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REPORT
1Tokyo Metropolitan Institute for Neuroscience, Tokyo 183-8526, Japan; 2Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki 444-8585, Japan; 3Institute of Physiology and Pharmacology, Department of Physiology, Göteborg University, 405 30 Göteborg, Sweden; 4Department of Integrative Medical Biology, Section of Physiology, Umeå University, 901 87 Umeå, Sweden; and 5Department of Integrative Physiology, Kyorin University School of Medicine, Shinkawa, Tokyo 181-8611, Japan
Submitted 2 April 2004; accepted in final form 25 May 2005
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ABSTRACT |
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INTRODUCTION |
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; Phillips and Porter 1971; Porter and Lemon 1993; Shapovalov 1975). Because the ability to perform skilled finger movements with the hand has likewise increased during development, it was suggested that the monosynaptic corticomotoneuronal (CM; henceforth referred to as direct CM) connection might play a decisive role in this control (Bernhard and Bohm 1954). In behavioral experiments in the macaque monkey, Lawrence and Kuypers showed that pyramidotomy caused near permanent loss of the precision grip and of independent finger movements (IFMs) of the hand (Lawrence and Kuypers 1968a, b). Transection of the rubrospinal tract (RST) after pyramidotomy aggravated the symptoms, suggesting a role also for the RST. It has later been shown that after pyramidotomy, some recovery may occur after 
1 yr (for references, see Porter and Lemon 1993). To test the role of the direct and indirect CM pathways, we have now made lesions of the CST in the lateral funicle at the border of the C4–C5 segments (C4/C5), which is just rostral to the forelimb MNs. |
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METHODS |
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Three female monkeys (Macaca fuscata), body weight 5.35, 4.75, and 4.5 kg, were trained to retrieve a morsel of food from a horizontal tube positioned in the mid-sagittal plane, at shoulder level and at a sagittal distance of 15 cm. Each experiment (30 min) consisted of 100 trials. In each trial, the animal retrieved, with the precision grip, a morsel of food positioned on a pin that was inserted through the bottom of the tube. The movements were filmed with standard video cameras (33 Hz) positioned above, below, and on the side of the performing limb.
Surgery
The animals were first anesthetized with ketamine (0.3 ml) and Xylazine (0.6 ml) and then with pentobarbital sodium (Nembutal, 60 mg/kg). The border between the C4 and C5 segments was exposed by a laminectomy, and a transverse opening was made in the dura. The CST lesion was made under a surgical microscope, in three steps.1) A small opening in the pia mater was made at the lateral convexity of the spinal cord. A horizontal strip in mediolateral direction of the lateral funicle was then made by inserting a minute hook into the opening. The hook was prepared from a 0.4 mm (OD) cannula. The tip (0.5 mm) was first bent (with fine pliers) at a right angle to assume the shape of a hook. To provide stability during insertion into the spinal cord, the cannula was bent a second time, at a right angle 5 mm from the tip. In other words, the cannula assumed an L-shape with a small hook at the tip. In this way, the proximal part of the cannula could be held firmly by a small surgical clamp during insertion of the tip into the spinal cord. In addition, bending the cannula a second time assured that the hook could not be inserted >5 mm deep, which corresponds to the distance from the lateral convexity of the spinal cord to the midline. 2) The dorsal part of the lateral funicle was transected, with watch maker's forceps, from the dorsal root entry zone ventrally to the level of the horizontal strip lesioned in step 1. 3) The lesion was extended ventrally, with watch maker's forceps, at the most lateral part of the lateral funiculus.
During surgery, the direct descending corticospinal volley, evoked by transcranial magnetic stimulation, was recorded from the dorsal part of the lateral funiculus in C5 before and after the lesion (in monkeys I and G, not illustrated).
The opening of the dura mater was closed by a substitute (Preclude, Gore and Associates). The skin and back muscles were sutured with nylon or silk thread.
