Central Locomotion Generators

Locomotion is controlled by several centers at different levels of the CNS. There is strong evidence that the most basic rhythmic, bipedal, synchronized stepping of mammalian quadrupeds originates in centers in the spinal cord referred to as the central pattern generators. Indeed, decerebrate cats can produce a rhythmic stepping pattern if they are put on a treadmill. Although anatomical demonstration of the existence of such centers is lacking in humans, central pattern generator-like centers probably exist in humans as well. The human central pattern generator also controls the timed coupling between arm and leg movements during normal walking.¹ In primates, including humans, the central pattern generator is probably located within the spinal cord, as is suggested by the production of gaitlike movements in paraplegic patients who, when placed with support on a moving treadmill, can also produce rhythmic stepping. Such spinal central pattern generators are under the influence of brainstem control mechanisms, which are most probably situated at the level of the mesencephalon in the brain. In humans, the caudal cholinergic mesencephalic nucleus, also referred to as the pedunculopontine nucleus (PPN), is considered as the human mesencephalic locomotion center. It is believed to control spinal pattern generators or to play a similar role as the spinal central pattern generator in animals and is considered the human mesencephalic locomotion center.² The PPN receives afferent GABAergic projections (secreting the neurotransmitter gamma-amino-butyric acid [GABA]) from the internal globus pallidus, subthalamic nucleus, and the substantia nigra pars reticulata. It sends efferent cholinergic and glutamatergic projections (secreting the neurotransmitters acetylcholine and glutamic acid) to the substantia nigra pars compacta and downward to the brainstem and spinal cord. The PPN is the only nucleus associated with the basal ganglia that has a direct connection with the spinal cord and, as such, it is believed to play a major role in motor control of gait and posture. PPN stimulation can induce stepping in primates while a lesion at the PPN causes severe akinesia and parkinsonism in primates that is reversed by blocking GABAergic stimulation of the PPN. Furthermore, a focal stroke within the dorsal mesencephalon (presumably involving the PPN) has been shown to cause severe gait initiation problems in a human patient.

Higher centers at the level of the basal ganglia, thalamus, and cortex are parts of the locomotion network that controls walking as a motor behavior, and they constantly interact with the internal and external environments. The frontal lobe and its premotor area are of special importance for planning, initiating, and continuous adjustment of the walking motor plan. The visual cortex produces information about the space where walking takes place, and this information is interpreted in other cortical areas in terms of visuospatial orientation, danger, and significance. The basal ganglia pass on information needed for the generation of a rhythmic gait pattern (i.e., internal cueing of gait) and play an especially critical role when there is a need for constant alertness and focused attention to the motor task or to a changing environment. Cortical and subcortical white matter and basal ganglionic lesions can lead to complete inability to initiate locomotion (akinesia), severe unsteady gait (disequilibrium), unorganized and dysfluent locomotion, and pathological interaction with the environment. Altogether, these types of lesions often lead to loss of mobility and a high risk for falls.

Walking is dependent heavily on the musculoskeletal system for its execution. Strong bones with flexible joints and elastic feet and spine are essential for effective gait. Similarly, strong muscles are responsible for maintaining the correct posture and moving the bones in harmonic fashion to create motion in space. The peripheral nervous system executes the motor plan of walking at the level of the spinal cord through the motor neurons and provides online information from the sensory receptors about the internal (e.g., sense of position) and the external environments. The centrally generated gait motor plan is tested by the degree of scaling and synchronized activation of multiple muscle groups at multiple levels of the spinal cord. Walking is not possible if muscle weakness or activation dyssynchronization exceeds a certain threshold. Similarly, an abnormal sensory input from the periphery leads to instability and frequent falls because balance is heavily dependent on data from the environment.

