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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
S U M M A R Y A N D CONCLUSIONS (^) 6. Activity from spindle secondary endings
- The naturally occumng activity patterns
of anterior thigh muscle spindle afferents were
recorded during unrestrained treadmill loco-
motion by means of floating microelectrodes
chronically implanted in the fifth lumbar dor-
sal root ganglion.
- Conduction velocity of units from pri-
mary and secondary endings was determined
by spike-triggered averaging of the signals from
a chronically implanted nerve cuff.
- Activity from knee extensor muscle
spindles generally occurred during periods of
muscle lengthening, but was often greater for
small stretches when the muscle was active
(during stance phase of walking) than for larger
stretches when the muscle was passive (swing
phase), indicating fusimotor enhancement of
spindle sensitivity in phase with extrafusal
muscle recruitment.
- Activity from spindles in biarticular
muscles acting across the knee and hip was
more variable and complex than that seen in
the pure knee extensors, and frequently in-
cluded activity during rapid muscle shortening
(swing phase) indicative of strong static fusi-
motor input.
- Changes in speed of gait caused changes
in the range and velocity of muscle length ex-
cursions monitored by chronically implanted
length gauges, but such changes were accom-
panied by only modest changes in spindle af-
ferent activity, suggesting concurrent and
compensatory changes in fusimotor influence
on spindles.
was generally lower, more regular, and less ve-
locity dependent than that from primary end-
ings, consistent with their lack of input from
the dynamic fusimotor apparatus.
- The activity of all spindle afferents stud-
ied was similarly well modulated during ex-
trafusal activity of the parent muscles, regard-
less of the kinematic conditions of muscle
length and velocity during which this muscle
work occurred. This suggests that the fusi-
motor apparatus is well orchestrated to regu-
late the static and dynamic sensitivity of pri-
mary spindle afferents at levels appropriate to
the anticipated motion.
I N T R O D U C T I O N
By virtue of their numbers, speed, and sen-
sitivity, muscle spindle afferents seem well
suited to providing much of the information
available to the spinal cord regarding the po-
sition and motion of the limb segments. Their
strong and widespread synaptic terminations
directly on motoneurons and on interneurons
subserving local motor control circuits, as well
as their contribution to ascending pathways,
support this presumption further. However,
the nature of the information that they provide
is difficult to predict from their receptor prop-
erties because these properties are so highly
dependent on the mechanical activity of the
intrafusal muscle fibers, which are under the
continuous and rapidly modulatible control
of gamma and beta motoneurons (for reviews
see Refs. 7, 29).
550 LOEB, HOFFER, AND PRATT
In this and the accompanying two papers,
we report the results of chronically recording
the activity of single muscle spindle afferents
during unrestrained, normal behavior. We
have examined the effects of various behaviors
on the afferent activity of different spindles in
the same muscle and across different muscles
and have contrasted these activity patterns
with the sensitivity of these afferentsto similar
length changes applied to relaxed muscles in
the anesthetized state. Although the complex-
ity and nonlinear interaction of the various
fusimotor influences on spindles preclude
quantitative assessment of fusimotor activity
from these records, they do provide a general
indication of the degree to which normal mo-
tor behavior is accompanied by fusimotor
programs that are specific to each muscle and
the task of the moment. Furthermore, because
of the distinctive effects of gamma dynamic
and gamma static fusimotor input on spindle
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.
552 LOEB, HOFFER, AND PRATT
several days after each surgery when the effects of anesthesia had worn off. Unit records were usually obtained in the second to fifth postoperative weeks. Both the implanted devices and the external con- nector were well tolerated throughout the course of the experiment, with no apparent discomfort o r ir- ritation either during recording sessions or between them, although some animals favored the operated leg for the first few postoperative days (see Fig. 5).
