Division of Neurobiology, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, Phoenix,Arizona 85013
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ABSTRACT |
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Turkin, Vladimir V., Katrina S. Monroe, and Thomas M. Hamm. Organization of recurrent inhibition and facilitation in motor nuclei innervating ankle muscles of the cat. J. Neurophysiol. 79: 778-790, 1998. The distribution of recurrent inhibition and facilitation to motor nuclei of muscles that act at the cat ankle joint was compared with the locomotor activity and mechanical action of those muscles described in published studies. Emphasis was placed on motor nuclei whose muscles have a principal action about the abductionadduction axis and the pretibial flexors: tibialis posterior (TP), peroneus longus (PerL), peroneus brevis (PerB), the anterior part of tibialis anterior (TA) and extensor digitorum longus (EDL). Most intracellular recordings in spinalized, unanesthetized decerebrate cats showed only inhibitory or excitatory responses to antidromic stimulation of peripheral nerves, but mixed effects were also seen. Recurrent effects among motor nuclei of ankle abductors and adductors were not distributed uniformly. TP motoneurons received recurrent inhibition from most other nuclei active in stance and stimulation of the TP nerve inhibited these motor nuclei. Although PerB motoneurons are also active during stance, they received primarily facilitation from most motor nuclei. PerL received mixtures of inhibition and facilitation from all sources. Stimulation of the nerves to PerL, PerB, and peroneus tertius (PerT) produced weak recurrent inhibition and facilitation, even in homonymous motoneurons and motoneurons of Ia synergists. The ankle flexors TA and EDL displayed different patterns of recurrent inhibition and facilitation. TA motoneurons received prominent homonymous inhibition and inhibition from semitendinosus (St). EDL, whose activity profile differs from TA and which also acts at the digits, did not receive strong recurrent inhibition from either TA or St, nor did stimulation of the EDL nerve produce much inhibition. The distribution of recurrent inhibition and facilitation is correlated with the pattern of locomotor activity, but with exceptions that suggest an influence of mechanical action, particularly in the antagonistic interactions between TP and PerB. The extended pattern of recurrent inhibition, the reduction or absence of inhibition produced by motor nuclei with individualized functions or digit function and the prevalence of facilitation suggest that the recurrent Renshaw system is organized into inhibitory and disinhibitory projections that participate in the control of sets of motor nuclei engaged in rhythmic and stereotyped movements.
Recent investigations of Renshaw recurrent inhibition have provided comparative data on its distribution to motor nuclei that innervate muscles of the upper and lower limbs in human subjects and muscles of the fore- and hindlimbs in cats. Although prominent in motor nuclei that innervate the proximal muscles of a limb, recurrent inhibition is often absent or reduced in motor nuclei that innervate distal musculature, particularly those acting at the digits, in both the cat (Hahne et al. 1988 The data reported in this study were obtained from 10 adult cats (3-4.5 kg). For initial surgical procedures, each cat was anesthetized with a mixture of isoflurane, nitrous oxide, and oxygen. Anesthesia was induced in a plexiglass chamber. After induction, anesthetic was delivered via a mask until a tracheal cannula was inserted for continued administration of anesthetic and ventilation. Isoflurane concentration was adjusted over a range of 1.7 to 2.1% to maintain a surgical level of anesthesia. Catheters were placed in one common carotid artery and external jugular vein for measurement of arterial blood pressure and administration of fluids and drugs, respectively. In addition, a catheter was placed in the urethra.
Characteristics of motor nuclei and muscles investigated
We determined patterns of recurrent inhibition and facilitation between motor nuclei of nine ankle muscles and two proximal muscles that exert various mechanical actions and display a range of locomotor activities. The focus of the current study concerns the projections to and from motor nuclei that have received less attention in previous studies of recurrent inhibition - TP, PerL, PerB, PerT, TA and EDL. Projections involving other motor nuclei are discussed when our results differ from or expand on previous results. The mechanical action and pattern of locomotor activity of the muscles innervated by these motor nuclei are summarized in Table 1.
