Brain Research, 514 (1990) 128-130
128
Elsevier BRES 24047
Short Communications
Monosynaptic connexions of single V interneurones to the contralateral V motor nucleus in anaesthetised rats Kwabena Appenteng, Lisa Conyers, John Curtis and Jane Moore Department of Physiology, University of Leeds, Leeds (U. K.) (Accepted 26 December 1989)
Key words: Spike-triggered averaging; Motor control; Trigeminal
We have used the extracellular spike triggered averaging method to obtain evidence for a monosynaptic connexion of single V (trigeminal) interneurones, located in the region immediately caudal to the V motor nucleus, onto neurones within the contralateral V motor nucleus. The extracellular fields recorded in the contralateral nucleus are of smaller amplitude than those detected within the ipsilateral nucleus and the implications of this are discussed. A significant difference between the hindlimb and masticatory m o t o r systems is that unilateral electrical stimulation of p e r i p h e r a l nerve fibres commonly results in bilaterally asymmetrical effects in hindlimb motoneurones 5"1° but symmetrical effects in masticatory motoneurones. F o r example electrical stimulation of the masseter nerve, inferior alveolar or lingual nerves produces an initial bilateral excitation of digastric motoneurones and an inhibition of masseter m o t o n e u r o n e s 4'6"9. The latency difference between the ipsilateral and contralateral effects is 0.4 ms or less, implying that the contralateral p r o j e c t i o n is a direct one. T h e r e is little specific evidence as to how the contralateral effects are m e d i a t e d but the available evidence is p e r h a p s strongest for an involvement of interneurones because extracellular injections of H R P into the m o t o r nucleus result in labelling of neurones on the contralateral side 7'8'12. One p r o m i n e n t l y labelled area is the region i m m e d i a t e l y caudal to the m o t o r nucleus and this is of interest because we have recently shown that many neurones in the same area make monosynaptic excitatory connexions within the ipsilateral m o t o r nucleus 2. We therefore set out to obtain specific evidence for a contralateral projection of interneurones from this area and then to compare the projections of interneurones to the ipsilateral and contralateral m o t o r nuclei. Our approach involved use of the extracellular spike triggered averaging technique 12 to assess if single identified interneurones m a d e synaptic connexions within the contralateral V m o t o r nucleus. The preliminary results have been r e p o r t e d to the Physiological Society I.
The methods used were essentially those described by A p p e n t e n g et al. 2, the only exception being that the masseter nerve on each side was isolated in continuity for electrical stimulation using the m e t h o d s described by A p p e n t e n g et al. 3. In brief, rats were anaesthetised with p e n t o b a r b i t o n e (initial dose = 60 mg/kg i.v., supplementary doses given as necessary), the trachea cannulated and blood pressure m o n i t o r e d via a femoral arterial cannula. Following exposure of the masseter nerves, animals were transferred to a stereotaxic frame, paralysed and holes drilled in the cranium to allow insertion of electrodes into both the left and right V m o t o r nuclei and the adjoining regions. A n i m a l s were maintained deeply anaesthetised throughout all stages of the experiment. The criterion used was that a noxious paw-pinch should elicit no change in blood pressure and under these conditions there was no flexion withdrawal reflex in the unparalysed animal. A glass electrode filled with oL-homocysteic acid ( D L H ) was used to m a k e unitary recordings from interneurones located in the region i m m e d i a t e l y caudal to the V m o t o r nucleus. N e u r o n e s that lay outside the m o t o r nucleus or the mesencephalic nucleus were assumed to be interneurones for the purposes of this study. Iontophoretic application of D L H was used to distinguish between somatic and axonal recordings. The latter were assumed to be fibres of passage and so were ignored. Somatic recordings were then further tested to determine the pattern of inputs on to them using both natural stimulation applied to the m a n d i b u l a r and maxillary areas and also electrical stimulation of the masseter nerve. The
Correspondence: K. Appenteng, Dept. of Physiology, Univ. of Leeds, Leeds LS2 9NQ, U.K.
