EHL, extensor hallucis longus.

The terms frontal release signs (FRS) and primitive, fetal, developmental, or atavistic reflexes refer to responses that are normally present in the developing nervous system, but disappear to a greater or lesser degree with maturation. While normal in infants and children, when present in an older individual they may be evidence of neurologic disease, although some may reappear in normal senescence. Many of these are exaggerations of normal reflex responses. Responses often included as FRS include the palmomental reflex (PMR), grasp, snout, suck, and others.

FRSs occur most often in patients with severe dementias, diffuse encephalopathy (metabolic, toxic, postanoxic), after head injury, and other states in which the pathology is usually diffuse but involves particularly the frontal lobes or the frontal association areas. The significance and usefulness of some of these release signs or primitive reflexes have been questioned. Jacobs and Grossman, investigating the palmomental, snout, and corneomandibular reflexes, found at least one of these was present in 50.5% of normal subjects in the third through ninth decades of life. The PMR appeared earliest and was the most frequent reflex at all ages, occurring in 20% to 25% of normal individuals in the third and fourth decades. In 20% of the group, more than one of the reflexes was elicited, and in about 2% all three were present. The Hoffman finger flexor reflex and its variants, which are sometimes classified as FRS and sometimes as corticospinal signs, are similarly present in a significant proportion of normal individuals. Clearly, these reflexes are a normal phenomenon in a significant proportion of the healthy population. They must be interpreted with caution and kept in clinical context. Even when such reflexes are briskly active in an appropriate clinical setting, the primitive reflexes do not have great localizing value, suggesting instead the presence of diffuse and widespread dysfunction of the hemispheres.

PATHOLOGIC REFLEXES IN THE LOWER EXTREMITIES

Pathologic reflexes in the lower extremities are more constant, more easily elicited, more reliable, and more clinically relevant than those in the upper limbs. The most important of these responses may be classified as (a) those characterized in the main by dorsiflexion of the toes and (b) those characterized by plantar flexion of the toes. The most important pathologic reflex by far is the Babinski sign, and a search for an upgoing toe has traditionally been part of every neurologic examination. There are, in addition, a few miscellaneous responses. Searching for upper-extremity pathologic reflexes is much less productive and often omitted.

Corticospinal Responses Characterized in the Main by Extension (Dorsiflexion) of the Toes

The Babinski Sign

In the normal individual, stimulation of the skin of the plantar surface of the foot is followed by plantar flexion of the toes (see Figure 39.2). In the normal plantar reflex, the response is usually fairly rapid, the small toes flex more than the great toe, and the reaction is more marked when the stimulus is along the medial plantar surface. In disease of the corticospinal system, there may be instead extension (dorsiflexion) of the toes, especially the great toe, with variable separation or fanning of the lateral four toes: the Babinski sign or extensor plantar response (Figure 40.1). Babinski worked in a clinical arena dominated by Charcot and a focus on hysteria. His primary aim was in trying to find reliable clinical signs to distinguish organic from nonorganic disease of the nervous system. Babinski described two components of the abnormal plantar reflex. He first described toe extension (1896) as phénomène des orteils (the dorsiflexion of the toes): “pricking of the sole… results in flexion of the thigh on the pelvis, of the leg on the thigh, and of the foot on the leg, but the toes, instead of flexing, execute a movement of extension upon the metatarsus.” This is in fact a description of a triple flexion response. He also pointed out that the extension response was most easily elicited on stimulation of the outer aspect of the sole, in contrast to the normal plantar response. In 1903, he described abduction of the smaller toes, later labeled by others as the signe de I’éventail (the fanning). The Babinski sign has been called the most important sign in clinical neurology. It is one of the most significant indications of disease of the corticospinal system at any level from the motor cortex through the descending pathways.

The Babinski sign is obtained by stimulating the plantar surface of the foot with a blunt point, such as an applicator stick, handle of a reflex hammer, a broken tongue blade, the thumbnail, or the tip of a key. Much has been written about the best tools for eliciting the plantar response. Henry Miller, a legendary English neurologist, contended that the only proper instrument was a Bentley key. In the United States, the different types of keys used by neurologists as opposed to neurosurgeons are a source of tiresome levity. Babinski allegedly favored a goose quill.