Characteristics of the recorded responses
Both inhibition and facilitation were recorded in our sample of motoneurons. Most responses were either inhibitory (317 responses; 38%) or facilitatory (311 responses; 38%), but responses in which inhibition was followed by facilitation were often observed (199 responses; 24%). Thus facilitation contributed to over half the responses. Examples of each of these forms of responses are shown in Fig. 1. Mixed responses in which facilitation followed inhibition displayed several forms. They sometimes consisted of a brief hyperpolarization followed by facilitation (Fig. 1E), as noted previously for antagonists (Renshaw 1941
Patterns of inhibition and facilitation for TP motoneurons
Figure 2 shows examples of RIPSPs and RFPs recorded in TP motoneurons. As shown in this figure, stimulation of LGS and Pla produced inhibition in TP motoneurons. The inputs from all motor nuclei are summarized in Fig. 3, showing that inhibition of TP motoneurons was mainly produced by stimulating nerves of ankle muscles active in stance, LGS, Pla, and FHL, regardless of their action in the adduction-abduction plane. Stimulation of the ABF muscle nerve produced inhibition in only two of the six motoneurons, although the amplitude of this inhibition was relatively large. Three of the other TP motoneurons received monophasic RFPs from ABF. Weak inhibition was received from PerL by most TP cells and four of six received inhibition from either EDL or TA. The inhibition from most of these sources was frequently mixed with facilitation.
Patterns of inhibition and facilitation for Perl, Perb, and Pert motoneurons
The PerL and PerB muscles, like TP, have substantial moment arms about the adduction-abduction axis of movement. Like TP, activation of these motor pools produces recurrent effects, consistent with a previous report that these motoneurons possess recurrent collaterals (Horcholle-Bossavit et al. 1988 Patterns of inhibition and facilitation for TA and EDL motoneurons
A previous study from this laboratory (Hamm 1990
Patterns of inhibition and facilitation for proximal group of motoneurons
Our data concerning inhibition between the motor nuclei innervating ABF, St, LGS, Pla, and FHL are in general agreement with previous observations (Eccles et al. 1961a Contributions of different functional groups of motor nuclei to recurrent inhibition
Our data augment evidence that recurrent inhibition is produced in different amounts by different functional groups of motor nuclei. Recurrent collaterals are absent in motoneurons of intrinsic plantar muscles (Cullheim and Kellerth 1978
This study demonstrated several features in the pattern of recurrent inhibitory and facilitatory projections linking motor nuclei that innervate muscles with actions at the ankle. Recurrent facilitation was widespread in our sample of recordings, contributing to more than half of the responses, and potential mechanisms underlying these responses and the significance of these projections are considered. The recurrent inhibition and facilitation received by each motor nucleus and produced by its activation was often correlated with its pattern of locomotor activity, its use in stereotyped or variable activity, or its mechanical action at the ankle or toes, but no single factor was sufficient as a basis for complete distribution of recurrent effects. Finally, we found that the recurrent inhibition produced by individual motor nuclei varied, with some making much larger contributions than others. The contribution of different motor nuclei to recurrent inhibition and facilitation are considered in relation to the function of this spinal system.
Mechanisms and significance of recurrent facilitation
Recurrent facilitation has been observed in previous studies in which the spinal cord was unanesthetized or only lightly anesthetized (Hamm 1990 Correlates to the distribution of recurrent inhibition
The most consistent factor associated with motor nuclei that receive and produce the largest amounts of recurrent inhibition is their participation in stereotyped patterns of locomotor activity. The TP, TA, Pla, LGS, and ABF motor nuclei all produce stereotyped patterns of locomotor activity and all figure prominently in recurrent inhibitory circuits. Conversely, the motor nuclei of PerL, PerT, and EDL exhibit variable locomotor activity and the amounts of recurrent inhibition they receive and produce after activation are considerably less than received and produced by the former group.
Contribution of different motoneuron pools to recurrent inhibition and facilitation
Motor nuclei that innervate hindlimb muscles of the cat do not contribute uniformly to recurrent projections in relation to their size. Projections were particularly weak from PerL, PerB, EDL, and FHL. This weakness may be related to the size of the recurrent collateral arbors of motoneurons in these pools, as seems to be the case with FHL (McCurdy and Hamm 1992
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Hamm 1990
; Horner et al. 1991
; McCurdy and Hamm 1992
) and human (Katz et al. 1993
; Rossi and Mazzocchio 1991
).
