Most forms of locomotion in VERTEBRATES are rhythmic, involving repeated cycles of movements of the body and/or the limbs. (An exception is BRACHIATION—the swinging through trees practised by certain PRIMATES.) During behaviours like WALKING, RUNNING, SWIMMING and FLIGHT, locomotor movements are produced by coordinated contractions of ANTAGONISTIC MUSCLE pairs. Rhythmic locomotion comprises two phases of movement: the POWER STROKE (when thrust is generated against the environment) and the RETURN STROKE (when reverse thrust is minimized). In swimming vertebrates, like fish and amphibian tadpoles, the segmented myotomal muscles on opposite sides of the body act as antagonists to bend the body to the left and right sides. Each side of the body acts alternately as the power and the return stroke. For limbed vertebrates, muscles controlling the joints of each limb are also arranged as antagonists that are active in alternation during locomotion. Most limb muscles are associated with either the FLEXOR PHASE (return stroke) or the EXTENSOR PHASE (power stroke) of the movement cycle. The power stroke, when the limb is generating thrust against the substrate, is also called the STANCE PHASE; when the limb is flexed, moving forwards above the substrate in preparation for the next power stroke, it is said to be in the SWING PHASE.
During each cycle of locomotion spinal MOTOR NEURONS discharge an ACTION POTENTIAL burst followed by a quiescent period when they are inhibited from firing. This cyclical bursting activity can be produced by a network of spinal cord neurons, often called an OSCILLATOR OF CENTRAL PATTERN GENERATOR (CPG). Spinal CPGs can generate rhythmic locomotor activity in the absence of both sensory information (following deafferentation) and descending signals from the brain (following SPINALIZATION). The sequence of rhythmic discharge in motor neurons generated after deafferentation and spinalization is called FICTIVE LOCOMOTION. The synaptic input to motor neurons during locomotion consists of periods of excitation (caused by excitatory postsynaptic potentials; see EPSP/IPSP) leading to action potential bursts, separated by periods of inhibition (caused by inhibitory postsynaptic potentials; see EPSP/IPSP) when motor neurons are prevented from firing. In a wide range of vertebrates the excitation results mainly from activation of GLUTAMATE RECEPTORS. Two types of glutamate reeeptor are activated: NMDA and non-NMDA (kainate/AMPA) receptors. In some vertebrates a component of the excitation during locomotion is known to result from central cholinergic connections between spinal motor neurons. Vertebrate motor neurons use the transmitter ACETYLCHOLINE (ACh) at the NEUROMUSCULAR JUNCTION to elicit muscle contraction. The intrinsic membrane properties of motor neurons may also contribute to rhythm generation: in several animals motor neurons oscillate between two voltage levels (one near RESTING POTENTIAL and the other near action potential THRESHOLD) following activation of NMDAtype glutamate receptors. These non-linear responses occur independently of, but may sum with, the synaptic drive during locomotion. They rely upon the unusual properties of the NMDA receptor type of ION CHANNEL which allows CALCIUM entry into neurons and which is voltage-dependent in the presence of MAGNESIUM ions.
The inhibition that occurs between motor bursts (called mid-cycle or RECIPROCAL INHIBITION) is coincident with activity in antagonistic motor neurons. The inhibition hyperpolarizes the membrane potential of motor neurons and reduces their input resistance to prevent action potentials. During reciprocal inhibition, chloride ion channels open to allow the influx of negatively charged chloride ions into motor neurons. The channels are associated with membrane bound receptors for the inhibitory amino acid GLYCINE and they are opened when spinal inhibitory INTERNEURONS release glycine onto motor neurons. Reciprocal inhibition during locomotion can be blocked by the glycine receptor antagonist, strychnine. The mid-cycle inhibition helps to ensure that antagonists are active in alternation.
Although spinal CPGs can operate without sensory information, feedback resulting from locomotor movements is important for adjusting the timing and intensity of motor neuron activity. Proprioceptive feedback (see PROPRIOCEPTION feedback) (also called REAFFERENCE) arises from sense organs that are activated by the movements that occur during locomotion. Two important sources of sensory feedback to spinal CPGs are the MUSCLE SPINDLE and GOLGI TENDON ORGAN that generate information about muscle length and tension, respectively. They generate information that encodes both limb position (for instance, joint angle) and the amount of load over the body. Proprioceptors are important in determining the timing of transitions between the two phases of movement. Golgi tendon organs generate positive feedback during the stance phase (power stroke), while muscle spindle activity increases towards the end of stance to terminate stance and trigger swing. The rhythmic signals from proprioceptive afferents can entrain the central motor program (see MOTOR PROGRAMMING): for example, during TREADMILL LOCOMOTION the feedback that is generated causes walking speed to match that imposed by the treadmill.