129
A
C
B
D
O.5~V 1ms
1ms
Fig. 1. Examples of e/c s.t.a, fields obtained in the contralateral motor nucleus when triggering off four different interneurones. A and B are examples of negative fields and C and D examples of positive fields. Responses in A and D obtained at same point in the motor nucleus in one experiment. Start of time bars mark onset of triggering interneurone spike; 3975 sweeps used to construct average in A, 710 for B, 3000 for C and 3744 for D; receptive fields of interneurones generating the fields: A; skin on upper lip, B; masseter muscle and also activated by muscle stretch, C; skin on lower lip, D; skin on both lips.
electrical stimulation consisted of stimulus pulses of duration 0.5 ms, applied at intensities of less than 3x the threshold (T) value required to elicit a just perceptible jaw-jerk in the unparalysed animal 3. The natural stimuli routinely used were: light brushing or stroking of the skin, lips and tongue with a cotton bud; gentle probing over the masseter and temporalis muscles; firm pressure applied to the skin and lips; and a strong (noxious) pinch of the skin and lips. A glass-coated tungsten electrode was then inserted into the centre of the contralateral masseter motoneurone pool which was signalled by the presence of a 1-2 mV antidromic field. All data was recorded online using a C.E.D. 1401 interface (Cambridge Electronic Devices) set to sample at 40 kHz for perispike averaging and at 60 kHz for poststimulus averaging. Extracellular activity recorded by the tungsten electrode was bandpass filtered between 55 Hz and 5 kHz and unitary activity recorded by the glass electrode filtered as appropriate. Electrode tracts were identified by standard histological techniques after the completion of each experiment. We have recorded from 96 interneurones and obtained unitary extracellular fields in the contralateral motor nucleus from 18 of them. Five gave negative fields and 13 positive fields. The fields were small but nonetheless discrete and were similar in form to those obtained in the ipsilateral motor nucleus 2. Fig. 1 shows examples of two negative fields (Fig. 1A,B) and two positive fields (Fig. 1C,D). Note that the fields are all preceded by an initial sharp biphasic presynaptic spike which is then followed after an interval by either a negative (Fig. 1A,B) or positive-going field (Fig. 1C,D). We have previously argued that the presence of prominent presynaptic spikes
is an indication that the response is unlikely to be significantly affected by synchronization of presynaptic neurones 2. All the extracellular fields were accompanied by clear but small presynaptic spikes. The amplitude of these ranged from 0.3 to 3.6 pV (mean = 1.2; S.D. = 0.9; n = 16). The latency from the onset of the triggering spike to the positive peak of the presynaptic spike provides an estimate of the conduction time from the interneurone somata to the motor nucleus and values for this ranged from 0.1 to 0.6 ms (n = 11) for the positive fields and from 0.1 to 0.5 ms (n = 5) for the negative fields (mean for total sample = 0.23; S.D. = 0.13; n = 16). The latency from the positive peak of the presynaptic spike to the onset of the fields provides an estimate of the synaptic delay and the values obtained ranged from 0.2 to 0.4 ms for the positive fields and 0.2 to 0.5 for the negative fields (mean for total sample = 0.33 ms; S.D. = 0.11; n = 12). Both sets of values suggest that the axons of interneurones travel directly to the contralateral motor nucleus where they then make synaptic connexions. Presynaptic spikes were obtained when averaging at a single point in the motor nucleus from 9 of the neurones
0.0 m m
]o.s v
lmv 0.2ram
~
~
0.4ram
/
0.6mm
]0.5/~V "
i
4ms
i
~
i
]lmV
J
1ms
Fig. 2. Variation in the extracellular responses generated at different depths in the motor nucleus by a single interneurone (same as in Fig. 1A). The left panel shows the unitary responses (2868-5776 sweeps used to construct averages) and the right panel the masseter-evoked antidromic field at the same depths (stimulus intensity of 3 x T for each, stimulus polarity reversed for response at 0.6 mm). Note that a presynaptic spike is seen at all depths but a clear unitary field is seen only at the point of maximum antidromic field (0.4 mm).