; Meunier et al. 1990
, 1994
). These variations in the distribution of recurrent inhibition suggest that its organization has been adapted to meet different requirements for the control of these various limb systems and the proximal and distal musculature of each limb.
; Meunier et al. 1990
, 1994
) and cat (Baldiserra et al. 1981) limb systems correspond to differences in the pattern of Ia facilitation and have suggested that recurrent inhibition limits the extent of Ia excitation and Ia reciprocal inhibition and increases the contrast between motor patterns in proximal motor nuclei, as postulated in earlier investigations (Brooks and Wilson 1959
; Hultborn et al. 1971a
; see also Hultborn et al. 1979
). Also, Windhorst (1996)
has proposed that recurrent inhibitory and Ia projections form an integrated system for parameter adjustment of spinal networks employed in stabilizing posture and movement.
; Katz et al. 1993
; Meunier et al. 1994
) and cat studies (Baldiserra et al.1981; Fritz et al. 1989
; Hahne et al. 1988
; Hamm 1990
; Horner et al. 1991
; Illert and Wietelmann 1989). For example, the cat flexor hallucis longus and flexor digitorum longus exchange strong Ia monosynaptic excitation (Dum et al. 1982
), but display very different patterns of activity during normal and fictive locomotion (O'Donovan et al. 1982
; Fleshman et al. 1984
; Trank et al. 1996
). The patterns of recurrent inhibition and facilitation received by the motor nuclei of these muscles reflect the differences in activity during locomotion, rather than their Ia synergism (Hamm 1990
), suggesting that patterns of recurrent inhibition reflect the organization of locomotor activity rather than patterns of Ia projections. Alternatively, the patterns of recurrent inhibition could reflect the mechanical requirements for the control of each limb, which would find their counterparts in the organization of other spinal circuits, like Ia facilitation and reciprocal inhibition, and in the organization of locomotor commands.
; Hultborn et al. 1971a
; Hamm 1990
), but little information is available on the distribution of recurrent inhibition and facilitation within the pretibial flexors or between adductors and abductors of the ankle. Our studies show that recurrent inhibition and facilitation are not uniformly or symmetrically distributed between these motor nuclei and that the patterns of recurrent inhibition and facilitation are correlated with patterns of locomotor activity and mechanical action.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View this table:
TABLE 1.
Pattern of locomotion and mechanical action of investigated muscles
)? 3) Do motor nuclei whose muscles act as agonists (or antagonists) at the ankle produce recurrent inhibition (or facilitation) in one another when activated? 4) Do motor nuclei whose muscles act at the digits produce and receive less recurrent inhibition?
). Although the number of motoneurons sampled for most motor nuclei was too small for a representative sample, this similarity indicated that motoneurons from most nuclei were sampled over most of the range of motoneuron properties. If any bias existed in the sample, it would be a bias toward larger RIPSP amplitudes in the groups with slower conduction velocities (cf. Friedman et al. 1981
), i.e., in PerB, PerT and EDL motoneurons. Judging from the results described below, the difference in conduction velocities in these cells did not appear to be a source of significant sampling error.
View this table:
TABLE 2.
Characteristics of motoneurons sampled from the investigated motor nuclei
; Wilson et al. 1960
). The initial IPSP in such responses could be as brief as 5 ms in some cases. The possibility that these IPSPs were actually extracellular fields was excluded by direct comparison to extracellular fields in 7 of 11 cases and by the observation that the extracellular fields of motoneurones produced by antidromic invasions were invariably shorter. In homonymous connections or in projections to synergists, longer lasting inhibition (25-55 ms) was often followed by facilitation (Fig. 1D). In addition, mixed responses were also observed in which the inhibition was of intermediate duration(Fig. 1C).
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FIG. 1.