Figure 2 shows a detail of the microelectrode im-
plantation and fixation technique together with the general strategy for maintaining a stable, long-term connection to the numerous implanted devices. The microelectrodes consisted of 50-pm diameter, plat- inum-20% iridium shafts with Pyre Tri-ML poly- imide insulation (California Fine Wire Co.) cross- welded to 25-pm diameter gold lead-out wires for flexibility. The recording surface was formed a t sur- gery by simply cutting the shaft obliquely to the
desired length using scissors. Each gold lead, in turn, was welded to a multistranded stainless steel lead anchored within silicone rubber tubes mounted on the dorsal spinous processes, to provide a flexible and strong percutaneous lead to the connector mounted outside on the back of the animal. The welds were reinforced with epoxy, and the entire assembly overcoated with Parylene insulation, the deposition of which is detailed elsewhere (2 1). The
L5 DRG was exposed through the usual midline
dorsal dissection of soft tissues followed by a small
burr hole (-3 X 5 mm) through the overlying bony
lamina. These electrodes were inserted by hand into
the DRG through small scalpel slits, with fine for-
ceps with tips ground to receive the reinforcing epoxy ball. Typical electrode impedances were 100-
300 kQ at I kHz; impedance was measured daily
prior to recording and proved to be a sensitive in- dicator of the loss of recording sources due to
FIG. 2. Detail of microelectrode, nerve cuff, and back-pack connector fixation. The silicone rubber tube array (TA) mounted on the L, and L6 dorsal spines carries the joint between the gold leads of the dorsal root ganglion (DRG) electrodes and the stranded, stainless steel percutaneous leads (L) that are soldered to the printed circuit boafd (PCB) mounted as a back pack via anchoring sutures (AS) through the L4and L, dorsal spines. The femoral nerve cuff (FNC) carries five circumferential contacts whose percutaneous leads (L) terminate similarly on PCB along with an intraluminal catheter (IC). For recordings, multipin connector C mates with a connecting ribbon cable and 12-channel preamplifier; between sessions, a light-weight aluminum cap protects the percutaneous leads and joints from being snagged.
SPINDLE
breakage of leads or insulation. Typically, a total
of 12 such electrodes were implanted in the LSspinal
root structures, including variable numbers of sim-
ilar ventral root electrodes whose recordings are de-
scribed elsewhere ( 13).
The external connector assembly consisted of a
convexly curved sheet of Dacron reinforced silicone
rubber (Dow Corning Silastic #501-7) on which a
3 X 10 cm printed circuit board carrying a 40-pin
ribbon cable connector was affixed (3M Scotchflex
#3432), termination pads for soldering the percu-
taneous leads, and stainless steel nipples for receiv-
ing the implanted catheters and their caps. The as-
sembly was anchored to the animal's back by snugly
tied #5 Ethibond sutures that had been passed
through the skin and subcutaneous tissue and
through holes drilled in the dorsal spinous processes
of the L4 and L7 vertebrae. This floating mount was
tolerated without imtation or infection for many
months and accepted the load of the preamplifier
array and connector cable without interfering with
the animal's normal activities.
All of the other implanted devices have been de-
scribed previously. The two length gauges were
made from silicone rubber tubing (0.044" ID by
0.065" OD, Sil-Med Corp.), filled with hypertonic
saline (45 g/liter NaCl in water with blue vegetable
coloring), and equipped with stranded stainless steel
electrodes and leads in each end (26). They were
anchored proximally to bone screws and distally by
a criss-cross tendon suture just above the patella
(Fig. I). Length changes were monitored as changes
in the impedance of the fluid column using a 30
kHz AC bridge circuit, rectified and integrated with
a 100-Hz frequency response; most figures here
show at least one such length gauge signal plus an
electrically differentiated velocity trace. The length
calibrations were obtained by measuring the joint
angles occumng at the extreme excursions of a step
cycle from video stills and trigonometrically deter-
mining the muscle length with a mathematical
model of the origin, insertion, and pulley dimen-
sions obtained from all of these muscles in a cadaver
specimen of similar size. During walking, the lengths
of rectus femoris and both parts of sartorius muscles
are dominated by the hip joint motion, permitting
at least a first-order estimate of length from the ap-
propriately scaled output of a single implanted
gauge L, (see Fig. 6 and text). However, due to
various differences among animals regarding skel-
etal structure and internal muscle fiber architecture
and nonlinearities in the gauges and their curved
path motion, these records should be taken as ap-
proximate and are intended primarily for relative
comparisons. (See Ref. 26 for discussion of differ-
ences of muscle lengths determined by implanted
gauges and calculation from stick figures.) Gains
and DC offsets are unchanged for all of the records
shown in any single figure. The sign of the velocity
ACTIVITY 553
should always be correct, but the absolute value
may not be similarly calibrated over the entire ex-
cursion range of muscles with long lever arms such
as sartorius. Velocity calibrations were taken from
the midrange length excursions. Also, the method
of electronic differentiation to obtain velocity had
to be adjusted to compensate for high-frequency
noise in some length recordings, producing slight
phase lags in some velocity traces (e.g., Fig. 4).