Strength of stimulus is an important variable. It is not true that the stimulus must necessarily be deliberately “noxious,” although most patients find it at least somewhat uncomfortable even if the examiner is trying to be considerate. It has been stated that eliciting the plantar responses brings out doctors’ masochistic tendencies. Every physician should undergo plantar stimulation in order to appreciate the discomfort. When the response is strongly extensor, only minimal stimulation is required. Babinski observed the extensor plantar response when the wind blew the curtains across the feet of spinal cord–injured patients. Some reports have Babinski using a feather. The stimulus should be firm enough to elicit a consistent response, but as light as will suffice. Some patients are very sensitive to plantar stimulation, and only a slight stimulus will elicit a consistent response; stronger stimuli may produce confusing withdrawal. If the toe is briskly upgoing, merely a fingertip stimulus may elicit the response. If no response is obtained, progressively sharper objects and firmer applications are necessary. Although some patients require a very firm stimulus, it is not necessary to aggressively rake the sole as the opening gambit. Both tickling, which may cause voluntary withdrawal, and pain, which may bring about a reversal to flexion as a nociceptive response, should be avoided.

Plantar stimulation must be carried out far laterally, in the S1 root/sural nerve sensory distribution. More medial plantar stimulation may fail to elicit a positive response when one is present. Far medial stimulation may actually elicit a plantar grasp response, causing the toes to flex strongly. The stimulus should begin near the heel and be carried up the side of the foot at a deliberate pace, not too quickly, usually stopping at the metatarsophalangeal joints. The response has usually occurred by the time the stimulus reaches the midportion of the foot. If the response is difficult to obtain, the stimulus should continue along the metatarsal pad from the little toe medially, but stopping short of the base of the great toe. The most common mistakes are insufficiently firm stimulation, placement of the stimulus too medially, and moving the stimulus too quickly so that the response does not have time to develop. The only movements of significance are those of the great toe. Fanning of the lateral toes without an abnormal movement of the great toe is seldom of any clinical significance, and an absence of fanning does not negate the significance of great toe extension.

The patient should be relaxed and forewarned of the potential discomfort. The knee must be extended; an upgoing toe may be abolished by flexion of the knee. The best position is supine, with hips and knees in extension and heels resting on the bed. Some neurologists will only check the plantar responses with the patient recumbent. If the patient is seated, the knee should be extended, with the foot held either in the examiner’s hand or on her knee. The response may sometimes be reinforced by rotating the patient’s head to the opposite side. It may be inhibited when the foot is cold and increased when the foot is warm.

Usually, the upward movement of the great toe is a quick, flicking motion sometimes mistaken for withdrawal by the inexperienced. The response may be a slow, tonic, sometimes clonic, dorsiflexion of the great toe and the small toes with fanning, or separation, of the toes. The slow great toe movement has been described as a “majestic rise.” The nature of the stimulus may be related to the speed of the toe movement; primarily proprioceptive stimuli (e.g., Gonda, Stransky, Szapiro) are more apt to be followed by a slow, tonic response; exteroceptive stimuli, by a brief, rapid extension (for video of the Stransky reflex see Amir and Helsen). There may occasionally be initial extension, followed by flexion; less often brief flexion precedes extension. There may be extension of only the great toe, or extension of the great toe with flexion of the small toes. Puusepp’s sign is tonic, slow abduction of the little toe on plantar stimulation and may be present when great toe extension is absent.