Electrophysiological experiments
The animals were first anesthetized with ketamine (0.3 ml) and Xylazine (0.6 ml) and after the tracheotomy, isofluorane was used throughout the surgery. After surgery, anesthesia was changed to 
-chloralose 75–100 mg/kg. Blood pressure was maintained around 100 mmHg and pCO2 at 4.0%. A drip of Ringer-glucose was given during the entire experiment, and the urinary bladder was emptied regularly. Atropin (0.5 mg), decadrone (4 mg), gentacine (1 ml) were given just after anesthesia. Atropin was given at intervals of 4–5 h. The animals were paralyzed with pancuronium bromide (Myoblock 1 ml, 0.2 mg/ml) given at 30-min interval and artificially ventilated with a pump. A pneumothorax was made just prior to intracellular recording.
A craniotomy was made that exposed the posterior part of cerebellum and the caudal brain stem to place the pyramidal electrode. It was calibrated at the obex (angle 65° from the vertical line) and placed 2.5 mm rostrally and 1.25 mm laterally and at depth of 5.0 mm from the bottom of IVth ventricle. The threshold for eliciting the descending pyramidal volley was usually 5 µA. Monopolar cathodal pulses (0.1-ms duration) were applied by using tungsten electrodes with an impedance 50–100 k
and a tip diameter of 10 µm. A laminectomy was made of the C2–Th1 and of the Th6–Th10 segments. The DR nerve was dissected and mounted in a cuff with bipolar silver electrodes. Other forelimb nerves were stimulated with inserted needle electrodes through the skin.
Bipolar recordings of the descending volleys were made from dissected spinal halves in the Th6–Th10 segments as described before (Alstermark et al. 1981). Intracellular recordings were made from antidromically identified forelimb MNs (and unidentified MNs) in the lateral motor nuclei of the C6–Th1 segments. Glass capillary electrodes (tip diameter: 1.0 µm, impedance: 3–5 M) filled with 2 M potassium citrate were used. The cord dorsum potential was monitored with a silver ball electrode.
The experiments were subjected to prior ethical reviews by the ethical committee of the Okazaki Organization of National Institutes and were performed in accordance with the National Institutes of Health guideline for the Care and Use of Laboratory Animals.
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RESULTS |
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; Porter and Lemon 1993) of CS fibers (Y) or were larger than this area (I and G). To assess the C4/C5 lesions, electrophysiological recordings were made caudally. Figure 1B shows recordings from the spinal half at mid thoracic level on the intact and lesioned sides. On the intact side, electrical stimulation of the contralateral pyramid (co Pyr) evoked a direct CS volley followed, with a delay of 1.2 ms, by a synaptic volley. The latter volley is presumably caused by monosynaptic Pyr activation of neurons with long descending axons. In contrast, on the lesioned side, the direct CS volley was completely abolished (solid line), while the synaptic volley (interrupted line) remained (mediated by descending axons in an intact funicle).
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The latency to the onset of the disynaptic field was similar on the intact and lesioned sides (interrupted line). Similar electrophysiological results were obtained in the three monkeys.
Intracellular recording was made from a total of 59 forelimb MNs in C6–C8 in the three animals on the intact (n = 22) and lesioned (n = 37) sides. Pyr stimulation evoked EPSPs in all MNs on the intact side (IPSP were recorded in 4 cells) and in 18 MNs on the lesioned side (IPSPs were seen in 9 cells). Measurements of the latency from the arrival of the descending CS volley to the onset of the EPSPs (Fig. 2H ) showed a monosynaptic range (from 0.4 to 1.0 ms) on the intact side (white area), but a disynaptic range (1.0–1.8 ms) in 15 cells on the lesioned side (black area) and possibly a trisynaptic range (from 1.8 to 2.0 ms) in 3 cells. Figure 2, A–C, shows intracellular recordings from a deep radial motoneuron on the intact side. A single Pyr stimulus (A) evoked a monosynaptic EPSP, which was cut by a disynaptic IPSP (see G,
). On the lesioned side (Fig. 2, D–F), recordings from another deep radial motoneuron show that Pyr stimulation failed to evoke a monosynaptic EPSP.