130 which did not give extracellular fields. The conduction time for these presynaptic spikes ranged from 0.1 to 0.3 ms and so suggests that they were directly conducted to the motor nucleus. The absence of a field after these spikes could indicate that the axons terminated elsewhere in the nucleus or were simply passing through the nucleus on their way elsewhere. We routinely averaged up to 1000 sweeps but occasionally up to 5000 were needed to produce a clear response and so it is also possible that we may have missed some of the weaker projections by not averaging enough sweeps. We recorded the fields generated at different depths in the motor nucleus for 5 neurones and found these to be of maximal amplitude near the point of maximal antidromic field (Fig. 2). Four of the neurones tested gave positive fields and one a negative field. When measured at the point of maximal antidromic field the amplitude of all the positive fields ranged from 0.3 to 2.0/~V (mean = 0.88/~V; S.D. = 0.55; n = 9) and from 0.5 to 1.7/~V (mean = 1.2/xV; n = 4) for the negative fields. Neurones giving positive fields were activated by afferent input from just one modality. This was cutaneous in 10 cases, intraoral in two and masseter muscle in one. In 5 cases the cutaneous input required was a firm pressure to the skin round the lips and in 3 a light stroking over a wider area. Neurones giving negative fields were activated by a variety of inputs ranging from a nonnoxious cutaneous input (n = 1), intraoral (n = 2), cutaneous and intraoral (n = 1) and masseter and cutaneous (n = 1). Four of the 9 neurones giving only presynaptic spikes were activated by cutaneous input alone (in one case involving a noxious pinch), one by intraoral input, another by input from the masseter muscle, two by both cutaneous and intraoral input and one by a combination of all 3 peripheral inputs. Thirty-six of the remaining 69 neurones that did not give either fields or
presynaptic spikes were activated by cutaneous input alone (8 requiring a noxious pinch), 13 by intraoral input, 3 by input from the masseter muscle and the remaining 17 neurones by a combination of 2 of these 3 inputs. The contralateral projection of interneurones differs from the ipsilateral one both as regards the relative proportion of positive and negative fields detected and in the amplitude of those fields. Positive fields were rare in the ipsilateral motor nucleus and accounted for only 4 of the 50 fields detected there 2 whereas they were the predominant type of field in the contralateral nucleus. Negative fields represent an excitatory projection TM but the positive fields may represent either an inhibitory input or outward current from remote excitation. Significantly more sweeps were required to reveal a contralateral projection than an ipsilateral one. For example between 50 and 100 sweeps were all that were required to reveal a projection of interneurones to the ipsilateral motor nucleus 2 whereas 1000 were routinely required to reveal a contralateral projection. The amplitude of the contralateral negative fields were towards the lower end of the range obtained ipsilaterally (range = 0.4-10.8 ~V; mean = 3.19; S.D. = 2.13; n = 46; ref 2). The smaller field amplitudes recorded contralaterally could imply that less current is injected into the contralateral masseter motoneurone pool, perhaps because fewer boutons are involved in the projection. Alternatively the fields could be smaller because there is more variability in transmission of synaptic effects contralaterally. This could result from an insecurity in conduction of activity to the synaptic terminals in the contralateral nucleus or else greater variability in release of transmitter in response to each impulse. We can not distinguish between these possibilities but our data does point to potential differences in organisation of synaptic connexions to the two motor nuclei.