This figure gives examples of averaged recurrent postsynaptic potentials, showing different combinations of recurrent inhibition and facilitation recorded in motoneurons innervating ankle muscles. A: recurrent inhibitory postsynaptic potentials (RIPSPs) in a motoneuron innervating lateral gastrocnemius-soleus (LGS) muscle in response to stimulation of tibialis posterior (TP) nerve. B: recurrent facilitatory potentials (RFPs) in a tibialis anterior (TA) motoneuron in response to LGS nerve stimulation. C-E: responses with different mixtures of facilitation and inhibition. Response recorded in a TP motoneuron to stimulation of anterior biceps femoris (ABF) nerve is shown in C; inhibition and facilitation recorded in a flexor hallucis longus (FHL) motoneuron in response to stimulation of ABF nerve is shown in D; and E shows brief inhibition followed by facilitation in an extensor digitorum longus (EDL) motoneuron after stimulation of semitendinosus (St) nerve. Zero on time axis indicates arrival of motor volley in ventral roots. Each average consisted of 32 samples. Strength of stimulation of muscle nerves was 3 times motor threshold.
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FIG. 2.
Examples of RIPSPs and RFPs recorded in TP, PerB, PerL, and PerT motoneurons in response to stimulation of different nerves (top of each plot). Responses in several motoneurons are superimposed in each plot. Each average was based on 32 or more samples. These averages have been aligned at time of arrival of motor volley recorded in ventral roots (0 on time axis).
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FIG. 3.
Distributions of inhibition and facilitation to and from TP, PerL, and PerB motoneurons are represented. Each set of bars represents mean and standard deviation of RIPSP and RFP amplitudes recorded in TP, PerL, and PerB motoneurons (top) or produced by stimulation of their muscle nerves (bottom). Positive values indicate facilitation, and negative values indicate inhibition, in mV. Means of inhibition and facilitation are based on all cells in which a particular combination was tested, and include cases in which a mixed response of inhibition and facilitation occurred. Row of bars below each set of means indicates proportion of responses with recurrent inhibition alone (dark), mixed responses (cross hatched), andfacilitation alone (dashed hatch). Proportion of cells with no responses are represented by open portion of each bar. Motor nucleus producing (top) or receiving (bottom) inhibition and facilitation are indicated by abbreviations for motor nucleus above bars and numbers in parentheses indicate number of cases tested in each combination.
). Stimulating the TP nerve inhibited most FHL motoneurons and produced inhibition in LGS motoneurons comparable in amplitude to the homonymous inhibition. Weak inhibition was also produced in the majority of ABF and TA motoneurons, while in EDL cells input from TP was evenly mixed between inhibition and facilitation. Most PerL and PerB motoneurons received facilitation in response to TP stimulation.
). However, recurrent effects from these motor nuclei are weak and recurrent effects received by these motor pools are dominated by recurrent facilitation.
) were sources of facilitation, in addition to the PerL pool itself. Inhibition was found from each of the peroneal motor nuclei, but its magnitude and prevalence were no greater than from the other motor nuclei we examined.
) and the secondary moment arm can vary between flexion and eversion in different animals (Young et al. 1993
). Kernell and his colleagues have also reported that different portions of the PerL muscle may be differentially active during some forms of motor behavior and are differentially activated by segmental and descending inputs (Hensbergen and Kernell 1992
; Kandou and Kernell 1989
). We reviewed the responses in each PerL cell to determine if the mixture of inhibition and facilitation resulted from differences in input to PerL motoneurons in distinct populations of PerL motoneurons or in different animals. We found that all but two PerL cells received mixtures of inhibition and facilitation and that the pattern of inhibition and facilitation varied from cell to cell. There did not appear to be distinct patterns in two groups of cells that accounted for the mixture. Nor did we find a particular pattern associated with each cat. Inhibition and facilitation from each nerve were found in nearly every experiment, except for RIPSPs from ABF and PerB and RFPs from PerT, each of which only occurred in two of the six cats in which we recorded PerL motoneurons.
). We recorded a complete set of responses in two PerT motoneurons and a partial set in a third. These PerT motoneurons received facilitation from most nerves (e.g., Fig. 2). No inhibition was observed in three cells from PerL, or in one cell each tested for input from PerB or PerT. Stimulation of PerT produced small recurrent effects in some motoneurons, including slight facilitation in ABF and St, and slight mixed effects in FHL and EDL (data not shown). Although RIPSPs were seen in some PerL and PerB motoneurons, facilitation was recorded as often in PerL motoneurons (4 of 17 cells) and more often in PerB motoneurons (3 of 7 versus 1 of 7 cells).
