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1 Department of Physiology, Göteborg University, 405 30 Göteborg, Sweden
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Abstract |
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(Received 10 April 2005;
accepted after revision 4 August 2005;
first published online 11 August 2005)
Corresponding author E. Jankowska: Department of Physiology, Medicinaregatan 11, Box 432, 405 30 Göteborg, Sweden. Email: elzbieta.jankowska{at}physiol.gu.se
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Introduction |
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Methods |
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The experiments were performed on 10 deeply anaesthetized adult cats (weighing 2.4–3.5 kg), some of which were also used for the study reported by Matsuyama and Jankowska (2004). Anaesthesia was induced with sodium pentobarbital (40 mg kg–1
I.P.) and maintained with intermittent doses of 
-chloralose sufficient to abolish any withdrawal reflexes (up to a total dose of 55 mg kg–1
I.V.). During recording, neuromuscular transmission was blocked by pancuronium bromide (Pavulon, about 0.2 mg kg–1 h–1
I.V.) and the animals artificially ventilated. The depth of anaesthesia was assessed by continuously recording blood pressure and heart rate and by monitoring pupil diameter. The mean blood pressure was kept at 100–130 mmHg and the end-tidal concentration of CO2 at about 4% by adjusting the parameters of artificial ventilation and the rate of infusion of a bicarbonate buffer solution with 5% glucose (1–2 ml kg–1 h–1). The core body temperature was kept at about 38°C by servo-controlled infrared lamps. At the end of the experiment the animals were killed with an overdose of anaesthetic. The experimental procedures were approved by Göteborg ethics committee and followed NIH and EU guidelines of animal care.
Inhibitory postsynaptic potentials (IPSPs) were recorded from motoneurones located on the left side of the spinal cord. They were evoked by stimulation of muscle nerves or the descending reticulospinal or vestibulospinal tract fibres on the right side. To eliminate synaptic actions evoked via descending tract fibres ipsilateral to the motoneurones, the spinal cord was hemisected on the left side at the level of the Th12 or 13 segments. The left L4–S1 dorsal roots were transected in order to allow a selective stimulation of motor axons by stimuli applied to muscle nerves. Alternatively motor axons were stimulated within the ventral roots in preparations in which all dorsal roots were left intact but the L6 or both the L5 and L6 ventral roots were transected and mounted on a pair of stimulating electrodes.
The preliminary dissection included cannulation of the trachea, a carotid artery, and the left and right cephalic veins. The left quadriceps (Q), and sartorius, (Sart) nerves were dissected, transected and mounted in subcutaneous cuff electrodes. Laminectomies were performed at the level of the lower thoracic (Th11–13) and lumbar (L3–L7) segments. The cerebellum was exposed to allow insertion of stimulating electrodes into the right medial longitudinal fascicle (MLF) and the right lateral vestibular nucleus (LVN) contralateral to motoneurones to be recorded from, as previously described (Jankowska et al. 2003; Matsuyama & Jankowska, 2003, 2004).
Stimulation
Axons of reticulospinal tract neurones in the MLF and of vestibulospinal neurones in the LVN were stimulated using an electrode made from an electrolytically etched tungsten wire (0.5 mm diameter) insulated except for its tip as a cathode, and a wire inserted into a neck muscle as an anode. Two to four stimuli of constant current 5.0 ms apart (0.2 ms, 50–100 µA) were applied in the MLF and one to five stimuli 3.3 or 2.5 ms apart (0.2 ms, 40–200 µA) in the LVN. The distribution of the stimulation sites, which were marked at the end of the experiments with an electrolytic lesion, is indicated in Fig. 1. These were within the MLF or at its lateral border at the level of the inferior olive (Fig. 1B) and within either rostral or caudal parts of LVN at the levels of the fastigial and interpositus nuclei (Fig. 1C and D). In two experiments, additional stimulation sites were rostral to the LVN, where fastigio-vestibular fibres providing input to it (Homma et al. 1995) were stimulated; one of these was at the medial border of the brachium conjunctivum (C). Peripheral nerves were stimulated with constant voltage stimuli (0.1 ms, intensity expressed in multiples of threshold (T) for the most sensitive fibres in a given nerve). The nerve stimulation was used to identify the motoneurones by their antidromic activation and to activate Renshaw cells via recurrent motor axon collaterals.
