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Activity of Spindle Merents from Cat Anterior Thigh Muscles. I

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Activity of Spindle Merents from Cat Anterior Thigh Muscles. I JOURNALOF NEUROPHYSIOLOGY Vol. 54. No. 3. September 1985. Prinled in U.S.A. Activity of Spindle Merents From Cat Anterior Thigh Muscles. I. Identification and Patterns During Nornid Locomotion G. E. LOEB, J. A. HOFFER, AND C. A. PRATT Laboratory of Neural Control, IRP, National Institute of Neurological and Communicative Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20205 SUMMARY AND CONCLUSIONS 6. Activity from spindle secondary endings 1. The naturally occumng activity patterns was generally lower, more regular, and less ve- of anterior thigh muscle spindle afferents were locity dependent than that from primary end- recorded during unrestrained treadmill loco- ings, consistent with their lack of input from motion by means of floating microelectrodes the dynamic fusimotor apparatus. chronically implanted in the fifth lumbar dor- 7. The activity of all spindle afferents stud- sal root ganglion. ied was similarly well modulated during ex- 2. Conduction velocity of units from pri- trafusal activity of the parent muscles, regard- mary and secondary endings was determined less of the kinematic conditions of muscle by spike-triggered averaging of the signals from length and velocity during which this muscle a chronically implanted nerve cuff. work occurred. This suggests that the fusi- 3. Activity from knee extensor muscle motor apparatus is well orchestrated to regu- spindles generally occurred during periods of late the static and dynamic sensitivity of pri- muscle lengthening, but was often greater for mary spindle afferents at levels appropriate to small stretches when the muscle was active the anticipated motion. (during stance phase of walking) than for larger INTRODUCTION stretches when the muscle was passive (swing phase), indicating fusimotor enhancement of By virtue of their numbers, speed, and sen- spindle sensitivity in phase with extrafusal sitivity, muscle spindle afferents seem well muscle recruitment. suited to providing much of the information 4. Activity from spindles in biarticular available to the spinal cord regarding the po- muscles acting across the knee and hip was sition and motion of the limb segments. Their more variable and complex than that seen in strong and widespread synaptic terminations the pure knee extensors, and frequently in- directly on motoneurons and on interneurons cluded activity during rapid muscle shortening subserving local motor control circuits, as well (swing phase) indicative of strong static fusi- as their contribution to ascending pathways, motor input. support this presumption further. However, 5. Changes in speed of gait caused changes the nature of the information that they provide in the range and velocity of muscle length ex- is difficult to predict from their receptor prop- cursions monitored by chronically implanted erties because these properties are so highly length gauges, but such changes were accom- dependent on the mechanical activity of the panied by only modest changes in spindle af- intrafusal muscle fibers, which are under the ferent activity, suggesting concurrent and continuous and rapidly modulatible control compensatory changes in fusimotor influence of gamma and beta motoneurons (for reviews on spindles. see Refs. 7, 29). 550 LOEB, HOFFER, AND PRATT In this and the accompanying two papers, ity and nonlinear interaction of the various we report the results of chronically recording fusimotor influences on spindles preclude the activity of single muscle spindle afferents quantitative assessment of fusimotor activity during unrestrained, normal behavior. We from these records, they do provide a general have examined the effects of various behaviors indication of the degree to which normal mo- on the afferent activity of different spindles in tor behavior is accompanied by fusimotor the same muscle and across different muscles programs that are specific to each muscle and and have contrasted these activity patterns the task of the moment. Furthermore, because with the sensitivity of these afferents to similar of the distinctive effects of gamma dynamic length changes applied to relaxed muscles in and gamma static fusimotor input on spindle the anesthetized state. Although the complex- afferent5 during states such as rapid muscle FIG. I. A: innervation of the anterior thigh muscles of the cat and the relationship to the instrumentation implanted for these studies. DRG, array of up to 12 individual metal microelectrodes implanted in the 5th lumbar dorsal root ganglion; IT, tripolar electrode configuration in the proximal half of the femoral nerve cuff electrode; FD, tripolar electrode configuration in the distal half of the femoral nerve CURSaph. n. and