The strain gauge on the patellar ligament em-
ployed a two-arm balanced-bridge configuration of
semiconductor elements (BLH #SPB 1-20-35-U 1)
epoxied to an E-shaped stainless steel substrate spe-
cifically designed for this broad, triangular shaped
ligament (30). Frequency response was flat from
DC to 100 Hz; calibrations are not given because
they drift over the implantation time and can only
be obtained accurately in situ in a terminal exper-
iment (26). These gauges tend to be quite linear,
and the records are intended for qualitative com-
parisons of force output and its temporal waveform;
gains and offsets are constant in any single figure.
The femoral nerve cuff consisted of a 2- to 3-cm-
long, longitudinally slit section of silicone rubber
tubing with a 2.8-mm ID (Sil-Med Corp.), equipped
with five equally spaced circumferential contacts
made from stranded platinum-10% iridium wire
(Medwire lOIR9149T). It was slipped over the fem-
oral nerve and tied closed with several circumfer-
ential sutures. Starting with the third cat in the series
reported here, the nerve cuffs were equipped with
catheters that permitted lidocaine solutions to be
instilled into the main lumen of the cuff from a
port on the connector assembly; results of these ex-
periments are described in a companion paper (23).
The transformer-coupled amplifier system (1- 10
kHz bandwidth) and spike-triggered averaging
techniques are described in detail elsewhere (12).
In the figures shown here, three buffered traces
(showing averages of signals that occurred before
as well as after the triggering signal) show the av-
eraged unit potential shape (as originally recorded
with 1- to 10-kHz bandwidth from the DRG mi-
croelectrode), the signal from the proximal tripolar
electrode (FT, center contact positive upward) and
the distal femoral tripolar electrode (FD). From the
time difference between the two negative peaks (de-
termined digitally) and the known separation be-
tween the two center contacts, the conduction ve-
locity has been calculated. Analysis of the errors to
which this method is subject indicate a 5% uncer-
tainty for the fastest conduction velocities and
somewhat less for those in the group I1 range (12,
34). Conduction velocities measured in this manner
may be slightly higher than those determined over
longer, more heterogeneous segments of peripheral
nerve where slowing may occur. The first five units
listed in Table 1 come from animals implanted with
a single tripolar femoral cuff. Conduction velocities
SPINDLE ACTIVITY 555
organ afferents were recorded but gave little or no
response to slow stretch of the passive whole muscle,
as would be expected (37). They were thus indis-
tinguishable from units that were lost before or
during the identification process. A small number
of tonically active units with no obvious source of
modulation or receptor fields were identified as in
previous recordings from similar chronically im-
planted electrodes (20). These probably represent
damaged fibers with spontaneous activity; occa-
sionally femoral nerve averages triggered by such
spontaneous spikes indicated an outgoing (anti-
dromic) direction. Electrical stimulation of muscles
via their chronically implanted EMG electrodes
provided useful clues regarding the location of
spindle receptors. However, both parallel unloading
from synergists and early twitch activation rather
than silencing could be produced with some stimuli
in some muscles, making this test less than conclu-
sive in this closely mechanically linked system.
RESULTS
Anatomical and functional organization of the muscles
The anterior thigh muscles of the cat, al-
though few in number, are mechanically and
kinematically quite diverse (see Fig. 1). The
three vastus muscles-intermedius (VI), me-
dialis (VM),and lateralis (VL)-make up three
of the four heads of the quadriceps, and act as
pure extensors of the knee. They are all
unipinnate (35) and take origin along an ex-
tended length of the femur and insert together
on the superior margin bf the patella. The
deepest lying VI is a red muscle composed al-
most exclusively of type I (presumably slow
twitch) muscle fibers, whereas the more su-
perficially lying parts of VM and VL are pro-
gressively whiter, with larger percentages of
type I1 (fast twitch) muscle fibers (3). All three
muscles were recruited synergistically during
the stance phase, with a small but consistent
phase difference. VI tended to be recruited
first, usually just before footfall, and its activity
tapered off well before the end of the stance
phase, whereas VM and particularly VL
tended to peak in mid to late stance, and to
cease activity more abruptly about 50-100 ms
before footlift (shown schematically in Fig.