Recording and analysis
Intracellular records were obtained from 63 Sart and five Q motoneurones located in the 4th and 5th lumbar segments using glass micropipettes (1.5–2.0 µm tip diameter) filled with a 2 M potassium citrate solution. Descending volleys associated with the postsynaptic potentials (PSPs) evoked from the MLF and LVN were recorded from the lateral funiculus on the same side of the spinal cord as the motoneurones, usually within 5–10 mm of the microelectrode recording site. DC recording or low-pass filters were used when recording from motoneurones, and both the original records and averages of 10–40 single sweep records were stored (using a computer system designed by E. Eide, N. Pihlgren and T. Holmström, Göteborg University). Amplitudes and latencies of PSPs were measured from the averaged records.
Extracellular records from seven Ia inhibitory interneurones were used to evaluate effects of reticulospinal and vestibulospinal tract neurones upon them. The interneurones were identified by using criteria of Hultborn et al. (1971b), including activation by lowest threshold group I afferents, inhibition following stimulation of motor axons and the ability to be activated at high frequencies. Effects of excitatory and inhibitory stimuli on these neurones were quantified by comparing the number and the latencies of responses to 20–40 successive stimuli, from peristimulus histograms and cumulative sums of these responses, as in previous studies (e.g. Jankowska et al. 1997). Student's t test for paired normally distributed data was used for the statistical analysis.
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Results |
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Figure 2 illustrates changes in IPSPs evoked by short trains of MLF stimuli following stimulation of motor axons and activation of Renshaw cells in preparations in which the L4–S1 dorsal roots were transected. The records in A and D show IPSPs evoked by test stimuli alone. These IPSPs were evoked at segmental latencies of 1.1–1.5 ms (measured from the MLF descending volleys), which indicates that they were evoked disynaptically, i.e. via single inhibitory interneurones interposed between the MLF fibres and the contralateral motoneurones. These interneurones are represented by the shaded circle labelled ‘C’ in Fig. 1A. The larger amplitudes and steeper rising phases of the IPSPs evoked by successive stimuli are in keeping with temporal facilitation of activation of these inhibitory interneurones. A notch in the declining phase of the last IPSP evoked by stronger stimuli (at the level of the second broken line in Fig. 2C where records from A are expanded), or a longer duration, suggested however, that the disynaptic components of the IPSPs were followed by longer latency components attributable to actions of two interposed neurones rather than one, an excitatory interneurone activated by reticulospinal tract fibres, represented by the upper commissural interneurone in Fig. 1A, and an inhibitory interneurone.
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A total of 36 Sart and one Q motoneurones in which amplitudes of IPSPs evoked from MLF exceeded 0.5 mV, and in which the IPSPs were not preceded by EPSPs, were investigated in the way illustrated in Fig. 2. Following conditioning stimuli the first components of IPSPs evoked by the second or third stimuli (within about 1 ms from their onset) decreased only insignificantly (Table 1 column 5). However when the areas of the test and conditioned IPSPs including both the early and the later components (within 4 ms from their onset) were compared, highly statistically significant differences were found (Table 1, column 7).
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The difference in effects of conditioning stimuli on the early and later components of the IPSPs allows the depression of the later components to be attributed to the actions of Renshaw cells at a premotoneuronal rather than motoneuronal level, since any depression secondary to the effects of recurrent IPSPs evoked in the motoneurones (e.g. shunting) should have affected the early and late components of the IPSPs in a similar way. This conclusion is also consistent with the lack of relationship between the degree of depression of trisynaptic components of IPSPs of MLF origin and the size of the recurrent IPSPs recorded in motoneurones.
In order to estimate the relative contribution of Ia inhibitory interneurones and of inhibitory commissural interneurones to the IPSPs evoked from the MLF, a comparison was made between the size of the depressed area (represented by the ‘difference’ trace in Fig. 2) and of the area that resisted the effects of the conditioning stimuli. These areas were measured within 3 ms from their respective onsets. The size of the depressed areas was on average less than half the size (Table 1, column 9) of the early components that were not depressed. Considering that under our experimental conditions Renshaw cells only weakened but did not prevent activation of Ia inhibitory interneurones, this ratio suggests that the degree of inhibition mediated via the two potential parallel inhibitory pathways (see Fig. 1A), i.e. by excitatory commissural interneurones and Ia interneurones and by direct actions of inhibitory commissural interneurones, was comparable.
Depression of trisynaptic components of IPSPs evoked from the contralateral lateral vestibular nucleus by Renshaw cells
Our previous observations revealed that a considerable number of commissural interneurones are coexcited from the MLF and from the LVN (Jankowska et al. 2005) and that their inhibitory subpopulation mediates disynaptic inhibition of contralateral motoneurones (Krutki et al. 2003). It was therefore expected that not only disynaptic but also trisynaptic inhibition, via excitatory commissural interneurones and Ia inhibitory interneurones, would be likewise evoked not only from the MLF but also from the LVN. In order to verify this, the effects of Renshaw cells were tested under two experimental conditions. They were tested, firstly in motoneurones in which stimuli applied within the contralateral LVN (Fig. 3A and B) successfully evoked IPSPs, and secondly in motoneurones in which the appearance of the IPSPs required joint actions of LVN and MLF stimuli.