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). After the second and third Pyr volleys, the EPSP was slightly facilitated and was followed by an IPSP (F, ), which started at the peak of the EPSP. Figure 2G shows a comparison of the averaged traces of the EPSPs evoked by a single stimulus on the intact (A) and lesioned (D) sides. The EPSP evoked in the motoneuron on the lesioned side starts 0.9 ms later than the EPSP in the motoneuron on the intact side, corresponding to one intercalated neuron. Note that the onset of the IPSP (G, ; intact side) was similar as for the EPSP of the lesioned side, with a disynaptic linkage in both cases. Based on these electrophysiological results, in addition to the histological controls (Fig. 1), we conclude that the CST lesions in the three monkeys were complete but that disynaptic Pyr excitation could still be evoked in forelimb MNs on the lesioned side.
The ability to take a morsel of food with a precision grip was tested as shown in Fig. 3 (A–C, view from above and D from below) with video frames and in Fig. 4 (A–C, top view) with stick figures of the index finger and thumb. A preoperative trial is shown in Fig. 3A. In monkey Y, the precision grip was present already the first postoperative day (Fig. 3B). The preshaping prior to contact with the morsel was reduced. The aperture between the finger tips was smaller than the thickness of the morsel, and it was common that the thumb hit the posterior part of the morsel. Then the monkey widened the aperture, and the thumb was positioned on the side of the morsel allowing a precision grip by flexion of the proximal interphalangeal joint of the index finger and opposing movement of the thumb (Fig. 4A). Compared with the preoperative movement, it was common that the digits slipped during removal presumably due to low grip force so that more than one attempt was required. Another difference from the preoperative state was that the duration of the movement was substantially increased as is evident from the time-lines in Fig. 3, A–C (postoperative day 7). These defects became gradually less pronounced but remained to the end of the observation period (3 mo). A decreased force and slowing of the movement was also found after pyramidotomy and after cervical hemisection of the spinal cord (Galea and Darian-Smith 1997).
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Postoperatively, it was evident in some trials already in the first experiments in monkey Y, that the thumb during preshaping could be moved without concomitant movements of digits 3–5. During the two first postoperative weeks, the ability to perform independent finger movements improved, and in several trials, the extension of the index finger during preshaping was not accompanied by parallel extension of the other digits.
Figure 4D shows superimposed stick figures of the index finger (D2) and of digit 5 (D5) viewed from the lateral side at the time of contact with the morsel. When the index finger was flexed during removal of the morsel, there was always parallel flexion of digit 5. This was the case throughout a postoperative observation period of 3 mo in the three monkeys.
Independent finger movements were present regularly on the 9th postoperative day in monkey Y (smallest lesion), on the 25th day in monkey I, and on the 28th day in monkey G.
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DISCUSSION |
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; Lawrence and Kuypers 1968a, b). After complete pyramidotomy, independent finger movements were abolished for the whole observation period of 
11 mo (Lawrence and Kuypers 1968a). In contrast, although all our monkeys showed deficits in preshaping and force between the index finger and thumb, they could grasp the morsel of food by using independent finger movements after 1–28 days postoperatively. Because the present lesions abolished both monosynaptic CM excitation as well as excitation mediated via segmental interneurons (below C5), we conclude that these pathways are not solely responsible for fine finger control as has been taken for granted during several decades especially for the monosynaptic excitatory CM connection. However, deficits in force and preshaping of the index finger and thumb prior to grasping were clearly evident after the lesions and are most likely dependent on the monosynaptic CM pathway.
It is indeed remarkable that the command for precision grip and independent digit movements can be mediated via nonmonosynaptic CM pathways. A comparison with the location of the RST (Holstege et al. 1988) suggests an incomplete RST lesion in monkey Y but not in monkeys I and G. One possibility is that the modest effect of the lesion in monkey Y on the precision grip is due to a RST takeover. It is noteworthy that 60% of the RS neurons are activated during grasping of food from small holes in the Klüver test (Miller et al. 1993). A reorganization of the RS output to forearm muscles was found after pyramidotomy, such that the normally predominant extensor excitation and flexor suppression was diminished (Belhaj-Saif and Cheney 2000).