1 Appenteng, K., Conyers, L., Curtis, J.C. and Moore, J.A., Mapping the monosynaptic connexions of identified trigeminal interneurones in anaesthetised rats, J. Physiol (Lond.), 416 (1989) 4P. 2 Appenteng, K., Conyers, L. and Moore, J.A., The monosynaptic excitatory connexions of single trigeminal interneurones to the v motor nucleus of the rat, J, Physiol. (Lond.), 417 (1989) 91-104. 3 Appenteng, K., Donga, R. and Williams, R.G., Morphological and electrophysiological determination of the central projections of jaw-elevator muscle spindle afferents, J. Physiol. (Lond.), 369 (1985) 93-113. 4 Goidberg, L.J. and Nakamura, Y., Lingually induced inhibition of masseteric motoneurones, Experientia, 24 (1968) 371-373. 5 Harrison, P.J. and Zytnicki, D., Crossed actions of group I muscle afferents in the cat, J. Physiol. (Loud.), 356 (1984) 263-273. 6 Kidokoro, Y., Kubota, K., Shuto, S. and Sumino, R., Reflex organisation of cat masticatory muscles, J. Neurophysiol., 31
(1968) 695-708. 7 Landgren, S., Olsson, K.A. and Westberg, K.G., Bulbar neurones with axonal projections to the trigeminal motor nucleus in the cat, Exp. Brain Res., 65 (1986) 98-111. 8 Mizuno, N., Yasui, Y., Nomura, S., Itoh, K., Konishi, A., Takada, M. and Kudo, M., A light and electron microscopic study of premotor neurones for the trigeminal motor system, J. Comp. NeuroL, 215 (1983) 290-298. 9 Nakamura, Y., Nagashima, H. and Mori, S., Bilateral effects of the afferent impulses from the masseteric muscle on the trigeminal motoneuron of the cat, Brain Res., 57 (1973) 15-27. 10 Perl, E.R., Effects of muscle stretch on excitability of contralateral motoneurons, J. Physiol. (Lond.), 145 (1959) 193-203. 11 Taylor, A., Stephens, J.A., Somjen, G., Appenteng, K. and O'Donovan, M.J., Extracellular spike-triggered averaging for plotting synaptic projections, Brain Res., 140 (1978) 344-348. 12 Travers, J.B. and Norgren, R., Afferent projections to the oral motor nuclei in the rat, J. Comp. Neurol., 220 (1983) 280-298.
128
Elsevier BRES 24047
Short Communications
Monosynaptic connexions of single V interneurones to the contralateral V motor nucleus in anaesthetised rats Kwabena Appenteng, Lisa Conyers, John Curtis and Jane Moore Department of Physiology, University of Leeds, Leeds (U. K.) (Accepted 26 December 1989)
Key words: Spike-triggered averaging; Motor control; Trigeminal
We have used the extracellular spike triggered averaging method to obtain evidence for a monosynaptic connexion of single V (trigeminal) interneurones, located in the region immediately caudal to the V motor nucleus, onto neurones within the contralateral V motor nucleus. The extracellular fields recorded in the contralateral nucleus are of smaller amplitude than those detected within the ipsilateral nucleus and the implications of this are discussed. A significant difference between the hindlimb and masticatory m o t o r systems is that unilateral electrical stimulation of p e r i p h e r a l nerve fibres commonly results in bilaterally asymmetrical effects in hindlimb motoneurones 5"1° but symmetrical effects in masticatory motoneurones. F o r example electrical stimulation of the masseter nerve, inferior alveolar or lingual nerves produces an initial bilateral excitation of digastric motoneurones and an inhibition of masseter m o t o n e u r o n e s 4'6"9. The latency difference between the ipsilateral and contralateral effects is 0.4 ms or less, implying that the contralateral p r o j e c t i o n is a direct one. T h e r e is little specific evidence as to how the contralateral effects are m e d i a t e d but the available evidence is p e r h a p s strongest for an involvement of interneurones because extracellular injections of H R P into the m o t o r nucleus result in labelling of neurones on the contralateral side 7'8'12. One p r o m i n e n t l y labelled area is the region i m m e d i a t e l y caudal to the m o t o r nucleus and this is of interest because we have recently shown that many neurones in the same area make monosynaptic excitatory connexions within the ipsilateral m o t o r nucleus 2. We therefore set out to obtain specific evidence for a contralateral projection of interneurones from this area and then to compare the projections of interneurones to the ipsilateral and contralateral m o t o r nuclei. Our approach involved use of the extracellular spike triggered averaging technique 12 to assess if single identified interneurones m a d e synaptic connexions within the contralateral V m o t o r nucleus. The preliminary results have been r e p o r t e d to the Physiological Society I.
