Information-theoretic analysis of de-efferented single muscle spindles

 The information transmission properties of single, de-efferented primary muscle-spindle afferents from the hind limb of the cat were investigated. The gastrocnemius medialis muscle was stretched randomly while recording spike trains from several muscle-spindle afferents in the dorsal root. Two classes of input stimuli were used: (i) Gaussian noise with band-limited flat spectrum, and (ii) Gaussian noise with a more “naturalistic” 1/f ⁿ spectrum. The “reconstruction” method was used to calculate a lower bound to the information rate (in bits per second) between the muscle spindles and the spinal cord. Results show that in response to the flat-spectrum input, primary muscle-spindle afferents transfer information mainly about high frequencies, carrying 2.12 bits/spike. In response to naturalistic-spectrum inputs, primary muscle-spindle afferents transfer information about both low and high frequencies, with “spiking efficiency” increasing to 2.67 bits/spike. A simple muscle-spindle simulation model was analyzed with the same method, emphasizing the important part played by the intrafusal fiber mechanical properties in information transmission. Received: 22 January 2002 / Accepted in revised form: 17 June 2002 Correspondence to: Y. Tock (e-mail: ytock@tx.technion.ac.il, Fax: +972-4-8323041)     

Spontaneous activity of passive muscle spindles of the cat triceps surae muscle

The hypothesis that one possible cause of the spontaneous discharge of muscle spindles in the totally relaxed and de-efferented triceps surae muscle, with its tendon divided, is the mechanical factor due to extrafusal-intrafusal interaction was tested in experiments on anesthetized cats. Responses of spontaneously active units were similar with respect to many indices to responses of silent receptors capable of generating a long discharge in response to an increase in static length of the muscle. Isotonic contraction of the relaxed muscle during direct or indirect stimulation was accompanied by a pause in spontaneous activity. The prolonged increase in discharge frequency sometimes arising as a result of pressure on the muscle in the region of the receptor also was abolished by weak isotonic contraction of the muscle. If a long posttetanic sensory discharge was induced in a spontaneously active receptor by intensive tetanization of the nerve to the muscle, and it was then abolished by short stretching of the muscle, the initial spontaneous discharge frequency was restored. The dynamic thresholds of spontaneously active receptors were lower than for silent receptors. In some spontaneously active receptors an initial slowing of the discharge was observed during linear or stepwise stretching of the muscle. It is suggested that the ability of sensory endings to generate a long spontaneous discharge is due to initial stretching of the spindle inside the relaxed muscle.I. P. Pavlov Institute of Physiology, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 10, No. 3, pp. 287–294, May–June, 1978.     

Myofibrillar ATPase activity of intrafusal fibers in chronically de-afferented rat muscle spindles

Summary Dorsal root ganglia L₄, L₅ were removed to accomplish long-term (1 year) de-afferentation of the rat soleus muscle. Muscle spindles in the muscles deprived of sensory innervation were morphologically and histochemically abnormal. The spindle periaxial fluid space was greatly diminished with a thicker capsular investment. De-afferented intrafusal muscle fibers lacked either nuclear bags or nuclear chains at their midlengths. The intracapsular myofibrillar ATPase staining pattern of de-afferented nuclear bag fibers resembled that which the bag fibers normally display in their extracapsular regions. These abnormalities are discussed with respect to the regulatory functions of spindle sensory and motor nerves.     

Development of immunohistochemical characteristics of intrafusal fibres in normal and de-efferented rat muscle spindles

Summary Intrafusal muscle fibres in adult muscle spindles differ in their myosin composition. After selective motor denervation intrafusal muscle fibres develop mature ultrastructural characteristics. In order to evaluate the role of fusimotor innervation on the maturation of the myosin composition of intrafusal muscle fibres we have examined with immunohistochemical techniques i) the postnatal development of muscle spindles in new-born rats and in 7–21 day old rats; ii) muscle spindles in the EDL of 21-day-old rats de-efferented at birth. For the characterization of myosins in intrafusal fibres we used three myosin antisera: antipectoral myosin, antiheart myosin and antiheart myosin adsorbed with muscle powder from the soleus muscle of guinea pig. We show in this study that during development intrafusal fibres change immunoreactivity and that in the absence of motor innervation bag fibres do not fully develop the myosin characteristics of control spindles. We conclude that the maturation of bag₁ and bag₂ fibres apparently requires next to the inductive influence of sensory axon terminals the presence and activity of fusimotor axons.     