Hamst. n., bipolar nerve cuffs used for stimulation experiments reported elsewhere (25); SA-a, bipolar EMG patch electrode on anterior part of sartorius muscle; SA-m, bipolar patch electrode on medial sartorius; RF, multipolar EMG spiral electrode in rectus femoris muscle; VM, spiral electrode in vastus medialis muscle; VI, spiral electrode in vastus intermedius muscle; VL, spiral electrode in vastus lateralis muscle; LV,length gauge across vastus muscles (knee joint only); LR, length gauge across rectus femoris and anterior sartorius muscles (knee and hip joints); Fp, strain gauge mounted on patellar ligament. SPINDLE ACTIVITY 551 shortening, it is occasionally possible to draw This paper describes the functional anatomy specific inferences about the nature and and kinematic and electromyographic patterns strength of fusimotor influence. of the anterior thigh muscles during normal Afferent unit recordings were obtained from locomotion, together with the simultaneously cell bodies or axons located in the fifth lumbar recorded activity of identified single spindle dorsal root ganglion (L5 DRG). About half of afferents. Two companion papers describe our the afferents in this ganglion derive their input attempts to dissociate intra- and extrafusal ac- from receptors in the median articular nerve tivity by fusimotor blockade (23) and by reflex- of the knee, the cutaneous saphenous nerve, generating stimuli (25). Preliminary reports and the motor nerves innervating the sartorius regarding the activity of 8 of the 23 units re- and quadriceps femoris muscles (see Fig. 1). ported here have been published previously All of these nerves together comprise the entire (10, 18, 24); none of the activity patterns femoral nerve as it passes through the inguinal shown here include those units, but conclu- canal, where its long, straight, and unbranched sions and summaries are based on the entire course permits the chronic implantation of a population. multilead nerve cuff. By using the method of spike-triggered averaging of the neurogram MATERIALS AND METHODS recorded at two points along the nerve, a uni- tary potential recorded in the L5 DRG can be Ten adult male cats ( Felis domesticus) were im- unequivocally associated with an afferent fiber planted with all or most of the various devices in- having a particular conduction velocity and dicated in Fig. 1, with aseptic surgical techniques innervating one of the above noted receptor- and general anesthesia consisting of intraperitoneal bearing structures. Because these structures are pentobarbital (45 mg/kg) followed by maintenance doses of intravenous pentobarbital. Surgery was all large, superficial, and relatively simple me- usually performed in two stages, with the peripheral chanically, manual manipulation and the ap- transducers of length and force and the nerve and plication of vibrating probes can be used to muscle electrodes implanted one week prior to im- further localize and characterize these afferents plantation of the recording microelectrodes in the with little ambiguity. DRG. All animals were walking normally within HG. 1. B: schematic representation of the typical walking step cycle showing the stance phase (E2-3,heavy line at bottom) and 2 complete swing phases divided into flexion phase (F) and first extension phase (El). The length and EMG records indicate the most commonly seen pattern under technically ideal conditions. Actual records tended to have minor variations as a result of variability of gait among steps and across animals and occasional hardware problems such as inadequately tensioned length gauges or mispositioned EMG electrodes. 552 LOEB, HOFFER, AND PRATT several days after each surgery when the effects of desired length using scissors. Each gold lead, in turn, anesthesia had worn off. Unit records were usually was welded to a multistranded stainless steel lead obtained in the second to fifth postoperative weeks. anchored within silicone rubber tubes mounted on Both the implanted devices and the external con- the dorsal spinous processes, to provide a flexible nector were well tolerated throughout the course of and strong percutaneous lead to the connector the experiment, with no apparent discomfort or ir- mounted outside on the back of the animal. The ritation either during recording sessions or between welds were reinforced with epoxy, and the entire them, although some animals favored the operated assembly overcoated with Parylene insulation, the leg for the first few postoperative days (see Fig. 5). deposition of which is detailed elsewhere (2 1). The Figure 2 shows a detail of the microelectrode im- L5 DRG was exposed through the usual midline plantation and fixation technique together with the dorsal dissection of soft tissues followed by a small general strategy for maintaining a stable, long-term burr hole (-3
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