The Gait Cycle

Walking can be regarded as a composite of numerous small and similar gait cycles, each based on an alternating single step accomplished by both legs. A full cycle can be calculated from any given point because of the rhythmic and stereotypic manner of locomotion. Classically, spatial description of the gait cycle starts when the right heel touches the ground while the right knee is stretched (locked) and the right foot is dorsiflexed. The foot rolls on the ground and carries most or all of the body mass as part of the stance phase. As the body mass moves forward, the heel leaves the ground. After a forced plantar flexion that pushes the body center of mass forward, the toes also leave the ground. When the toes of the right foot leave the ground, the swing phase of the right leg starts. In the swing phase, the right leg swings forward after the right hip is pulled up (flexed) while the knee initially will be flexed and later extended to reach the ground in a locked position. During the swing phase, the foot is dorsiflexed to avoid any contact of the toes with the ground. The cycle ends when the right heel again comes in contact with the ground (Fig. 36-1).

Figure 36-1 The gait cycle.

The gait cycle can also be characterized temporally. The right foot normally touches the ground for about 60% to 65% of the gait cycle. Only one leg is in contact with the ground (single support time) during 30% to 40% of the cycle, and both legs touch the ground in the double support phase during one third of that time or 20% to 25% of the whole cycle. Based on this time frame, the swing phase of the right leg and the stance phase of the left leg (single support time of the left leg), which, by definition are equal in time, take place during 35% to 40% of the gait cycle. The proportion of each phase of the gait cycle is changed in relation to the speed of walking, as well as in relation to the individual’s physical state, security, and equilibrium. Accelerated walking is associated with shortening of all phases, but proportionally more of the double-limb support time shrinks. Aging, physical weakness, and disequilibrium lead to slower gait speed and increased double-limb support time.

Three additional spatiotemporal features of locomotion are stride length, cadence, and step width. Stride length is the distance between the places where the right heel first touches the ground at the initiation of one gait cycle to the place where it touches the ground again at the beginning of the next gait cycle. Stride length is also the summation of the distances of two steps (left plus right). Cadence is the step rate or the number of steps in a given time (e.g., steps per minute), and step width describes the distance between the two feet along the perpendicular axis to the walking direction for a given step.

Clinical Assessment

The “bedside examination” of gait and balance involves taking a careful history and a detailed physical examination.

History Taking

Interviewing patients about their problems with gait or balance can be a challenge. When asking about gait problems, the clinician has to understand the amount of walking a person does in daily life. In addition, the nature of the questions themselves should try to help the patient describe his difficulties in terms of walking speed, amount of effort required, confidence or degree of fear from falling, and whether any assistance or walking aids are used. It is informative to look at the patient’s step length as a good general marker and to note if one can hear the soles dragging on the floor during each step as a practical marker for the height and duration of the swing phase. For patients presenting with gait disorders, try to distinguish between consistently present walking difficulties versus an episodic gait disorder, such as freezing of gait, festination, or sensory ataxia in the dark. When asking about possible freezing of gait, one must specifically inquire about the characteristic subjective feeling of the feet “being glued to the ground.” A specific Freezing of Gait Questionnaire has been developed that may assist in screening for and rating the severity of freezing of gait.⁵ To make sure that the patient understands what is meant by freezing of gait, it may be useful to demonstrate an imitation of a typical freezing of gait episode.

Falls are one of the most serious complications of gait disturbances and should receive special attention. Many elderly persons tend to forget their falls, particularly when there is concurrent cognitive impairment, as is often the case. Some persons may even purposely deny the occurrence of falls because they fear being admitted to a nursing home or another form of sheltered care. Many elderly persons find it extremely difficult to indicate under which circumstances their falls occur. Nevertheless, obtaining a careful fall history is important, because the presence of a prior fall in the preceding 6 to 12 months consistently emerges as an excellent, simple predictor for repeated falls in the future.⁶ Patients should be asked not only about falls but also about the presence of “near-falls.” These are at least as common and can be debilitating in their own right. In light of the characteristic amnesia for falls, eyewitness reports are often indispensable, and every effort must be made to retrieve the accounts of bystanders who witness falls.