As an alternative to an RST takeover, the possible role of propriospinal neurons (PNs) should be considered. It was recently shown that disynaptic CM EPSPs in the macaque monkey can be mediated via PNs in the C3–C4 segments (Alstermark et al. 1999). This system was first described in the cat (Illert et al. 1977), which lacks monosynaptic CM connections. In the macaque monkey, the C3–C4 PNs are under strong inhibitory control, and disynaptic EPSPs were found regularly only after intravenous injection of strychnine (Alstermark et al. 1999). In the present study, disynaptic CM EPSPs could be induced even without strychnine in half of the forelimb MNs after the CS lesion in C4/C5, occasionally even by a single stimulus (Fig. 2D). It is postulated that the strength of inhibition has decreased so that C3–C4 PNs mediating disynaptic EPSPs are more readily activated after a chronic CST lesion. Enhanced propriospinal excitation of upper limb MNs was found in stroke patients (Mazevet et al. 2003).
In monkeys I and G (Fig. 1A), the lesions extended more ventrally than in monkey Y and probably completely transected the RST. However, it is unlikely that these lesions have transected a significant part of the axons of the C3–C4 PNs because intracellular recording from forelimb MNs confirmed that disynaptic Pyr EPSPs could be evoked in all three monkeys, and threshold mapping of the axons of C3-C4 PNs has shown that they surround the ventral horn and extend ventromedially to the base (Alstermark and Isa, unpublished data). Furthermore, in monkey G, we added an acute transection of the CST in C2 (not illustrated), where after disynaptic CM EPSPs were abolished in six of six tested MNs, which shows that disynaptic Pyr EPSPs indeed could be mediated via C3–C4 PNs despite the larger lesion.
In the cat, C3–C4 PNs mediate the command for forelimb target reaching, while the command for grasping with the forepaw is mediated by interneurons in the forelimb segments (Alstermark et al. 1981). However, recently Blagovechtchenski et al. (2000) found that after combined spinal cord lesions (CST+RuST in C5 and ventral quadrant lesion in C2) the C3–C4 PNs can mediate the command for some components of grasping like flexion in the proximal interphalangeal joints, but not supination and flexion in the metacarpophalangeal joints by which intact cats bring the morsel of food to the mouth. It may be hypothesized that evolution has given the C3–C4 PN system a new or additional role in primates to command the precision grip in relation to reaching. This may explain why the precision grip and independent digit movements remain after transection of the CST. There is some evidence from cortical lesions which may support a C3–C4 PN takeover. Some CS fibers originate in the premotor (PM) area and terminate in the C2–C4 segments (Martino and Strick 1987). The recovery of manual dexterity after lesion of the hand area in MI was abolished by reversible inactivation of PM (Liu and Rouiller 1999). The recovery after the MI lesion was very slow and incomplete. Structural reorganization in PM has been observed after M1 lesion (Frost et al. 2003).
Our findings suggest that the role of CM pathways in commanding the precision grip and independent digit movements must be broadened and include not only the direct connection but also indirect ones. Transmission is apparently so effective that the precision grip and independent finger movements can be made within a day (monkey Y) even if the monosynaptic CM connection (and to segmental interneurons) is broken.
The fact that interneuronal networks exist may be important for neuro-rehabilitation. Physiotherapy must aim at mobilizing these networks, and such a mobilization may explain the recovery of the precision grip and independent digit movements that may be observed in humans after complete interruption of the CM pathways in the brain stem (Bach-y-Rita 1981).
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Address for reprint requests and other correspondence: B. Alstermark, Dept. of Integrative Medical Biology, Section of Physiology, Umeå University, S-901 87 Umeå, Sweden (E-mail: Bror.Alstermark{at}physiol.umu.se).
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ABSTRACT
INTRODUCTION