1 B). The rectus femoris (RF), the fourth head
of the quadriceps, is a nonpinnate muscle that
takes origin along the wing of the ilium and
inserts with the vasti on the patella. Its mo-
ment arm about the hip joint, which it flexes,
is similar to that about the knee, but its overall
length changes during walking tend to be
dominated by the larger excursions of the hip
joint. At slow to moderate gaits (walking and
slow trotting), RF was recruited with the vasti,
although it tended to reach peak activity later
in the stance phase than any of the vasti (see
Fig. 5). At faster speeds, it usually had a burst
of EMG activity in mid to late swing phase,
synergistically with the anterior part of sar-
torius.
Sartorius is a mechanically complex muscle
that originates on the anterior iliac crest and
inserts in a continuous sheet extending from
the superior margin of the patella, along the
medial edge of the patella and its ligament,
and onto the anterior tibia1 ridge. The inner-
vating nerve bifurcates early, dividing the
muscle into an anterior part ( SA-a) with knee
extending action and a medial part (SA-m)
with knee flexing action. During walking, the
lengths of both parts tended to be similarly
dominated by the large lever arm acting
around the hip joint (but spindles in the two
parts of the muscle were readily differentiated
by their selective reaction to motion at the
knee joint when the hip was stabilized). The
anterior sartorius had two periods of extrafusal
activity: one during stance and one during
swing, predominately in the later El phase of
the Phillipson step cycle (3 1; Fig. 1B) when its
combined hip flexion and knee extension ac-
tions are both appropriate. The medial sar-
torius tended to have all or most of its activity
during the early to mid swing phase (depend-
ing on precise electrode placement), when its
combined knee and hip flexion actions are
both appropriate. We will deal with the an-
terior and medial parts as if they constituted
separate muscles, although there is no fascia
plane between them.
Spindle aferents identified Table I gives the coded name and putative
identity of each of the units that we identified
as spindle afferents from one of the six muscles
innervated by the femoral nerve distal to the
cuff electrode. The identification of a unit sen-
sitive only to knee flexion as originating in
any particular one of the three vasti is based
largely on the apparent locus of best response
to weak vibration. This is subjective at best
and subject to error; however, given the sim-
ilarity in mechanical action, fiber architecture,
and EMG recruitment of the three muscles,
556 LOEB, HOFFER, AND PRATT
such an error in-the classification of parent muscle would not affect the interpretation of the spindle activity. A similar consideration applies to the distinction between SA-a and RF, although the more superficial SA-a muscle provided a better subject for vibratory local- ization of the receptor. A couple of units re- sponded well to passive hip motion but only weakly to knee motion; these presumably came from the intermediate region of the SA muscle, which attaches to the medial edge of the patellar ligament, and hence has no exten- sor or flexoraction on the knee. From the conduction velocities, it is appar- ent that our method of recording was biased toward the larger, faster fibers, as noted pre- viously (20). In addition to the usual biases of extracellular recording electrodes, it is possible that many group I1 units with conduction ve- locities slower than 72 m/s were recorded but not identified as passing through the femoral nerve cuff. This is because the amplitude of the extracellular action potential decreases as a power function of decreasing fiber diameter (12, 27), and signal-to-noise increases as the square root of the number of averaged sweeps.
TABLE 1. Spindle afferents recorded and identified
CV, Vib., Gamma ID# Muscle m/s Hz Block Ref.
J6AlO VM 115 200 X K12A9 VM 33 NS L3A29 SA-a 121 320 X 23 N5A6 SA-a 119 300 X 23, N6A15 SA/RF 103 N D N6A27 SA-m 94 210 X 10, OlOA6 SA-a 120 250 X 25 S9A12 SA-m 65 NS X T9B6 VM 109 220 X 23 T12A8 VL 109 330 X 23, 25 T3A15 SA/RF 100 N D T9A17 SA-m 98 220 X 23 T9A22 VM 1 1 1^400 X^^23 T2B8 V? 45 N D
NS, not sensitive; ND, not determined; CV, conduction velocity; Vib., vibration.