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The depression of IPSPs evoked at latencies of 1.4–1.8 ms was generally weak (Table 1, column 5). The depression of IPSPs evoked at latencies 
1.9 ms, was much more potent (Table 1, column 7) for IPSPs evoked by the fourth stimuli, and it was near total for IPSPs following the second and third stimuli (Fig. 3D and F).
When LVN stimuli alone did not evoke sufficiently distinct short-latency IPSPs, effects of Renshaw cells were tested on IPSPs induced by joint actions of LVN and MLF stimuli (Krutki et al. 2003). As shown in Table 1 (columns 5 and 7) the effects on these IPSPs were similar to those illustrated in Fig. 3. Since the IPSPs were due to the spatial facilitation of actions from the MLF and LVN, their depression reflects more directly effects mediated by commissural interneurones coexcited from the MLF and LVN.
In the whole sample the depressed area of IPSPs of LVN origin, constituted about one half (Table 1 column 9) of the early area that was not affected by Renshaw cells. The depressed components were evoked at segmental latencies 0.9 ± 0.1 ms longer than the latencies of the first components of the test IPSPs (Table 1, column 8). It appears thus that effects of Renshaw cells on IPSPs evoked from the LVN generally replicate the effects on IPSPs evoked from the MLF, and that the conclusions from the previous sections can be generalized to neurones mediating disynaptic and trisynaptic IPSPs of LVN origin.
Additional evidence for the mediation of IPSPs evoked from the reticular formation by Ia inhibitory interneurones
The depression of trisynaptic components of IPSPs of MLF or LVN origin by stimulation of motor axons would be compatible with these components being mediated not only by Ia inhibitory interneurones but also by Renshaw cells, in view of the mutual inhibitory interactions between Renshaw cells (Hultborn et al. 1968; Ryall, 1970; Hultborn et al. 1971a). Two additional tests were therefore made for the involvement of Ia interneurones.
The first test is illustrated in Fig. 4, which shows that mutual facilitation occurs between effects of stimuli that evoke IPSPs from group Ia afferents of an antagonist (Ia reciprocal IPSPs) and IPSPs from the MLF. When only very small IPSPs were evoked from the MLF (Fig. 4A) and from ipsilateral Q (Fig. 4B), joint application of the MLF and Q stimuli induced a much larger IPSP (Fig. 4C, black trace). The latter was much larger than the algebraic sum of effects of the two stimuli applied separately (Fig. 4C, grey trace) and it was almost as large as the IPSP evoked by stimulation of the Q nerve at an intensity near maximal for group Ia afferents (Fig. 4D). Since the two stimuli were timed so that the relayed MLF volley coincided with the Q volley (broken line in Fig. 4A–C), the facilitation is fully in keeping with the excitation of the same interneurones by Q group Ia afferents and by interneurones activated by MLF stimuli. Such facilitation was found in all seven motoneurones tested (3 Sart and 4 posterior biceps-semitendinosus (PBST)).
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Effects of Renshaw cells on IPSPs evoked from contralateral group II afferents
The most potent inhibition of contralateral hindlimb motoneurones is evoked via polysynaptic pathways from high-threshold muscle, skin and joint afferents, including group II as well as group III afferents (Eccles & Lundberg, 1959; Lundberg et al. 1987). Of these, group II afferents evoke inhibition that is particularly distinct (Harrison & Zytnicki, 1984). In addition to polysynaptic actions via several interneuronal systems (Lundberg et al. 1987), group II afferents may evoke IPSPs via only one or two interneurones interposed between these afferents and the contralateral motoneurones, i.e. disynaptically or trisynaptically (Arya et al. 1991). Disynaptic components of IPSPs of group II origin would thus be attributable to inhibitory commissural interneurones, but the trisynaptic and polysynaptic components could be mediated by Ia inhibitory interneurones as last-order interneurones, as proposed in Fig. 1A, in the same way as trisynaptic components of IPSPs evoked from the MLF.
In order to test this possibility we investigated effects of Renshaw cells on IPSPs evoked in 16 left-side Sart and Q motoneurones by group II afferents of the right Q nerve. The IPSPs were evoked by 3–5 T stimuli, but not by weaker stimuli, at segmental latencies of 2.5–4 ms. Conditioning stimuli were applied to the left deafferented Q nerve, and the resulting depression was evaluated in the same way as the depression of IPSPs evoked from the MLF and LVN.