The methods used were essentially those described by A p p e n t e n g et al. 2, the only exception being that the masseter nerve on each side was isolated in continuity for electrical stimulation using the m e t h o d s described by A p p e n t e n g et al. 3. In brief, rats were anaesthetised with p e n t o b a r b i t o n e (initial dose = 60 mg/kg i.v., supplementary doses given as necessary), the trachea cannulated and blood pressure m o n i t o r e d via a femoral arterial cannula. Following exposure of the masseter nerves, animals were transferred to a stereotaxic frame, paralysed and holes drilled in the cranium to allow insertion of electrodes into both the left and right V m o t o r nuclei and the adjoining regions. A n i m a l s were maintained deeply anaesthetised throughout all stages of the experiment. The criterion used was that a noxious paw-pinch should elicit no change in blood pressure and under these conditions there was no flexion withdrawal reflex in the unparalysed animal. A glass electrode filled with oL-homocysteic acid ( D L H ) was used to m a k e unitary recordings from interneurones located in the region i m m e d i a t e l y caudal to the V m o t o r nucleus. N e u r o n e s that lay outside the m o t o r nucleus or the mesencephalic nucleus were assumed to be interneurones for the purposes of this study. Iontophoretic application of D L H was used to distinguish between somatic and axonal recordings. The latter were assumed to be fibres of passage and so were ignored. Somatic recordings were then further tested to determine the pattern of inputs on to them using both natural stimulation applied to the m a n d i b u l a r and maxillary areas and also electrical stimulation of the masseter nerve. The
Correspondence: K. Appenteng, Dept. of Physiology, Univ. of Leeds, Leeds LS2 9NQ, U.K.
129
A
C
B
D
O.5~V 1ms
1ms
Fig. 1. Examples of e/c s.t.a, fields obtained in the contralateral motor nucleus when triggering off four different interneurones. A and B are examples of negative fields and C and D examples of positive fields. Responses in A and D obtained at same point in the motor nucleus in one experiment. Start of time bars mark onset of triggering interneurone spike; 3975 sweeps used to construct average in A, 710 for B, 3000 for C and 3744 for D; receptive fields of interneurones generating the fields: A; skin on upper lip, B; masseter muscle and also activated by muscle stretch, C; skin on lower lip, D; skin on both lips.
electrical stimulation consisted of stimulus pulses of duration 0.5 ms, applied at intensities of less than 3x the threshold (T) value required to elicit a just perceptible jaw-jerk in the unparalysed animal 3. The natural stimuli routinely used were: light brushing or stroking of the skin, lips and tongue with a cotton bud; gentle probing over the masseter and temporalis muscles; firm pressure applied to the skin and lips; and a strong (noxious) pinch of the skin and lips. A glass-coated tungsten electrode was then inserted into the centre of the contralateral masseter motoneurone pool which was signalled by the presence of a 1-2 mV antidromic field. All data was recorded online using a C.E.D. 1401 interface (Cambridge Electronic Devices) set to sample at 40 kHz for perispike averaging and at 60 kHz for poststimulus averaging. Extracellular activity recorded by the tungsten electrode was bandpass filtered between 55 Hz and 5 kHz and unitary activity recorded by the glass electrode filtered as appropriate. Electrode tracts were identified by standard histological techniques after the completion of each experiment. We have recorded from 96 interneurones and obtained unitary extracellular fields in the contralateral motor nucleus from 18 of them. Five gave negative fields and 13 positive fields. The fields were small but nonetheless discrete and were similar in form to those obtained in the ipsilateral motor nucleus 2. Fig. 1 shows examples of two negative fields (Fig. 1A,B) and two positive fields (Fig. 1C,D). Note that the fields are all preceded by an initial sharp biphasic presynaptic spike which is then followed after an interval by either a negative (Fig. 1A,B) or positive-going field (Fig. 1C,D). We have previously argued that the presence of prominent presynaptic spikes
