56 SECTION 1 Exercise and Responses of Biologic Systems
Sources of Peripheral Sensory Information
CHAPTER 2 The Nervous System and Movement 57 all of the skeletal muscles and joints, more than one-half
of the axons in the muscle nerves are sensory and most of the body mass is comprised of muscle. Thus, if one considers only the muscle nerves, one must expect that exercise and motor training can play a signifi cant role in shaping how the CNS functions. Among these sensory axons are a number of types of mechanoreceptors that are capable of detecting changes in muscle length, force, and pressure. In addition, some nerve branches are essentially all or predominantly sensory and they project to tendons, joints, and skin. One of the most studied mechanoreceptors is the skeletal muscle spindle that provides proprioceptive information to the CNS (54).
During exercise, the brain also receives input from axons that convey touch, sound, vision, smell, and taste and these sources of information infl uence the physiol- ogy of the CNS. There are many examples of ways these sensory systems affect our motor performance, refl ecting the fact that each of these sensory modes has input to the motor system. A loud sound can increase voluntary strength. Cutaneous cues shape our reactions in main- taining posture and in the kinematics of locomotion.
Vision is a major source of input for guiding virtually all movements. Sound can direct our posture and head position. Even olfactory input can initiate locomotor movements.
Muscle spindles
A muscle spindle consists of about four to six small muscle fi bers surrounded by a collagenous sheath. The maximum diameter of the collagenous sheath usually approximates the size of the extrafusal muscle fi bers. The muscle fi bers within the capsule are striated, similar to the extrafusal muscle fi bers—these are intrafusal muscle fi bers. The ends of these intrafusal fi bers commonly proj- ect beyond the clearly defi ned spindle capsule. The intra- fusal fi bers are innervated by -motoneurons and each intrafusal muscle fi ber is surrounded by several sensory axons called primary and secondary spindle afferents (Fig. 2.22). These sensory axons generate action potentials when the length of the intrafusal fi ber changes. Stretch of the intrafusal fi bers can be caused by two events: (a) acti- vation of the -motoneurons, which will cause shortening of the distal ends of the intrafusal fi bers and, therefore, stretch the center where the annulospiral sensory nerve endings are; and (b) passively lengthening or shorten- ing the intrafusal fi bers because they lie parallel and are physically attached indirectly to the extrafusal muscle fi bers. Very small changes in length can stimulate the primary (also referred to as Ia afferents) and secondary sensory fi bers from the spindle. In general, the primary afferents from the muscles spindles demonstrate a more dynamic response, whereas the secondary fi bers have a more static response to changes in length. The primary Ia fi bers are the main afferents responding to a tendon tap and vibration (55).
FIGURE 2.22 A muscle spindle attaches at its ends to connective tissues within a muscle. Sometimes two or even three spindles are interconnected in series. A con- nective tissue capsule surrounds three to eight intrafusal fi bers located within each spindle. Motor end plates are located at the ends of each intrafusal fi ber. These end- plates represent the junction of the -motoneuron with the intrafusal muscle fi ber and provide a mechanism for inducing the intrafusal fi ber to shorten or place tension on the center of the muscle fi ber. This increased tension triggers action potentials in the sensory endings—that is, annulospiral (primary) and fl ower spray (secondary) afferent fi bers. These endings also can be activated by passively stretching the muscle and therefore the spindles. The afferent input projects to the spinal cord making synaptic contact on most motoneurons that project to that muscle. This input also projects to some motoneurons that innervate synergistic muscles, as well as to interneurons that inhibit motoneurons innervating antagonistic muscles. (Modifi ed from Ross M, Romrell L, Kaye G. Histology: A Text and Atlas . 3rd ed. New York:
Harper and Row; 1995:227.) Primary
(annulospiral) endings
Nuclear bag
γ-Efferent fiber
Motor end plates
Extrafusal muscle fibers
Aponeurosis
Secondary afferent fiber
Primary afferent fiber
γ-Efferent fiber
Secondary flower-spray endings
Intramuscular nerve trunk
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58 SECTION 1 Exercise and Responses of Biologic Systems
active during all phases of the step cycle to sustain some sensitivity of the spindle to the intramuscular mechanical events (55).
One of the most common ways to demonstrate the responsiveness of muscle spindles to stretch is to tap the tendon to trigger a muscle contraction. Tapping the tendon induces a monosynaptic refl ex by activating the spindle afferents that project to the dendrites of the motoneurons associated with the same muscle containing the spindle.