The main results are illustrated in Fig. 6 where the test IPSPs are shown in A and D, and IPSPs preceded by conditioning stimuli (grey traces) are superimposed on recurrent IPSPs (black traces) in B and E. When the test and conditioned IPSPs were superimposed, and the latter subtracted from the former, as in C and F, only small differences between their earliest components were found. For the whole sample the decrease was not statistically significant (Table 1, column 5). However, the later components, as those after the second broken lines in Fig. 6C and F, were often depressed. The mean depression was also small (Table 1, column 7) but highly statistically significant. When the areas of the differences between the later components of the test and conditioned IPSPs were related to the areas of the earliest components that were not, or were only weakly depressed, the mean depressed area was found to amount to about one-third of the early ones (Table 1, column 9).
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Discussion |
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The results of this study show that disynaptic inhibition of contralateral motoneurones by reticulospinal and vestibulospinal tract fibres, evoked via commissural interneurones (Hongo et al. 1975; Bannatyne et al. 2003; Jankowska et al. 2003; Krutki et al. 2003), is associated with trisynaptic inhibition mediated by Ia inhibitory interneurones. The evidence rests on the demonstration that Renshaw cells selectively depress those components of IPSPs that are evoked at latencies about 1 ms longer than the latencies of the disynaptic components.
The depression is attributed to activation of Renshaw cells because typical recurrent IPSPs induced in motoneurones showed that conditioning stimuli effectively activated Renshaw cells. Furthermore, any effects of high-threshold afferents entering the spinal cord via ventral roots that might add to effects of Renshaw cells would require much stronger conditioning stimuli (> 10 T rather than 2–5 T) to excite C fibres as well as group III and IV fibres (Coggeshall et al. 1974). The depression is attributed to actions of Renshaw cells located on the same side of the spinal cord as the motoneurones, since terminal projection areas of lumbar Renshaw cells are exclusively ipsilateral (see, e.g. Scheibel & Scheibel, 1969; Lagerback & Kellerth, 1985).
IPSPs depressed by Renshaw cells are attributed to Ia inhibitory interneurones (those mediating reciprocal inhibition between flexors and extensors) in view of the previous evidence that only Ia inhibitory interneurones are both excited by group Ia afferents and inhibited by Renshaw cells (see Jankowska, 1992), and in keeping with the demonstration of the mutual facilitation between effects of stimulation of group Ia afferents and of the MLF, both on IPSPs and on responses of individual interneurones (Figs 4 and 5).
Ia inhibitory interneurones are proposed to be activated by axon collaterals of commissural interneurones which are monosynaptically excited by reticulospinal neurones, as outlined in Fig. 1A, i.e. trisynaptically, in view of only about 1 ms longer latencies of the depressed components (Table 1 column 9) than of the earliest components which have been previously shown to be evoked disynaptically (Jankowska et al. 2003). The morphologically delineated areas of location of target cells of commissural interneurones, both within and just outside the motor nuclei (Harrison et al. 1986; Bannatyne et al. 2003; Matsuyama et al. 2004) are also appropriate for this connection.
Our study thus reveals another case of the operation of Ia inhibitory interneurones as premotor interneurones – in trisynaptic pathways between contralaterally descending reticulospinal and vestibulospinal neurones and motoneurones. The previously demonstrated actions of Ia inhibitory interneurones included disynaptic inhibition from the ipsilateral vestibular nuclei in the cat (Hultborn & Udo, 1972; Bruggencate & Lundberg, 1974) and from the contralateral corticospinal tract neurones in primates (Jankowska et al. 1976), as well as polysynaptic inhibition evoked via ipsilaterally descending cortico-, rubro- and reticulospinal tract fibres in the cat (Hultborn & Udo, 1972). The present observations show thus that supraspinal inhibition of both contralateral and ipsilateral motoneurones may be modulated as a function of muscle stretch (monitored by group Ia afferents and their excitatory actions on Ia interneurones inhibiting these motoneurones) and of muscle activation (associated with activation of Renshaw cells by motor axon collaterals).
The degree to which Ia inhibitory interneurones contribute to inhibition evoked from contralateral group II muscle afferents is more difficult to estimate. With respect to the total inhibition evoked from contralateral group II afferents, the results of this study show that Ia inhibitory interneurones and Renshaw cells may modulate it to a smaller extent than inhibition of reticulospinal origin (Table 1, column 7). However, if the components of IPSPs mediated by Ia inhibitory interneurones (later components depressed by Renshaw cells) are related to the earliest (most likely disynaptic) components, the situation is different. As shown in Table 1 (column 9), Ia inhibitory interneurones may be used as last-order interneurones in pathways from group II afferents to a similar extent as the inhibitory commissural interneurones.