Proprioceptive units with hip and/or knee motion sensitivity were frequently recorded without such averages being obtainable even with 4,000 sweeps; these were all rejected as potentially arising from noninstrumented muscles such as tensor fascia lata. In addition to the figures published here, Table 1 lists references where we have pub- lished records of activity of other anterior thigh spindle afferents, usually for conditions other than unperturbed locomotion.
Vasti muscle spindles Figure 3 shows activity from a spindle pn- mary afferent typical of those identified as arising from the pure knee extensor vasti group. During the extrafusal muscle activity of the stance phase, the spindle activity was modulated between -50 and 200 pps, with a clear tendency to increase its rate in response to a combination of both amplitude and rate of stretch. At the slower walking speeds, the swing phase activity was much lower despite larger and faster stretching of the passive mus- cle during the flexion phase than during stance. At the fast trot speed, the even larger, faster flexion movements began to cause more spin- dle activity than that seen during the nearly isometric stance phase. Spindle activity was generally quite low or zero during muscle shortening in both swing and stance (although it was occasionally maintained at significant levels through the end-stance extension; see fast walk and end of first stance phase in lower set of traces). The muscle velocities were gen- erally in the range of? 1 rest lengthis, but be- cause of the high angle of pinnation and rel- atively short muscle fibers (-2 cm; Ref. 3 3 , the velocities experienced by muscle fibers and parallel structures such as the muscle spindles were probably closer to four times that value (if expressed as fiber lengths/s). The sequence of events at the bottom of Fig. 3 gives some indication that the pattern of discharge observed during walking was not caused by the transducer properties of a passive spindle lacking in fusimotor drive. At the be- ginning of the trace, the animal was sitting with the knee highly flexed, maximally stretching the vasti muscles but causing only low-frequency, irregular afferent activity. As the animal built up muscle tone in preparation for extending the knee and standing, the ac- tivity of the afferent rose dramatically but
LOEB, HOFFER, AND PRATT
medial
Spike Triggerea Average n-
DRC --.J) &-
Fp A -. Stance~ -
FD.
FIG. 4. Records from anterior sartoriusspindle primary 010A6, sensitiveto knee flexion and hip extension as shown in the insert sketch, with 120 m/s conduction velocity from the spike-triggered average at lower left. (Slight phase lag of electronically derived velocity trace is artifactual.) Raw microelectrode recording is shown under the unit frequen- cygram.
ably more complex and diverse, even when the division into anatomically distinct anterior and medial parts was taken into account. Fig- ure 4 shows the most common pattern, with activity during both the swing and stance phases, despite the fact that the muscle was rapidly shortening during swing and rapidly lengthening during stance. The only period of silence was at the end of stance and early swing, when the niuscle had reached maximal length and began passively shortening prior to the active shortening in E,. Figure 5 shows another spindle primary from the same anterior part of the muscle, again with generally similar levels of activity during both the lengthening stance phase and the shortening swing phase. This unit is of fur- ther interest for two reasons. First, the stance- phase activity had a sudden drop during the fastest rates of lengthening (see arrow in record A), a feature that we have noted previously (18) and that was not uncommon during such
large excursions. Second, the animal was only 6 days postoperative at the time of this re- cording and began to limp progressively more severely in the later records Band C. The pos- tural shift can be seen in the decreased am- plitude and velocity of the hip joint excursions and a subtle decrease in the rate of rise of the patellar force. The changes in the spindle ac- tivity were much less than those in the muscle excursions, with about a 50% decrease during the stance phase lengthening and no consistent change during the reduced swing phase short- ening. Figure 6 shows a spindle secondary ending (conduction velocity 65 m/s) located in the medial part of the sartorius muscle. The peak firing rate rarely exceeded 100 pps and was relatively smoothly modulated (perhaps even more so than shown in the frequencygram that appears to have been influenced by a few missed action potentials). The length gauge across the rectus femoris and anterior sartorius
SPINDLE ACTIVITY
N5A SA-a I a medial
Spike Triggered Averege n-
DUG -qr-
Walking with Limp A B
!?. ... a *.. ..^.^ :
FD ---\I"-----
VI ; & Iw+r~;C.