Sensory information changes if unexpected motor errors occur (for example, when an unexpected obstacle is encountered). This activates EXTEROCEPTIVE afferents that elicit cor-rective reflexes. The form of the reflex can depend upon the phase of the movement cycle in which the sensory input occurs (called PHASE-DEPENDENT REFLEXES). In cats, for example, tactile stimulation of the dorsal surface of the paw elicits limb flexion if the stimulus coincides with the stance (flexion) phase, but limb extension is evoked if the same stimulus occurs when the limb is on the ground during the stance phase.
Spinal CPGs are also influenced by systems of neurons in higher brain centres, especially those of the BRAINSTEM. Populations of brainstem neurons that influence locomotion form discrete clusters called nuclei. Brainstem nuclei interact with spinal CPGs in three ways: (1) initiation of locomotion; (2) fast adjustments to locomotion; and (3) slow modulation of locomotor intensity and frequency. Locomotor activity can be initiated following electrical stimulation of the so-called MESENCEPHALIC LOCOMOTOR REGION which might initiate locomotion by activating reticulospinal neurons. Once in progress, locomotion can be altered by activation of fast descending pathways. These pathways derive from particular brainstem nuclei and act on specific phases of the movement cycle. For example, DEITER’S NUCLEUS gives rise to the VESTIBULOSPINAL TRACT and is thought to regulate ipsilateral extensor activity; the RETICULAR FORMATION and the RED NUCLEUS give rise to the RETICULOSPINAL TRACT and the RUBROSPINAL TRACT and are thought to act on the flexion phase of the movement cycle. The intensity and duration of motor bursts during locomotion can also be modulated by descending brainstem pathways such as those from the LOCUS COERULEUS and the RAPHE NUCLEI. Most is known about the raphe nuclei whose neurons are predominantly SEROTONERGIC. Serotonin affects many aspects of CPG function but the main effect is to increase the intensity and duration of motor bursts in each cycle of locomotion.
There is considerable interest in the neural mechanisms of locomotion, both in their own right and for functional reasons. The analysis of gait, posture and the pattern of running and walking is, for instance, of considerable value to professional athletes and to physiotherapists developing rehabilitation programmes for pa tients who have suffered injuries. In psychopharmacological studies of animals, locomotion is often examined to determine whether or not a treatment of some sort—typically drug administration—has a generalized effect on behaviour. It is assumed (not always correctly) that if a drug has stimulant properties it will, in the absence of anything more interesting for the recipient to do, generate locomotion. For instance, AMPHETAMINE will increase selectively responding on a lever associated with CONDITIONED REINFORCEMENT (as opposed to a non-reinforced lever) but the doses of amphetamine that have this effect will also stimulate locomotion, if there is nothing else for the animal to do. Locomotion can thus be seen in this example as a ‘default activity’ in which an animal will engage if there is nothing more interesting to do. These actions of amphetamine have been associated not with brainstem mechanisms but with activation of dopamine systems in the NUCLEUS ACCUMBENS. Stimulation of the HIPPOCAMPUS can also elicit a strong locomotor response. There has been some debate in the literature about whether the locomotion stimulated from the nucleus accumbens and hippocampus is merely activation or EXPLORATION.
The measurement of locomotion in laboratory animals can be done in several ways. The simplest way is to count the numbers of times an animal crosses floor markers. If an arena is divided on the floor into quadrants, the numbers of crosses from one quadrant to another can be counted, either by direct observation or from video recordings. Rather more sophisticated are cages equipped with photocell beams that detect and register movement without an animals being aware of the recording. Hinged floor plates which activate microswitches are occasionally used to give similar output, though movement of the floor can distract an animal. Exploration can be measured in a BERLYNE BOX, CARLSON BOX OF HOLEBOARD TEST. OPEN FIELD locomotion can also be measured. In these, animals will typically restrict their movements to the perimeter until they have became accustomed to the environment. Movement into the centre of an open field can therefore be used experimentally to measure degrees of NEOPHOBIA or ANXIETY.
References
Robbins T.W. (1997) A critique of the methods available for the measurement of spontaneous locomotor activity, in Handbook of Psychopharmacology, vol. 7, Prindples of Behavioral Pharmacology,, eds Iversen L.L., Iversen S.D. & Snyder S.H., pp.37–82, Plenum Press: New York.
Sillar K.T. (1994) Synaptic specificity: development of locomotor rhythmicity. Current Opinion in Neurobiology 4:101–107.
KEITH T.SILLAR
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