The Babinski sign is a part of the primitive flexion reflex. The central nervous system is organized according to movement patterns, and one of the most basic patterns is avoidance or withdrawal from a noxious stimulus. In higher vertebrates, the flexion response includes flexion of the hip and knee, and dorsiflexion of the ankle and toes, all serving to remove the threatened part from danger. Although the relevant muscles are anatomical extensors, and have extensor names (e.g., extensor hallucis longus [EHL]), physiologically flexors serve to shorten a limb, so toe “extension” is in fact part of the flexion response. In human infants, the primitive flexion response persists, and an extensor plantar response is normal in infancy. The plantar response in infancy has been studied on several occasions, with variable results; Gingold et al. found extensor responses at birth in 100% of infants, at 6 months in 10.9%, at 1 year in none. There are several examples of infantile upgoing toes in Renaissance Madonna and child paintings (Boticelli recorded the extensor plantar response 400 years before Babinski). Maturation of the descending motor systems suppresses the primitive flexion response. This may be necessary for normal ambulation, or else our legs and feet might be whipping into flexion unexpectedly, just from stepping on a pebble. The corticospinal tract is myelinated by about the end of the first year of life, about the time babies begin to walk. When there is disease involving the corticospinal tract, the primitive flexion response may reappear, and the first clinical evidence of this is the Babinski sign. With more severe and extensive disease, the entire flexion response emerges, so that stimulation of the sole causes dorsiflexion not only of the toe, but also the ankle, as well as flexion of the hip and knee (the “triple flexion” response, which for some perplexing reason has four parts). In addition, there is often contraction of the tensor fascia lata causing slight internal rotation at the hip and more rarely abduction of the hip (Brissaud’s reflex). The Brissaud reflex may be useful in the rare patient whose great toe is missing. These movements are all part of a spinal defense reflex mechanism, also known as the reflex of spinal automatism (Marie), the pathologic shortening reflex, reflex flexor synergy, the withdrawal reflex, mass flexion reflex, and the refléxe or phénomène des raccourcisseurs. The dorsiflexion of the toes may be the only visible effect, but the contraction of the thigh and leg muscles is also present and may be detected by palpation. The response may be bilateral and is then called the crossed flexor reflex.

A small but provocative study questioned whether the Babinski sign should be part of the routine neurologic examination, contending that its validity and interobserver reliability was limited. The authors suggested that slowed foot tapping was a more useful clinical sign. The article provoked an editorial and a flurry of correspondence challenging the conclusions and the methodology.

There are many other corticospinal tract responses in the lower extremities characterized by dorsiflexion of the toes. With severe corticospinal tract disease, the threshold for eliciting an upgoing toe is lower, the reflexogenic zone wider, and more and more of the other components of the primitive flexion reflex appear as part of the response. This has led to a profusion of variations on the Babinski method of eliciting the extensor plantar response. Foster Kennedy referred to the 30 years around the turn of the twentieth century as “open season for the hunting of the reflex.” Grant referred to it as the “assault on the great toe.” Many clinicians sought eponymic immortality by describing different ways of making the toe go up, other components of the reflex, and other variations on the theme. There are too many modifications to mention all. The most useful variation is the Chaddock sign, and the Oppenheim is also often done. Other responses have been relegated to the category of minor toe signs, which now amount to clinical parlor tricks (Table 40.1). Some may occasionally be useful in cases where, for some reason, the plantar surface of the foot cannot be stimulated.

The Chaddock sign is elicited by stimulating the lateral aspect of the foot, not the sole, beginning about under the lateral malleolus near the junction of the dorsal and plantar skin, drawing the stimulus from the heel forward to the small toe. The reflex was described first by Yoshimura, but in Japanese so the observation was lost. In the “reverse Chaddock,” the stimulus moves from the small toe toward the heel. The Chaddock is the only alternative toe sign that is truly useful (according to Sapira, in his time the best neurologist in St. Louis was C.G. Chaddock; the second best was C.G. Chaddock drunk). It may be more sensitive than the Babinski but is less specific. It produces less withdrawal than plantar stimulation. The two reflexes are complementary; each can occur without the other, but both are usually present. The Oppenheim sign is usually elicited by dragging the knuckles heavily down the anteromedial surface of the tibia from the infrapatellar region to the ankle. The response is slow and often occurs toward the end of stimulation. Oppenheim allegedly did this by raking the handle of his reflex hammer down the shin. A common ploy is to combine the Oppenheim and the Babinski to make a suspicious toe declare itself, but this is more painful and less useful than the Chaddock.