I ,.oms I
Stance - - - T.................... 1 1 10m18 50cm18^ 3 5 c m l s^ 4Ocmla I (^) 1.08 I
FIG. 5. Records from anterior sartorius spindle primary N5A6, sensitive to knee flexion and hip extension, with 119 m/s conduction velocity. Relatively normal walking in A reverted to a limp in B and C with progressively less motion at the hip and knee as the animal (6 days postoperative) became tired. Arrow in A indicates pause possibly related to yielding of intrafusal structures.
muscles (LR)would not accurately reflect the record from the vastus gauge (Lv) was scaled
effect of the knee joint motion for this medial appropriately and subtracted from the LRout-
part of the sartorius, which flexes rather than put. The resultant^ LR-LVis shown with a cal-
extends the knee. A crude attempt to estimate ibration based on trigonometric reconstruc-
the maximal effect of this factor is shown in tion^ oflhe^ excursions of this part of the muscle
the uppermost length trace, in which the length from video stick figures. When interpreted us-
S9A SA-m 11 Slow Walk-40cmls Fast Walk-80cmls
Lv v SA-m
HG. 6. Records from medial sartorius spindle secondary S9A12, sensitive to knee extension and hip flexion, with 65 m/s conduction velocity. See text for explanation of length traces.
SPINDLE
some fusimotor influence acting on almost all anterior thigh spindles studied. For the vasti muscles, this is indicated by the larger response of the afferents to small stretches during stance (active lengthening) than to much larger stretches during swing (passive lengthening). For the biarticular muscles, fusimotor action is indicated by afferent activity during rapid muscle shortening, which is never seen in deef- ferented spindle afferents. In the accompa- nying paper (23) we present data from func- tional deefferentation experiments using li- docaine blockade to provide some qualitative and quantitative estimates of these fusimotor effects. How far can this apparent fusimotor influ- ence be dissected before resorting to pure con-
jecture? The responses of the vastus medialis spindle primary during walking in Fig. 3 were highly velocity dependent, suggesting dynamic fusimotor influence, but the initial sequence as the animal stood up before walking would be more consistent with biasing by static fu- simotor activity (note steady, somewhat irreg- ular activity during shortening). On different grounds, it seems clear that the activity of sar- torius spindle afferents during swing phase shortening (e.g., Figs. 4 and 5) must be the result of static fusimotor activity, but it is not clear from these records whether the stance phase activity during stretching is consistent with passive spindle properties, static fusi- motor, or dynamic fusimotor effects. The pause in the middle of a large stretch noted in Fig. 5A suggests a sudden yielding of a stiff intrafusal element with a slow recovery time, perhaps a bag, fiber under dynamic fusimotor activation, but this is again conjectural. If one considers all of the possible interactive effects of temporally modulated fusimotor ac- tivity, many combinations will be consistent with these data. Perhaps more importantly, many combinations are not likely. The sudden silencing of most spindles following length peaks in late stance indicates little or no static fusimotor activity, whereas sustained discharge during rapid shortening requires such static activity. It is clear that the similar range of firing rate noted in all of these spindle pri- maries during various periods of active parent muscle use cannot have been achieved by the same fusimotor program in all cases. In order to interpret all of these patterns of spindle ac- tivity as resulting from alpha-gamma coacti-
vation (9), it must be assumed that the dy- namic and static fusimotor systems, with their very different effects, can be independently turned on or off. That is, some phases of alpha motoneuron recruitment would have to be accompanied by coactivation of gamma static motoneurons, whereas other phases would have to be accompanied by gamma dynamic motoneurons, probably to the exclusion of gamma statics. This possibility becomes more consistent with traditional ideas about fixed recruitment order in motoneuron pools in light of the finding that the two EMG bursts occurring in each step cycle in anterior sar- torius are the work of two separate groups of independently recruited alpha motoneurons (1 I). However, the two companion papers shed further light on the amount and com- plexity of fusimotor influence on spindle af- ferent activity and reveal circumstances in which the extrafusal activity appears to be in- dependently modulated. For all of these rea- sons, it seems unwise to presume that the re- cruitment of various parts of the fusimotor apparatus is determined simply and invariably by activation levels in the alpha motoneuron pool. We propose that during voluntary move- ments, the fusimotor system functions to con- tinuously adjust the sensitivity and bias of the spindle afferents to improve the transduction of the particular range of mechanical events anticipated by the animal. The evolving use of limbs for multiple, independent, finely controlled tasks in mammals (as opposed to lower vertebrates) has been accompanied by the separation of intra- and extrafusal control into at least three types of motoneurons having very different effects: alpha motoneurons modulate force output without influencing spindle sensitivity, gamma static motoneurons maintain spindle bias during muscle short- ening (extending dynamic range) without adding to force output, and gamma dynamic motoneurons enhance spindle sensitivity to small length and velocity perturbations (nar- rowing dynamic range). Various combinations of these systems (including hardwired com- binations offered by beta motoneurons) can be and apparently are used to cope with such varied kinematic behavior as we have noted in the various anterior thigh muscles during various phases of locomotion. In this discussion, it seems more useful to