is an indication that the response is unlikely to be significantly affected by synchronization of presynaptic neurones 2. All the extracellular fields were accompanied by clear but small presynaptic spikes. The amplitude of these ranged from 0.3 to 3.6 pV (mean = 1.2; S.D. = 0.9; n = 16). The latency from the onset of the triggering spike to the positive peak of the presynaptic spike provides an estimate of the conduction time from the interneurone somata to the motor nucleus and values for this ranged from 0.1 to 0.6 ms (n = 11) for the positive fields and from 0.1 to 0.5 ms (n = 5) for the negative fields (mean for total sample = 0.23; S.D. = 0.13; n = 16). The latency from the positive peak of the presynaptic spike to the onset of the fields provides an estimate of the synaptic delay and the values obtained ranged from 0.2 to 0.4 ms for the positive fields and 0.2 to 0.5 for the negative fields (mean for total sample = 0.33 ms; S.D. = 0.11; n = 12). Both sets of values suggest that the axons of interneurones travel directly to the contralateral motor nucleus where they then make synaptic connexions. Presynaptic spikes were obtained when averaging at a single point in the motor nucleus from 9 of the neurones
0.0 m m
]o.s v
lmv 0.2ram
~
~
0.4ram
/
0.6mm
]0.5/~V "
i
4ms
i
~
i
]lmV
J
1ms
Fig. 2. Variation in the extracellular responses generated at different depths in the motor nucleus by a single interneurone (same as in Fig. 1A). The left panel shows the unitary responses (2868-5776 sweeps used to construct averages) and the right panel the masseter-evoked antidromic field at the same depths (stimulus intensity of 3 x T for each, stimulus polarity reversed for response at 0.6 mm). Note that a presynaptic spike is seen at all depths but a clear unitary field is seen only at the point of maximum antidromic field (0.4 mm).
130 which did not give extracellular fields. The conduction time for these presynaptic spikes ranged from 0.1 to 0.3 ms and so suggests that they were directly conducted to the motor nucleus. The absence of a field after these spikes could indicate that the axons terminated elsewhere in the nucleus or were simply passing through the nucleus on their way elsewhere. We routinely averaged up to 1000 sweeps but occasionally up to 5000 were needed to produce a clear response and so it is also possible that we may have missed some of the weaker projections by not averaging enough sweeps. We recorded the fields generated at different depths in the motor nucleus for 5 neurones and found these to be of maximal amplitude near the point of maximal antidromic field (Fig. 2). Four of the neurones tested gave positive fields and one a negative field. When measured at the point of maximal antidromic field the amplitude of all the positive fields ranged from 0.3 to 2.0/~V (mean = 0.88/~V; S.D. = 0.55; n = 9) and from 0.5 to 1.7/~V (mean = 1.2/xV; n = 4) for the negative fields. Neurones giving positive fields were activated by afferent input from just one modality. This was cutaneous in 10 cases, intraoral in two and masseter muscle in one. In 5 cases the cutaneous input required was a firm pressure to the skin round the lips and in 3 a light stroking over a wider area. Neurones giving negative fields were activated by a variety of inputs ranging from a nonnoxious cutaneous input (n = 1), intraoral (n = 2), cutaneous and intraoral (n = 1) and masseter and cutaneous (n = 1). Four of the 9 neurones giving only presynaptic spikes were activated by cutaneous input alone (in one case involving a noxious pinch), one by intraoral input, another by input from the masseter muscle, two by both cutaneous and intraoral input and one by a combination of all 3 peripheral inputs. Thirty-six of the remaining 69 neurones that did not give either fields or