Each spindle afferent sends axonal branches to nearly every motoneuron within that motor pool and to a signifi cant proportion of the motoneurons that innervate synergistic muscles (56). In addition, the same Ia afferent from the spindle projects to interneurons that inhibit the motoneu- rons innervating antagonistic muscles (Fig. 2.24).
One can vibrate a muscle-tendon unit with a wide range of cycle frequencies such that the peak-to-peak change in length is 1 mm. This stretch will activate the Ia afferents that, in turn, will excite motoneurons innervating that muscle, and thus enhance its force gen- eration even when the muscle is fatiguing during a MVC (Fig. 2.25).
The density of muscle spindles varies widely among muscles. Muscles or muscle regions having a high percent- age of slow fi bers usually have a relatively high incidence of spindles and thus are highly sensitive to length changes (57). The intrinsic muscles of the hip, for example, have a high spindle density, are extremely sensitive to length
Afferents during locomotion
Some specifi c examples of how Ia fi bers form muscle spindles in the ankle extensors (plantarfl exors) of the cat function during locomotion are shown in Fig. 2.23. In Fig. 2.23A, the spindle was fi ring throughout the step cycle with the frequency being modestly higher during stance ( i.e. E1 through E3). The E1 phase is the extension of the limb at the end of the swing phase prior to paw contact. The E2 phase begins at paw contact and extends to the end of the yield phase of stance. The E3 phase continues through- out the remainder of the stance phase. In Fig. 2.23B, again, the spindle Ia is activated throughout the step cycle but at a higher fi ring rate during E2 and E3. Also, the level of acti- vation of the extensor muscle was higher in Fig. 2.23B than in Fig. 2.23A. In early E1 in Fig. 2.23B, a few pulses with a very short interpulse interval can be seen. Fig. 2.23C shows a similar pattern to that in Fig. 2.23A and B, but in the fi rst step cycle shown the highest fi ring frequency occurred at mid E3, whereas in the next step, it occurred at mid E1. This emphasizes the variation in the details of the activation patterns of - and -motoneurons, not only among different afferent fi bers but even from step to step for the same afferent. This step-to-step variability is a steadfast feature of locomotor networks even under the most controlled conditions possible. All three of these examples illustrate the likelihood that the -motoneurons innervating the intrafusal muscle fi bers were suffi ciently
E2 − E3 F E1 E2 − E3
A
E2 − E3 F E1 E2 − E3
500 μV
B
E2 − E3 E2 − E3 F−
200 ms E1
F
C
100 μV 200 i/s
500 μV
200 i/s 100 μV
FIGURE 2.23 Discharge trains of intermediately active ( A and B ) and very active ( C ) ankle extensor spindle primary afferents during step cycles. Upper traces: lateral gastrocnemius electromyography (EMG);
lower traces: afferent discharges and their instantaneous fi ring rate. All three afferents showed slightly different fi ring patterns, but each had a higher fi ring rate during stance. C represents the most extreme degree of presumed - coactivation observed since the afferents were active during the phase of the cycle when the muscle was shortening. Note lack of correspondence between primary afferent fi ring rate and EMG amplitude. (Reprinted with permission from Prochazka A, Westerman RA, Ziccone SP. Dis- charges of single hindlimb afferents in the freely moving cat. J Neurophysiol . 1976;39:1090–1104.)
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CHAPTER 2 The Nervous System and Movement 59
some muscles and inhibit others, with these effects being highly state-dependent. For example, the specifi c neurons that are excited or inhibited can change with the phase of a step cycle and probably other physiologic condi- tions. A third type of muscle mechanoreceptor is referred to as free nerve endings because there is no remark- able specialization at the ends of these axons. These free endings generate action potentials when excited by mechanical as well as biochemical or metabolic stimuli (metaboreceptors). Free nerve endings actually constitute most of the sensory endings from muscle. Their function is not well understood, although they are thought to be actively involved in muscle spasticity in individuals with a spinal cord injury.
From the perspective of the systems level, all of the muscle spindle afferents, GTOs, and free nerve endings serve as mechanoreceptors that provide important infor- mation associated with proprioception.
changes and provide very important information for mod- ulating the motor output during routine motor tasks such as stepping (58). These length sensors provide important cues as to when the stance and swing phases of a step should begin and terminate and when the body weight is being shifted from one leg to the other while standing.
Other mechanoreceptors
Another mechanoreceptor within the muscle tendon unit is the GTO. In spite of the name, most GTOs are within the muscle. They are able to detect small changes in force generated within the muscle. The high level of sensitiv- ity to force of the GTOs contrasts with the traditional concept that they are activated only by high forces and that their function is to prevent tendon injury by inhibit- ing the muscle from generating excessive forces (54,59).