When the response is very active and the reflexogenic zone wide, the toe may go up with such minor stimuli as pulling back the bed sheets (the “bed sheet Babinski”) or rapid removal of the sock or shoe. Occasionally, there is a “spontaneous Babinski,” occurring with no apparent manipulation of the foot. There may even be contralateral or bilateral responses. The response may occur with passive extension of the knee or passive flexion of the hip and knee. Sometimes, the toes are held in a tonic position of dorsiflexion and fanning. Such a tonic toe may become problematic, causing skin breakdown on the dorsum of the great toe from friction against the shoe (an example of the maladaptive effect of an unsuppressed primitive flexion reflex). Botulinum toxin is sometimes injected into the EHL to control the tenacious toe extension. A tonic extensor plantar response must be distinguished from a “striatal toe” (see Chapter 30)

The complete primitive flexion reflex can become tonic and permanent. This occurs most often in patients with severe myelopathy, usually traumatic, and produces a posture referred to as paraplegia in flexion. The exaggeration of the flexion reflex causes involuntary flexor spasms that hold the legs intensely flexed with increasing frequency and for longer and longer periods until they can no longer be actively or even passively extended. This terminates eventually in a tonic flexion posture, with permanent fixed flexion of the hips and knees and dorsiflexion of the ankles and toes. Secondary joint contractures are common. In the severest cases, the legs and thighs are completely flexed and the knees pressed against the abdomen. Even after the development of a fixed flexion posture, any additional stimulus may aggravate the degree of flexion.

Problems in Interpreting the Plantar Response

The extensor plantar response is one of the most reliable, dependable, and consistent signs in clinical neurology. It has good interobserver reliability, and its presence is, with rare exception, credible evidence of organic neurologic disease (as Babinski had originally hoped). But it is not perfect, and the response to plantar stimulation may at times be difficult to evaluate. The most common problem is distinguishing an upgoing toe from voluntary withdrawal, especially when the plantar surface of the foot is unusually sensitive. Occasionally, even a seasoned clinician cannot be sure or makes the wrong interpretation. The Babinski sign is part of a withdrawal reflex, so flexion of the hip and knee are by no means reliable indicators that the withdrawal movement is voluntary. Voluntary withdrawal rarely causes dorsiflexion of the ankle, and there is usually plantar flexion of the toes. Voluntary withdrawal is more likely when the stimulus is too intense and uncomfortable. It helps if the patient understands the importance of holding still and receives some explanation of the relevance of this seemingly inane and cruel test. Some patients have ticklish feet and will pull away from even a light stimulus. If the patient is ticklish, it may help to simply hold the ankle firmly. Some believe withdrawal is less if the patient performs the plantar stimulation himself (an auto-Babinski); others (author included) have not found this useful. Some contend pressure over the base of the great toe will inhibit the withdrawal extensor response, but not eliminate the extension associated with corticospinal tract disease. Internal rotation of the leg during the “withdrawal” signals recruitment of the tensor fascia lata into the movement (the Brissaud reflex component) and makes it more likely the response is reflex and not voluntary.

The most important observation is the initial movement of the great toe. With repeated stimulation of the sole, the extensor movement may decrease and then disappear. So the crucial observation is the first toe movement on the first stimulation. Occasionally, withdrawal makes it impossible to be certain whether the toe was truly extensor or not; these are equivocal plantar responses. Some patients have no elicitable plantar response, in which case the plantars are said to be mute or silent. An extensor plantar response may also show itself in formes frustes. There can be flexion of the hip and knee with no movement of the toes. Asymmetry of the plantar responses may be significant; a toe that does not go down as crisply as its fellow may be suspect, even if it does not frankly go up. A toe is more likely to go up late in the day or when the patient is tired.

Van Gijn and Bonke investigated the biasing effect of other signs and symptoms on the interpretation of plantar reflexes. They found physicians place the toe in clinical context and this affects interpretation. The history and other examination findings have a significant influence, and many neurologists have a significant bias about the expected direction of toe movement before touching the foot. It appears preknowledge makes it easier to call an equivocal response extensor.

