregg, Haffner, & Korner, 1976).

Another example of the maturation of otolithic organs was found in a series of experiments about head-righting responses (Jouen, 1984). In one experiment, we found that babies under 3 months, who do not yet have a muscular control of head and neck antigravity muscles, are, however, able to detect otolithic stimulation provided by a 25 degree lateral body tilting by compensating for body tilting with a continuous horizontal head rotation. This head-turning brings the head to exactly the same final horizontal position as in older infants reacting to body tilting via a vertical head-righting.

Tonic neck and labyrinthine reflexes belong to the category of primitive reflexes involved in early equilibrium reactions (Capute et al., 1978, 1982). Tonic neck reflexes originate from proprioceptive receptors in the neck extensors and are found in neonate (Peiper, 1962). Tonic labyrinthine reflexes are closely connected to the tonic neck reflexes. They are thought to be mediated by the medial and lateral vestibulo-spinal tracts and the reticulo-spinal pathway with primary afferents in the otoliths and perhaps the neck extensors. Little is known about their appearance, strength, and disappearance in normal children. In cerebral palsied children, these reflexes have strong effects on the regulation of muscle tonus (Illingworth, 1978). They are involved in basic postural activities such as the change of body position (by body rolling) or the extension of the head when prone.

The tonic labyrinthine reflex in prone position (TLP) has been systematically studied in 149 infants followed from birth up to 2 years of age by Capute et al. (1982). For a child held in prone suspension, the position of the limbs changes with respect to the position of the head in space and the orientation of the labyrinths. When the neck is extended by 45 degrees, the limbs extend, whereas they flex when the neck is flexed by 45 degrees. The TLP is present in 80% of infants at 2 weeks of age and persists throughout the first 18 months, with a maximum occurrence between 4 and 6 months.

Stimulating vestibular and neck receptors by turning the infant’s head affects the position of his/her arms and legs (Gesell, 1938; Peiper, 1962, 1963; Turkewitz, Gordon, & Birch, 1965): The limbs on the side toward which the face is turned will extend, and the limbs on the opposite side will be in flexion. This reflex is accompanied by a modification of the muscle tonus regulation: The side of the body where the face is turned is more tonic, whereas the opposite flexed limbs are less tonic. This pattern seems relatively rare in premature infants (Mellier & Jouen, 1985; Allen & Capute, 1986) but reaches a peak frequency around 6 to 8 weeks after birth (Coryell & Michel, 1978; Coryell & Cardinalli, 1979). This reflex usually disappears around the third month.

The Moro reflex has been widely studied in preterm infants (Allen & Capute, 1986). As early as 25 weeks post-conception, a Moro reflex is observed. This vestibular reaction is observed in 80% of 30-week-old fetuses. Eviatar and Eviatar (1978) describe a reaction in neonates in response to a vertical acceleration that is similar to the Moro reflex.

To summarize, from birth, the vestibular sensory system is able to tune postural and oculomotor activities involved in head-eye coordination and body spatial orientation relative to gravity. Moreover, different data suggest that vestibular sensitivity is not only peripheral but also central: Vestibular responses can be habituated in neonates and young infants (Ornitz et al., 1979). This is important because experiments with animals have demonstrated that vestibular habituation requires a central coding of information relative to self-motion. In other words, the brainstem structures involved in the control of the vestibular system are mature and functional at birth (Stein & Meredith, 1993).

24-1.3 Behavioral Evidence