The sensory information generated by GTOs will excite
FIGURE 2.24 Spinal connections between sensory receptors located in muscle and motoneurons. The Ia axon conveys afferent information from the muscle spindle to the CNS. The Ib axon represents a similar connection but from the tendon organ.
A. Homonymous relationships: muscle spindles and tendon organs located in a mus- cle connect with the motoneurons that activate the same muscle. Afferent and efferent axons that service muscles located on the right side of the body enter and exit the spinal cord on the right side, and vice versa. B. The same connections for an agonist–antagonist muscle set ( e.g. , the hamstrings and quadriceps for the right leg) but this time emphasizing the complexity of the interneuronal connections.
Also note the input from the brain to the same interneurons that receive peripheral afferent input from the muscles. Open circles represent excitatory connections; fi lled circles indicate inhibitory effects; , alpha motoneuron; , gamma motoneurons;
I, Ia inhibitory interneuron; 1a, muscle spindle afferent; 1b, tendon organ afferent;
R, Renshaw cell. (Modifi ed from Enoka R. Neuromechanical Basis of Kinesiology . Champaign, IL: Human Kinetics; 1988:139.)
Supraspinal Input
B A
l b l b
l a l a
Spinal cord
Peripheral nerve
Muscle set
γ α α γ
l
l l
l
R R
l b l a
α
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60 SECTION 1 Exercise and Responses of Biologic Systems
state. Even the effi cacy of the monosynaptic input from muscle spindles to the motoneuron changes readily from one portion of the step cycle to another and according to whether a subject is running or walking (60,61).
Smart responses in the spinal cord of humans
Another excellent example of the ability of the spinal cord to receive complex proprioceptive input and to use this information in a functional way was shown by Harkema and associates (62) (Fig. 2.26). These authors demon- strated that the level of activation of an extensor muscle, the soleus, is modulated according to the amount of load that is placed on the lower limbs of a human subject. In the example on the left of Fig. 2.26, the increase in the level of activation, as illustrated by the EMG amplitude, is directly related to the load imposed on the limb. The results of a similar experiment on a subject who has a complete spinal cord injury (no voluntary control of any muscles below the lesion and no sensation from tissues below the lesion) are shown on the right of Fig. 2.26. The similarity of the rela- tionship between the level of loading and the level of acti- vation of the motor pool (EMG amplitude) in the uninjured and the complete spinal cord injured subjects demonstrates that the spinal cord circuitry is able to sense the level of load and activate the soleus and other motor pools accord- ingly. Two of several interpretations of how the spinal cord senses load “online” are (a) sensory receptors in the limbs ( e.g. , soles of the feet, tendons, muscles, and joints) that specifi cally sense load; and (b) an ensemble of many types of sensory receptors at multiple locations within the limbs generate a highly recognizable “image” to inform the spinal circuitry of the biomechanical status of the weight bearing.
The second interpretation is the one we favor. It is consis- tent with the concept that has been alluded to many times previously—that is, it is the ensemble of sensory input that As noted previously, mechanoreceptors seem to have
specialized in the periphery, which enables them to pro- vide detailed information about the kinematics of a move- ment from a micro and macro perspective and also from a dynamic and static perspective.
FIGURE 2.25 Vibration of the tibialis anterior temporarily counteracts ( A ) the decline in motor unit fi ring rates and ( B ) muscle force that occurs during a maximum voluntary con- traction of foot dorsifl exors. (Modifi ed from Bongiovanni LG, Hagbarth KE. Tonic vibration refl exes elicited during fatigue from maximal voluntary contractions in man. J Physiol . 1990;423:1–14.)
Motor Unit Firing Rate (Hz)
10
0 20 30 40
A Vibration
Force (N)
150
100 200 250 300
B Vibration
10 s 10 s
KEY POINT
Proprioception is a broad term often used to convey the idea that there are sensory receptors that pro- vide precise information to the spinal cord and brain regarding the exact biomechanical state of the muscu- loskeletal system at any given time.
KEY POINT
The combined effect of all of these mechanorecep- tors projecting to the spinal circuits is to provide an ensemble of sensory information that provides the instructions needed for the spinal cord to control and modulate the kinematics of the movements in a very predictable way, thus minimizing the necessity for supraspinal (conscious) control of routine movements.
As noted previously, an important basic neurophysi- ologic concept with respect to proprioceptive input from the mechanoreceptors, as well as cutaneous receptors, is that their synaptic functional connectivity to the spinal cir- cuitry is highly dynamic. The connectivity between these mechanoreceptors and specifi c interneuronal populations within the spinal cord vary according to the physiologic
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