A toe may occasionally fail to go up when expected, despite good technique. It is occasionally possible to elicit one or more of the other extensor toe signs, especially the Chaddock, when the Babinski cannot be obtained. A more extensive lesion may be necessary for production of the Oppenheim or Gordon sign than for the Babinski or Chaddock. It is occasionally useful to try two maneuvers simultaneously (e.g., Babinski and Oppenheim or Babinski and Gordon) to bring forth a latent extensor response by means of reinforcement. In a study of the consistency of the Babinski reflex and its variants, the combination of the Babinski and Chaddock reflexes was the most reliable.

Toe extension may occasionally fail to occur because of disruption of the lower motor neuron innervation to the EHL (e.g., radiculopathy, peroneal nerve palsy, peripheral neuropathy, amyotrophic lateral sclerosis [ALS]), in which case the toe is paralyzed for voluntary contraction as well. Contraction of the other muscles involved in the primitive flexion reflex may betray the upper motor neuron pathology. Frontal lobe lesions may cause a hyperactive plantar grasp reflex (see next section), driving the toes downward. The toe may not go up during the neural shock phase of acute insults to the corticospinal tract. Sometimes, the plantar response remains inexplicably flexor despite an abundance of other corticospinal tract signs. This may happen in ALS, in part because of lower motor neuron involvement of the toe extensors. In other instances, the absence of a toe sign remains a curious paradox. With pes cavus and high-arched feet, the response is difficult to evaluate because of fixed dorsiflexion of the toes.

An extensor plantar response may occasionally occur in patients with no other evidence of corticospinal tract disease and in a small percentage of individuals who appear otherwise neurologically normal. It may be the only residual sign of previous disease. With extensive disease involving both the basal ganglia and the corticospinal tract, there may be no extensor response. In all probability, intact extrapyramidal pathways are essential to its production. The extensor plantar response does not occur in lesions of the basal ganglia alone; its presence in some extrapyramidal disorders, such as Parkinson’s disease, suggests associated corticospinal tract involvement. Paralysis of the toe flexors may cause a false-positive extensor plantar response.

An extensor plantar response does not always signify structural disease; it may occur as a transient manifestation of physiologic dysfunction of the corticospinal pathways. A Babinski sign may sometimes be found in deep anesthesia and narcosis, in drug and alcohol intoxication, in metabolic coma such as hypoglycemia, in deep sleep, postictally, and in other conditions of altered consciousness. The plantar response returns to normal with recovery of consciousness. During Cheyne-Stokes respirations, an upgoing toe may appear during the apneic phase and disappear during the phase of active respiration.

Corticospinal Tract Responses Characterized by Plantar Flexion of the Toes

In the newborn infant, there is a grasp reflex in the foot as well as the hand, with flexion and adduction of the toes in response to a light pressure on the plantar surface of the foot, especially its distal and medial portions. The plantar grasp normally disappears by the end of the first year. A grasp reflex of the foot may reappear in adults, along with a grasp reflex of the hand, in disease of the opposite frontal lobe. The plantar grasp may be elicited by drawing the handle of a reflex hammer from the midsole toward the toes, causing the toes to flex and grip the hammer (Figure 40.2).

In addition to the superficial plantar reflex, there is a plantar muscle reflex consisting of contraction of the toe flexors following sudden stretching. This response is barely, if at all, perceptible normally, but becomes more obvious with reflex hyperactivity and, therefore, with corticospinal tract lesions. Plantar flexion of the toes may also be elicited by application of the stimulus to other portions of the foot and ankle. The best known of this group of reflexes is the Rossolimo sign (Table 40.2, Figure 40.3). Many others have been described, all variations on the same reflex elicited by striking slightly different parts of the foot (Figure 40.4). In describing Figure 40.4 in his foreword to Wartenberg’s monograph The Examination of Reflexes, Foster Kennedy said, “… a welter of the names of reflex describers has been placed in appropriate positions around a foot, like a litter at suck. And all describing small distinctions without differences, of no true significance and usually of little help.” These variations are primarily manifestations of an exaggerated plantar muscle reflex, comparable to the variations of the finger flexor reflex in the upper extremities (see “The Hoffman and Trömner Signs and the Flexor Reflexes of the Fingers and Hand” below). Some correspond to alternate methods of eliciting the ankle reflex and may reflect spread of the reflexogenic zone.