Differentiation of commissural interneurones mediating inhibition from the reticular formation, lateral vestibular nucleus and group II afferents
There are strong indications that interneurones mediating crossed disynaptic actions of reticulospinal fibres and of group II afferents belong to two distinct subpopulations, since no commissural interneurones recorded so far were found to be monosynaptically excited by both reticulospinal fibres and by group II afferents (Jankowska et al. 2005). For this reason separate commissural interneurones are indicated in Fig. 7 as mediating disynaptic inhibition of group II and reticulospinal origin (cells C1 and C2). Interneurones mediating disynaptic IPSPs from the MLF and LVN are represented by the same cell, labelled C2, although it is not known how large a proportion of their total population is shared and how many may have more selective actions.
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It should be added in this context that input from group I afferents to the excitatory commissural interneurones with input from reticulo- and/or vestibulospinal tract fibres (Jankowska et al. 2005) is in keeping with the enhancement of Ia reciprocal inhibition of motoneurones by stimulation of contralateral group I afferents (Harrison & Zytnicki, 1984). Polysynaptic input from contralateral flexor reflex afferents (including group II afferents) to commissural interneurones with monosynaptic vestibulospinal input would also explain joint inhibitory actions of these afferents and of ipsilateral vestibulospinal tract neurones via Ia inhibitory interneurones (Bruggencate & Lundberg, 1974).
The shared use of commissural interneurones (Krutki et al. 2003) or other spinal neurones (Li et al. 2001; Yeomans et al. 2002) as relay neurones by reticulospinal and vestibulospinal neuronal systems appears to parallel mutual interactions between these neuronal systems at the medullary level (Peterson & Felpel, 1971; Bolton et al. 1992). The question might therefore be asked whether the reported facilitation of reticulospinal actions on commissural interneurones by vestibular neurones does occur at the spinal, or at a medullary level. The latter possibility has to be kept in mind since effects of stimuli applied in the brain can seldom be restricted to only one particular neuronal system, even though previous control experiments demonstrated that the bulk of effects of stimuli applied in the MLF and LVN can be attributed to separate actions of reticulospinal and vestibulospinal neurones (Jankowska et al. 2003; Krutki et al. 2003; Matsuyama & Jankowska, 2004).
Functional considerations
It is still an open question whether all subpopulations of commissural interneurones, and if not which ones, play an essential role in inducing rhythmic locomotor movements, postural reactions and/or other movements evoked from the reticular formation and the vestibular nuclei (Wilson & Peterson, 1978; Grillner, 1981; Armstrong, 1986; Mori et al. 1989; Grillner et al. 1995; Li et al. 2001; Day & Cole, 2002; Noga et al. 2003). Whether the answer to this question is positive or negative, the two parallel ways of inducing inhibition of contralateral motoneurones of descending origin, either directly via inhibitory commissural interneurones (C2 interneurones in Fig. 7) or indirectly, via excitatory commissural interneurones (C3 interneurones in Fig. 7) and Ia inhibitory interneurones, will allow inhibitory effects of these interneurones to be modulated in a number of ways. The directly induced inhibition would to a greater extent depend on descending commands via reticulospinal neurones and their activation by corticospinal neurones (Jankowska et al. 2003; Edgley et al. 2004), or via vestibulospinal neurones and their activation from the cerebellum (Krutki et al. 2003; Matsuyama & Jankowska, 2004), motor cortex (Wilson et al. 1999) and the vestibular apparatus (see e.g. Carleton & Carpenter, 1983; Wilson et al. 1990). Inhibition mediated via Ia inhibitory interneurones would on the other hand be a function of the length and tension of the ipsilateral muscles, monitored by group Ia afferents and Renshaw cells, and their resulting actions, in addition to any descending actions on Ia inhibitory interneurones (see Jankowska, 1992).
The two parallel ways of inducing inhibition of contralateral motoneurones by group II afferents, directly via C1 interneurones in Fig. 7, and indirectly via C4 interneurones and Ia inhibitory interneurones, would likewise allow it to be a function of the length and tension of the ipsilateral muscles monitored by group Ia afferents and Renshaw cells, but also of the length of the contralateral muscles monitored by group II afferents themselves (see Matthews, 1972). On the top of these modulatory actions, transmission from group I and group II muscle afferents will be selectively modulated by GABAergic presynaptic inhibition (see Riddell et al. 1995) and transmission from both primary afferents and reticulospinal fibres by monoamines (see Riddell et al. 1993; Edgley et al. 2004).
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