Development of immunohistochemical characteristics of intrafusal fibres in normal and de-efferented rat muscle spindles

Intrafusal muscle fibres in adult muscle spindles differ in their myosin composition. After selective motor denervation intrafusal muscle fibres develop mature ultrastructural characteristics. In order to evaluate the role of fusimotor innervation on the maturation of the myosin composition of intrafusal muscle fibres we have examined with immunohistochemical techniques i) the postnatal development of muscle spindles in new-born rats and in 7-21 day old rats; ii) muscle spindles in the EDL of 21-day-old rats de-efferented at birth. For the characterization of myosins in intrafusal fibres we used three myosin antisera: antipectoral myosin, antiheart myosin and antiheart myosin adsorbed with muscle powder from the soleus muscle of guinea pig. We show in this study that during development intrafusal fibres change immunoreactivity and that in the absence of motor innervation bag fibres do not fully develop the myosin characteristics of control spindles. We conclude that the maturation of bag1 and bag2 fibres apparently requires next to the inductive influence of sensory axon terminals the presence and activity of fusimotor axons.     

One-bag-fiber muscle spindles in tenuissimus muscles of the cat

Summary Over 150 complete and 139 incomplete single muscle spindles were examined in serial transverse sections of cat tenuissimus muscles in search for spindles lacking one of the two types of nuclear bag intrafusal fiber. Several histochemical reactions were used to type the intrafusal muscle fibers and assess the spindle motor and sensory innervation. One complete spindle lacked a bag₁ fiber, and another spindle lacked a bag₂ fiber. Several incomplete spindles also lacked bag₁ fibers. In addition, ten double tandem spindles contained one capsular unit each that lacked the bag₁ fiber, and one triple tandem spindle had two such capsules. All one-bag-fiber spindles had primary sensory innervation, but none had secondary sensory innervation. Their motor innervation was similar to that of the usual two-bag-fiber spindles in the number and disposition of intrafusal motor endings. It is unclear whether the one-bag fiber spindles, either single or tandem-linked, are products of an aberrant spindle development or represent a true anatomical and functional subcategory of the cat muscle spindle.     

Multiple-bag-fiber muscle spindles in tenuissimus muscles of the cat

Over 300 complete and incomplete cat muscle spindles were examined in serial transverse sections of tenuissimus muscles in search of spindles with more than two nuclear bag intrafusal muscle fibers. Several histochemical and histological stains were used to identify the intrafusal fibers and assess their motor and sensory innervation. About 13% of the spindles contained either three or four bag fibers rather than the usual two. Every multiple-bag-fiber spindle possessed at least one nuclear bag1 and one nuclear bag2 fiber. The supernumerary bag fibers were either another bag1 and/or bag2 fiber, or a mixed bag fiber. The extra bag fibers had the usual morphologic and histochemical properties of cat nuclear bag fibers. All multiple-bag spindles received primary sensory innervation, and most had secondary sensory endings in addition. Their motor pattern was similar in the number, appearance and disposition of intrafusal motor endings to that of the usual two-bag-fiber spindles. Bag fibers of the same kind shared motor nerve supply in three multiple-bag spindles in which tracings of individual motor axons were obtained histologically. It is unclear whether any functional advantage is conveyed to a muscle spindle by its having more than one bag1 and one bag2 fiber.     

One-bag-fiber muscle spindles in tenuissimus muscles of the cat

Over 150 complete and 139 incomplete single muscle spindles were examined in serial transverse sections of cat tenuissimus muscles in search for spindles lacking one of the two types of nuclear bag intrafusal fiber. Several histochemical reactions were used to type the intrafusal muscle fibers and assess the spindle motor and sensory innervation. One complete spindle lacked a bag1 fiber, and another spindle lacked a bag2 fiber. Several incomplete spindles also lacked bag1 fibers. In addition, ten double tandem spindles contained one capsular unit each that lacked the bag1 fiber, and one triple tandem spindle had two such capsules. All one-bag-fiber spindles had primary sensory innervation, but none had secondary sensory innervation. Their motor innervation was similar to that of the usual two-bag-fiber spindles in the number and disposition of intrafusal motor endings. It is unclear whether the one-bag fiber spindles, either single or tandem-linked, are products of an aberrant spindle development or represent a true anatomical and functional subcategory of the cat muscle spindle.     

Appearance of sensory nerve terminals in cat muscle spindles stained for NADH-tetrazolium reductase

Cat muscle spindles were studied histochemically in serial transverse sections of the tenuissimus muscle stained for myofibrillar ATPase, cholinesterase or NADH-tetrazolium reductase. The terminal sites of the primary and secondary axons on intrafusal muscle fibers could be demonstrated due to their high NADH-TR activity. This sensory NADH-TR reactivity at the equator and in the juxtaequatorial regions disappeared following spindle chronic de-afferentation, but not after de-efferentation. Spindle poles that carried both primary and secondary sensory endings had a longer periaxial fluid space than poles with primary endings only, and their motor innervation, as determined by staining for ChE, was positioned at the greater distance from the equator. Some of the secondary endings occurred in intrafusal regions that displayed surface fiber ChE activity. The histochemical reaction for NADH-TR represents a simple, rapid and reliable method for studies of the distribution of sensory nerve terminals in the spindle.     