Table 36-1 can serve as a guideline for the interview. Several important elements of this clinical approach are discussed in more detail next.

TABLE 36-1 Elements of History Taking in Persons With Gait Disorders or Falls

* If needed, evaluate domestic situation by community nurse, physiotherapist, or occupational therapist.

For any patient presenting with falls, the first thing to do is to clarify the circumstances surrounding the fall and, in particular, to identify any specific pattern, because this may reveal the underlying pathophysiology and offer opportunities for prevention. The second step involves a distinction between single versus recurrent (two or more) falls and between “internal” and “external” falls, features that are important for secondary prevention. One should therefore evaluate whether any environmental factors were obviously responsible for the falls. When the role of environmental factors is unclear or frankly denied, the fall can then be classified as “intrinsic” (usually defined as a fall that was caused by gait or balance disorders or misperception of the environment). The third step is to inquire whether any transient loss of consciousness preceded the fall. The absence of a preceding transient loss of consciousness indicates a probable involvement of an underlying gait disorder and/or balance deficit. This will become evident during physical examinations between falling episodes. If the gait or balance disorder is severe enough, even small movements can be destabilizing and the patient may start to fall almost spontaneously. In patients with apparently unprovoked falls, care must be taken not to miss a possible preceding transient loss of consciousness. Explicit inquiry into the use of medication is vitally important, because this is one of the most common risk factors for gait disorders, falls, and hip fractures in elderly persons. In particular, benzodiazepines and antidepressants are associated with falls in the elderly, but other psychotropic medications (e.g., neuroleptics) and drugs causing orthostatic hypotension or arrhythmia also increase the risk of falls. Dopaminergic medication may paradoxically increase the fall frequency of patients with Parkinson’s disease by causing excessive dyskinesias, orthostatic hypotension, or confusion. The risk of falls increases dramatically if different drugs are used at the same time (Fig. 36-2).

Figure 36-2 The clinical work-up of falls. An “obvious extrinsic cause” refers to an overwhelming external hazard, which would make almost every person fall (e.g., a pedestrian being knocked down by an automobile). Medical notes provide a wealth of easily accessible information about relevant risk factors (age, sex, medical history, and medication) that could serve to guide the selection of patients at risk for falls. TLC, transient loss of consciousness. *In patients with seemingly spontaneous falls, consider one of the following three possibilities: TLC that was apparently forgotten or misperceived by the patient; a mimic of TLC (drop attacks, cataplexy, or hyperexplexia); or a seemingly spontaneous fall that was in fact caused by a severe underlying gait or balance disorder.

(Modified from Bloem BR, Boers I, Cramer M, et al: Falls in the elderly. I. Identification of risk factors. Wien Klin Wochenschr 2001; 113:352-362, with permission.)

The psychological consequences of falls can be severe. Thus, it is important to assess whether a patient has a fear of falls and whether this fear is reasonable (in persons with extremely poor balance) or if it is inappropriate (a pathological fear induced by a single but otherwise innocent fall). “Self-confidence” (confidence in not falling) should also be evaluated as this provides valuable complementary information about the impact of falls on activities of daily living and independence. Some patients feel overly confident despite marked balance deficits, and they have a high risk of falling.

Physical Examination

Table 36-2 lists several important elements of the physical examination. The examination should include a battery of functional tests to capture the full repertoire of gait and balance abnormalities. Ideally, physicians should examine the patients in the environment where they walk and function in daily life (i.e., home and surroundings), but this is not practical. A homemade video can sometimes be extremely informative, especially for episodic gait disturbances. Similarly, examining the patient immediately after a fall can help with the identification of its cause(s) and consequences, but this is rarely possible. A problem with the inevitably “interictal” examinations is that the observed abnormalities may not be causally related to the gait disturbance or the fall. Physical examinations can appear to be entirely normal in between freezing of gait or fall episodes.

TABLE 36-2 Elements of Physical Examination in Patients With Gait Disorders or Falls