562 LOEB, HOFFER, AND P R A n
take a broader view of the phenomenology of spindle afferent traffic and to consider its pos- sible interpretation by the spinal cord and the higher motor control structures that presum- ably rely on these signals to guide and refine their output decisions. In that context, the most striking general finding is that almost all of the spindle afferents from which we re- corded had similarly well-modulated activity during the periods of extrafusal activity of their parent muscles. Spike rates rarely exceeded -200 pps and rarely fell below 20-50 pps (somewhat lower for secondaries), although sustained low-frequency activity was a typical feature of these same muscle spindles when the animal was lying quietly or lightly anes- thetized with the limb at an intermediate an- gle. A similar tendency has been noted for spindles in a wide variety of muscles and mo- tor tasks (for review see Ref. 19). The sequence shown at the bottom of Fig. 3 was typical of the systematic biasing of activity that accom- panied the onset of locomotor activity in the anterior thigh muscles. In a perhaps related feature, the activity of these afferents changed very little with changes in the speed or extent
of the joint angle excursions and/or changes in parent muscle EMG during locomotion made by voluntary actions of the animal. This suggests that such voluntary changes in the extrafusal motor program were accompanied by compensatory changes in the intrafusal program, consistent with the servo-control notion of using sensory feedback to provide an error signal to the motor controller (see Ref. 36). All of this is consistent with a systematic optimization of instantaneous transducer sen- sitivity to make the best use of the informa- tion-conveying properties of an afferent data stream consisting of all-or-none action poten- tials propagating along an axon (for quanti- tative analysis, see Ref. 25a). Firing rates above 200 pps appear to be difficult to sustain; the rare instances of such rates in our own data (e.g., Figs. 4 and 5) and similar records in other muscles (22, 32, 33) appear intermittent and noisy, tending to degrade the information that can be extracted from the afferent signal. Fir- ing rates below 50 pps cannot signal instan- taneous changes in mechanical input simply because they must be integrated over at least their interpulse intervals (20 ms or longer) be- fore changes can be appreciated. The integra-
tion of many afferents by postsynaptic neurons solves this problem only at the expense of low signal-to-noise levels or degraded spatial res- olution (25a). If the central nervous system is interested in optimizing the sensitivity of its motor control apparatus to unexpected per- turbations in the limb trajectory (either short- ening or lengthening the muscle), it must do two things: 1)It must keep the spindle afferent firing rates within this window of optimal firing rates. 2) It must adjust afferent sensitivity so that the range of perturbations anticipated during the movement causes maximal mod- ulation of afferent discharge within this window. The different independent effects of the static and dynamic fusimotor neurons on spindle afferent dynamic range noted above are particularly well suited to these tasks, but only if the central nervous system has inde- pendent control of the various types of mo- toneurons. Such an interpretation of fusimotor activity suggests a specific division of labor between the primary and secondary endings. The same programming of the primary endings that might optimize instantaneous sensitivity to unexpected perturbations of limb trajectory can also be expected to greatly complicate the extraction of kinesthetic information about posture. Information about wide-ranging but slowly changing aspects of limb and trunk po- sition is probably an important output of the muscle spindles, in concert with joint and skin stretch receptors. The secondary endings, with their less rapidly modulated firing rates and more linear responses to length, might provide a better input signal to a central integrating circuit with relatively long time constant for keeping track of overall limb position. Of course, at least part of the fusimotor control system that influences the primary endings is shared with the secondaries (the chain fibers innervated primarily by gamma static moto- neurons). However, the transducer sensitivity effects of these fibers tend to improve rather than degrade linearity of the response to length changes by reducing velocity-dependenteffects (16) and extending the useful range of the transducer into the negative velocity (short- ening) regions (2). The spindle afferent activity studied here includes examples of muscles classified as ex- tensors (vasti and rectus fernoris) and as flexors
564 LOEB, HOFFER, AND PRA'IT
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