) reported that EDL motoneurons received some recurrent inhibition from extensor motor nuclei. Unlike TA, the locomotor activity of EDL remains strong during the latter part of the swing phase and overlaps the initial extensor burst at the start of stance when the extensor motor pools are active (Abraham and Loeb 1985
; Engberg 1964
; Goslow et al. 1977
; Trank et al. 1996
). The data from the present study provide only partial confirmation of previous results; inhibition from Pla and FHL was weaker than found by Hamm (1990)
. The present result do show differences in the participation of TA and EDL in recurrent circuits. TA motoneurons received prominent inhibition from stimulation of nerves innervating both proximal and distal muscles (Figs. 4 and 5). The largest RIPSPs recorded in TA motoneurons were evoked by stimulation of the homonymous and St nerves. Stimulation of the nerve supplying EDL produced only small IPSPs and in only half of the TA motoneurons. In a previous study (unreported data from Hamm 1990
) stimulation of the EDL nerve failed to evoke recurrent IPSPs in six TA motoneurons. TP and PerL nerve stimulation also evoked small RIPSPs in some TA motoneurons. Large RFPs were evoked in TA motoneurons on stimulation of the ABF, LGS and, less frequently, Pla nerves. (cf. Wilson et al. 1960
).
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FIG. 4.
Examples of responses recorded in TA, EDL, and LGS motoneurons are shown in this figure. Format is same as in Fig. 2.
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FIG. 5.
This figure shows distribution of inhibition and facilitation to and from TA and EDL motoneurons. Format is same as in Fig. 3.
; Hultborn et al. 1971a
). Consistent with the results of Hultborn et al. (1971a)
, we found small amounts of recurrent inhibition from LGS to St (mean amplitude: 0.22 mV), but found recurrent facilitation more often than in that previous study. Weak facilitation was observed in St, LGS, and Pla motoneurons; the strongest projection was from ABF to St (mean of 0.22 mV). In turn, facilitation was found from St to ABF, as well as to LGS and Pla. LGS motoneurons provided recurrent facilitation to ABF, St, and FHL, while activation of Pla motoneurons produced facilitation in St, LGS,and FHL.
) and flexor digitorum longus (McCurdy and Hamm 1992
) and activation of these motor pools produces no recurrent inhibition (Fleshman et al. 1984
; Hamm 1990
). The present study demonstrates that although a substantial degree of recurrent inhibition is produced by the TP motor nucleus, the three peroneal motor nuclei produce only small recurrent effects and that EDL produces recurrent inhibition that is considerably smaller than that produced by TA.
). All of the mean RIPSP amplitudes fall below this line, indicating that each composite RIPSP is less than the sum of individual RIPSPs produced by the total number of motoneurons in each pool. This sublinear summation of RIPSPs may indicate nonlinear summation or saturation of motoneuron input at the Renshaw cell level (e.g., Hultborn et al. 1988
) or possibly the effect of interactions between Renshaw cells (see DISCUSSION). Figure 6 shows that the motor nuclei most effective in producing recurrent inhibition in relation to their size are TP, TA, and St. LGS, ABF, and Pla are somewhat less effective. The RIPSPs produced by FHL, EDL, PerL, PerB, and PerT are the least effective in producing recurrent inhibition. Of these, three are involved in digit function (FHL, EDL, and PerT), two express variable patterns of activity during locomotion (PerL and PerT) and three are primarily facilitated by the activity of other motor nuclei through other recurrent pathways (PerL, PerB, and PerT). Although two of these motor nuclei have principal actions about the abduction-adduction axis (PerL and PerB), TP, which is one of the most effective motor nuclei, also has a principal action about this axis.
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FIG. 6.