presynaptic spikes were activated by cutaneous input alone (8 requiring a noxious pinch), 13 by intraoral input, 3 by input from the masseter muscle and the remaining 17 neurones by a combination of 2 of these 3 inputs. The contralateral projection of interneurones differs from the ipsilateral one both as regards the relative proportion of positive and negative fields detected and in the amplitude of those fields. Positive fields were rare in the ipsilateral motor nucleus and accounted for only 4 of the 50 fields detected there 2 whereas they were the predominant type of field in the contralateral nucleus. Negative fields represent an excitatory projection TM but the positive fields may represent either an inhibitory input or outward current from remote excitation. Significantly more sweeps were required to reveal a contralateral projection than an ipsilateral one. For example between 50 and 100 sweeps were all that were required to reveal a projection of interneurones to the ipsilateral motor nucleus 2 whereas 1000 were routinely required to reveal a contralateral projection. The amplitude of the contralateral negative fields were towards the lower end of the range obtained ipsilaterally (range = 0.4-10.8 ~V; mean = 3.19; S.D. = 2.13; n = 46; ref 2). The smaller field amplitudes recorded contralaterally could imply that less current is injected into the contralateral masseter motoneurone pool, perhaps because fewer boutons are involved in the projection. Alternatively the fields could be smaller because there is more variability in transmission of synaptic effects contralaterally. This could result from an insecurity in conduction of activity to the synaptic terminals in the contralateral nucleus or else greater variability in release of transmitter in response to each impulse. We can not distinguish between these possibilities but our data does point to potential differences in organisation of synaptic connexions to the two motor nuclei.
1 Appenteng, K., Conyers, L., Curtis, J.C. and Moore, J.A., Mapping the monosynaptic connexions of identified trigeminal interneurones in anaesthetised rats, J. Physiol (Lond.), 416 (1989) 4P. 2 Appenteng, K., Conyers, L. and Moore, J.A., The monosynaptic excitatory connexions of single trigeminal interneurones to the v motor nucleus of the rat, J, Physiol. (Lond.), 417 (1989) 91-104. 3 Appenteng, K., Donga, R. and Williams, R.G., Morphological and electrophysiological determination of the central projections of jaw-elevator muscle spindle afferents, J. Physiol. (Lond.), 369 (1985) 93-113. 4 Goidberg, L.J. and Nakamura, Y., Lingually induced inhibition of masseteric motoneurones, Experientia, 24 (1968) 371-373. 5 Harrison, P.J. and Zytnicki, D., Crossed actions of group I muscle afferents in the cat, J. Physiol. (Loud.), 356 (1984) 263-273. 6 Kidokoro, Y., Kubota, K., Shuto, S. and Sumino, R., Reflex organisation of cat masticatory muscles, J. Neurophysiol., 31
(1968) 695-708. 7 Landgren, S., Olsson, K.A. and Westberg, K.G., Bulbar neurones with axonal projections to the trigeminal motor nucleus in the cat, Exp. Brain Res., 65 (1986) 98-111. 8 Mizuno, N., Yasui, Y., Nomura, S., Itoh, K., Konishi, A., Takada, M. and Kudo, M., A light and electron microscopic study of premotor neurones for the trigeminal motor system, J. Comp. NeuroL, 215 (1983) 290-298. 9 Nakamura, Y., Nagashima, H. and Mori, S., Bilateral effects of the afferent impulses from the masseteric muscle on the trigeminal motoneuron of the cat, Brain Res., 57 (1973) 15-27. 10 Perl, E.R., Effects of muscle stretch on excitability of contralateral motoneurons, J. Physiol. (Lond.), 145 (1959) 193-203. 11 Taylor, A., Stephens, J.A., Somjen, G., Appenteng, K. and O'Donovan, M.J., Extracellular spike-triggered averaging for plotting synaptic projections, Brain Res., 140 (1978) 344-348. 12 Travers, J.B. and Norgren, R., Afferent projections to the oral motor nuclei in the rat, J. Comp. Neurol., 220 (1983) 280-298.