Effects of stimulating the lumbar sympathetic trunk on cat hindlimb muscle spindles

1. The effect of stimulating the lumbar sympathetic trunk has been observed on cat lumbrical and tenuissimus muscle spindles. 2. Spindle afferent discharges were recorded either from single Ia fibers in teased dorsal root filaments or from a large number of spindles by integrating their discharges led from muscles nerves. 3. Blood flow in small arteries supplying the muscle was observed through a microscope during and after the stimulation of the sympathetic trunk. 4. In some spindles repetitive stimulation of the sympathetic trunk elicited, after a few seconds delay, a small increase in firing rate. This can be ascribed to a direct action of sympathetic axons on the spindles because it precedes by about 20-30 sec the reduction of blood flow observed in the muscle arteries. This effect is not accompanied by a change in dynamic sensitivity of the primary ending. 5. This early effect is followed, after 20-30 sec, by a later rise in firing frequency which still progresses after the end of stimulation and eventually terminates in an abrupt fall in firing often leading to interruption of the ending activity. Recovery takes places at a variable time after the blood flow has bee reestablished. These long lasting effects can be ascribed to reduction of blood flow in muscle spindles since they are always associated with changes in blood flow in muscle arteries and since they are mimicked by occlusion of the muscle circulation. 6. In some spindles, the amplitudes of frequencygrams elicited by stimulation of static gamma axons were slightly increased suggesting a weak facilitatory effect on the contraction of some intrafusal muscle fibers.     

The organization of muscle spindles in the tenuissimus muscle of the cat during late development

Intrafusal muscle fibers in the tenuissimus muscle of the cat develop as two separate groups; one being a single nuclear bag fiber while the other comprises a second nuclear bag fiber along with all the nuclear chain fibers. The groupings are very distinctive in the late fetus (55 days gestation) and remain so until 18 days of age. In the adult, the grouping is less distinctive but can often be recognized and followed for considerable distances within the capsular region of the spindle. Each group develops under its own basement membrane and is separated from the other by fibrocytes. ATPase histochemistry indicates the isolated single nuclear bag fiber is slow twitch while the fibers of the other group, the second bag and all the nuclear chains, are fast twitch. The organization of intrafusal fibers in late development into two groups of different fiber types is discussed in relation to their selective innervation by γ fibers.     

Observations on the primary sensory ending of tenuissimus muscle spindles in the cat

Summary The arrangement of preterminal and terminal axon branches in the primary sensory endings of cat tenuissimus muscle spindles was studied using whole-mount and serial-section techniques. Although in every case one firstorder preterminal branch was supplied exclusively to the bag₁ type of intrafusal muscle fibre, the preterminal branching patterns differed considerably in detail.Terminals varied widely in size and location. Their precise form varied according to their position on the intrafusal muscle fibres rather than their relationship to preterminal branches. Terminals derived from separate preterminal branches remained separate and did not fuse with themselves or each other. Individually bag₁ fibres had most terminals, chain fibres least. The surface of the muscle fibres were differentially indented by the terminals, least in bag₁ fibres and most in chain fibres.The results are discussed in relation to mechanosensory transduction and to the factors involved in determining the form of the primary ending.     

Motor innervation of the cat muscle spindle studied by the cholinesterase technique

Summary Muscle spindles were traced in serial transverse sections of cat tenuissimus muscles. Myofibrillar adenosine triphosphatase staining reaction was used to identify nuclear bag₁, nuclear bag₂ and nuclear chain intrafusal muscle fibers. Typical chain fibers and long chain fibers were distinguished, the latter extending for more than 1,000 m beyond the termination of the spindle capsule. Simple rim and more elaborate plate deposits were demonstrated histochemically along the poles of the typical chain fibers in staining for cholinesterases. They were considered to correspond, respectively, to the trail and plate motor nerve terminals. Most long chain fibers and the majority of nuclear bag fibers had their motor innervation limited to plate-type endings. In addition, faint diffuse cholinesterase staining occurred along the spindle capsule and the surface of some intrafusal fibers. These histochemical observations are discussed with regard to the current concepts concerning the morphological and functional organization of the motor innervation of the cat muscle spindle.