Effectiveness of each motor nucleus in producing recurrent inhibition in relation to its size is shown in this figure. Mean RIPSP amplitudes recorded in this study are plotted as a function of number of alpha motoneurons in motor nucleus that produces inhibition. For each motor nucleus, the 3 largest mean RIPSPs have been plotted. Recipient motor nuclei are indicated by symbols identified at bottom right. Three RIPSP means produced by each motor nucleus are linked by dotted lines and identified by labeling on this graph. (- - -): expected composite RIPSP amplitude on the basis of product of number of alpha motoneurons and mean RIPSP amplitude between individual motoneurons. This mean amplitude (18.94 µV) is based on average of all significant and nonsignificant recordings from data of McCurdy and Hamm (1994a) . Effectiveness of each motor nucleus in producing recurrent inhibition can be assessed from distance of its mean composite RIPSPs from this line; motor nuclei with similar efficacy should cluster about a line parallel to dashed line. Numbers of alpha motoneurons in each nucleus are based on following sources. ABF: Letbetter and English (1981)
, on the basis of total number of motoneurons in biceps femoris nucleus that innervate anterior and middle parts of muscle (1100) and an assumed composition of 60% alpha motoneurons (cf. Boyd and Davey 1968
). LGS: Weeks and English (1985)
. St, Pla, FHL, TP, and EDL: Boyd and Davey (1968)
. PerL, PerB, and PerT: Horcholle-Bossavit et al. (1988)
. TA: Boyd and Davey (1968)
and Iliya and Dum (1984)
.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
; Hultborn et al. 1971b
; Illert and Wietelmann 1989; Renshaw 1941
; Wilson et al. 1960
). Following evidence by Wilson and Burgess (1962)
that recurrent facilitation is a disinhibition, Hultborn et al. (1971b)
demonstrated that most recurrent facilitation is produced by the Renshaw-mediated inhibition of tonically active Ia reciprocal inhibitory interneurons. Much of the recurrent facilitation observed in this study is consistent with this mechanism. For example, Ia reciprocal inhibition from gastrocnemius-soleus to TA and EDL is well-documented and the recurrent facilitation that is produced in TA and EDL from triceps surae (cf. Wilson et al. 1960
) is readily accounted for by this mechanism. Recently, Bonasera and Nichols (1996)
have demonstrated length-sensitive reciprocal inhibitory reflexes between TP and PerB, whose characteristics are consistent with Ia reciprocal inhibition. Because activation of TP produces inhibition in the homonymous and synergist motoneuron pools, facilitation from TP to PerB found in this study is likely attributable to recurrent inhibition of Ia reciprocal interneurons that receive Ia input from TP and project to PerB. Hultborn et al. (1971a)
found an extended pattern of recurrent inhibition of Ia reciprocal inhibitory interneurons similar to the pattern of inhibition of motoneurons. Accordingly, motor nuclei that inhibit the TP motor nucleus (e.g., LGS, ABF, TA) should also facilitate PerB via inhibition of the Ia interneurons that project to PerB.
, 1981
) and direct projections of recurrent collaterals to motoneurons (Cullheim et al. 1984
). Indirect evidence suggests that mutual inhibition may occur between Renshaw cells excited by the same or synergistic motoneuron pools (Ryall et al. 1972
; cf. Windhorst et al. 1989
). McCurdy and Hamm (1994b)
observed recurrent facilitatory potentials produced in individual motoneurons by stimulation of another synergistic motoneuron. Of several mechanisms considered, only mutual inhibition between Renshaw cells explained all of the single-neuron RFPs they observed.
; Wilson et al. 1960
) and RIPSPs from TA and EDL to ABF and LGS motoneurons (see Figs. 4 and 5). This diversity is consistent with the convergence observed from different motor pools onto individual Renshaw cells (Eccles et al. 1954
, 1961b
; Ryall 1981
), which "present a bewildering variety of excitatory input patterns" (Ryall 1981
). It should be noted that the distribution of inhibition and facilitation observed experimentally, obtained by activating motor pools individually, may differ from that in effect during activities like locomotion, in which multiple pools are active. During volitional movements, the pattern of inhibition and facilitation may also be restricted by descending pathways, which influence both Ia reciprocal interneurons and Renshaw cells (Jankowska 1992
; Windhorst 1996
). In addition, any mutual inhibition between Renshaw cells would tend to silence those cells only weakly activated by a pattern of activity, while concurrently augmenting the activity of those strongly activated by that pattern (cf. Ryall 1981
). This mechanism would shape the projections from Renshaw cells to motoneurons and Ia interneurons according to the pattern of activity.
; English and Weeks 1987
; Smith et al. 1993
). Despite this adaptive variability, evidence suggests that St receives stereotyped locomotor commands. Perret and Cabelguen (1980)
demonstrated in thalamic cats that St activity during the extensor or flexor phase of fictive locomotion could be controlled by the activity of flexor reflex afferents and they argued that bifunctional motor nuclei like St receive stereotyped locomotor commands from either the extensor or flexor components of the spinal pattern generator depending on such sensory control. The possibility that St receives stereotyped locomotor commands is supported by recent studies of correlations between the activity of motor pools during fictive locomotion. These studies, in which neurogram activity was analyzed in the frequency domain to determine the presence of locomotor signals shared by different motor nuclei, demonstrated correlations between St (or St and posterior biceps femoris) and either flexors like TA or extensors like LG and medial gastrocnemius, depending on the pattern of activity in the bifunctional motor nuclei (Hamm and McCurdy 1996
; Turkin and Hamm 1996
). In contrast, preliminary observations provide evidence of weak correlations between the activity of TA and EDL (Turkin and Hamm 1996
), which are not linked by strong recurrent inhibition. The activity of EDL may be altered in different forms of locomotion that further distinguish it from TA activity (Trank et al. 1996
; Trank and Smith 1995
). These data support the hypothesis that the motor nuclei comprising a set that receive recurrent inhibition from one another are those that receive the same commands during activities like locomotion.
; Loeb 1993
); yet, it receives practically no recurrent inhibition from other motor nuclei with regular stance phase activity. Instead, PerB receives recurrent facilitation from these sources. PerB acts primarily as an abductor in direct opposition to TP, and Bonasera and Nichols (1996)
have demonstrated that TP and PerB are linked by mutually inhibitory length dependent reflexes. These findings suggest that the mechanical and reflex antagonism between TP and PerB excludes the latter from the set of motor nuclei active in stance that are subject to recurrent inhibition from each other during activity.
). However, although the extended pattern includes motor nuclei that lack a common mechanical action, our results also suggest that the mechanical action of individual muscles is a factor in the distribution of recurrent inhibition. The control of posture and locomotion requires the production of torques about the abduction-adduction and inversion-eversion axes of the ankle, in addition to flexor and extensor torques. The partial correlation between the organization of recurrent inhibition in motor nuclei of ankle muscles and their mechanical actions suggests that recurrent inhibition is involved in the control of actions outside the sagittal plane.
). McCurdy and Hamm (1992)
noted a gradient in the complexity of recurrent collaterals that seemed to be correlated with action at the digits and individualized patterns of use. This observation is consistent with the digit functions of EDL, FHL, and PerT, and with observations of variable activity in EDL (Trank et al. 1996
; Trank and Smith 1995
) and PerL (Hensbergen and Kernell 1992
; Loeb 1993
), which suggest that these muscles are used in an individualized manner. But the weak recurrent effects produced by PerB suggest that other factors than digit function and individualized use may influence the participation of a motor pool in recurrent inhibition.
estimated that recurrent inhibition would have little influence on the discharge rate of a motoneuron. However, McCurdy and Hamm (1994a)
estimated that recurrent inhibition produced by several motoneuron pools could alter force development of recently recruited motor units by 25%. Although these estimates were based on studies in which fast, large-diameter motor axons were activated with slower, small-diameter motor axons, studies in both cat (Hultborn et al. 1988
) and human (Bussel and Pierrot-Deseilligny 1977
) indicate that the recruitment of smaller motor units effectively contributes to the activation of Renshaw cells and the production of recurrent inhibition.
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ACKNOWLEDGEMENTS |
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We thank T. Fleming for excellent technical assistance and Drs. M. Maltenfort and T. Trank for helpful discussions and comments on a draft of this report. We also thank Dr. Trank for assistance with reviewing some of the data obtained in this study.
This work was supported by National Institutes of Neurological Disorders and Stroke Grants NS-22454 to T. M. Hamm and NS-07309 to the University of ArizonaBarrow Neurological Institute Motor Control Neurobiology Training Program. K. S. Monroe received support from the Undergraduate Biology Research Program at the University of Arizona.
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FOOTNOTES |
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Present address of K. S. Monroe: Washington University School of Medicine, Program in Physical Therapy, 4444 Forest Park Blvd., Campus Box 8502, St. Louis, MO 63108.
Address for reprint requests: T. M. Hamm, Division of Neurobiology, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, 350 W. Thomas Rd., Phoenix, AZ 85013.
Received 3 March 1997; accepted in final form 21 October 1997.
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REFERENCES |
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