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Somatotopic organization within the brain-stem trigeminal complex of the cat
EXPERIMENTAL
NEUROLOGY
Somatotopic
2, 290-309
(1960)
Organization Within the Brain-Stem Trigeminal Complex of the Cat I. DARIAN-SMITH
Department
of Physiology,
AND
University Received
of
February
G.
Sydney,
MAYDAYS Sydney,
N.S.W.,
Australia
IS, 1960
Potentials evoked by mechanical and electrical stimulation of the skin of the cat’s face were recorded throughout the extent of the brain-stem nuclear complex of the trigeminal nerve. A synchronous presynaptic component and a negative postsynaptic component were identified in the potential evoked within the nucleus. The sites of maximal postsynaptic activity evoked by both mechanical and electrical stimulation of the same peripheral area were identical in all experiments. Along the rostrocaudal axis the presynaptic spike evoked from a fixed area of skin had a single peak of activity rostra1 to the obex. The postsynaptic negative wave, however, had two maxima along this axis, occurring in the rostra1 part of the nucleus tractus spinalis oralis and in the ‘nucleus tractus spinalis caudalis, respectively. Little or no activity was recorded in the intervening nucleus tractus spinalis interpolaris. The positions of the peaks of postsynaptic activity within the respective nuclei were dependent on the site of cutaneous stimulation. Stimulation of the ipsilateral upper or lower lip evoked maximal activity in the most rostra1 part of these two nuclei. Stimulation of the supraorbital skin evoked maximal activity 1 to 2 mm caudal to this, and stimulation of preauricular skin evoked activity still more caudally. The projection was more closely correlated with the distance of the stimulus site from the mouth, than with the division of the nerve supplying this site. On the other hand, there was dorsoventral lamination of the regions of activity within both the spinal tract and the nuclei which was closely related to the distribution of the divisions of the nerve. Stimulation of skin supplied by the ophthalmic division evoked maximal activity in the ventral third of the tract and nuclei, while stimulation of skin supplied by the mandibular division evoked maximal activity in the most dorsal third of these structures. Introduction
Recently Olszewski (10) and Astriim (1) have emphasized the nonuniform structure of the spinal trigeminal complex. Using cytoarchitectural 1 Aided by a grant from the National Health and Medical Research Council, Australia. Dr. Darian-Smith is a Senior Research Fellow, National Health and Medical Research Council, Australia. The authors thank Professors P. 0. Bishop and P. I. Korner for constructive criticism. 290
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criteria Olszewski divided the spinal nuclear component into three nuclei: the nucleus tractus spinalis caudalis, the nucleus tractus spinalis interpolaris, and the nucleus tractus spinalis oralis. Previous investigations of somatotopic organization within the spinal trigeminal complex have not taken into account this structural nonuniformity. While there has been general agreement concerning the representation of the face in the caudal part of the spinal nucleus (6, 9) the nature of the somatotopic organization has been incompletely defined. In the present experiments tactile representation of the face within the spinal trigeminal tract, the spinal trigeminal nuclei, and the main sensory nucleus have been investigated, using the evoked potential technique. The representation of different regions of the face within this brain-stem structure has been mapped, and this somatotopic organization related to the different structural components. A well-defined correlation between the tactile representation of the face within the spinal trigeminal complex and the structural subdivisions of the latter has been established. Methods Adult cats lightly anesthetized with intravenous sodium pentobarbital were used for all experiments. Flaxedil (4-5 mg) was given intravenously every 20 to 25 minutes and respiration maintained with a pump. Respiratory pulsation of the brain stem was reduced by decreasing the respiratory excursion, to one-third of the normal value, increasing its rate to 26 per minute and the administration of 90 per cent oxygen. Details of this procedure are described elsewhere (3 ) . The head of the animal was fixed in a stereotaxik apparatus, bilateral occipital craniotomy performed, and the dura overlying the cerebellum and brain stem removed. Removal of the dura was done after a mineral oil pool (at 38” C) had been constructed using the scalp flaps. Tungsten microelectrodes (8) with a tip diameter of 1 to 2 p and resistance to direct current of 1 to 5 megohms were used for all recording. Penetrations were made at an angle of 30” to the Horsley-Clarke vertical in order to reach the upper pons and midbrain under the sloping tentorium cerebelli. The reference lead was a flat platinum plate in close contact with the scalp flaps. Amplification was attained using a capacitycoupled amplifier with a time constant of SO msec, and responses were recorded by means of a Grass kymograph camera attached to a doublebeam oscilloscope. In all records an upward deflection indicated a negative change in potential at the electrode tip.
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The skin of the face was stimulated electrically, using a bipolar electrode (interpolar distance, 2 mm), the stimulus duration being 100 usec and the voltage 60 to 90. Also mechanical stimulation of the skin within 3 mm of the electrodes was obtained by pulsing a dynamic earphone, to the diaphragm of which was attached a short glass rod with a rounded tip about 1 mm in diameter. Axial movement of the probe when in contact with the skin was approximately 0.25 mm. The duration of the pulse was 1 msec. In each experiment the potentials evoked in the brain stem were mapped in 8 or 10 transverse planes, at l-mm intervals, with electrode penetrations at 0.7 mm intervals in the transverse plane. Records were taken at 0.25 mm intervals during each penetration. As the full recording period was 6 to 8 hours, care was taken that the animal’s condition did not deteriorate during this period. Hourly blood pressure recordings were taken. In no experiment in the present series did the mean blood pressure fall below 110 mm Hg. The mean blood pressure during the whole recording period for all experiments was 130 t 15 mm Hg. Very little change occurred during the course of the experiments. Serial paraffin sections were made of all brain stems after each experiment. The plane of section was transverse to the brain stem and inclined so as to be paralle1 to the penetrations of the electrode. Sections were cut at 20 p, and every fifth section mounted. Alternate mounted sections were stained using Einarson’s gallocyanin method (5) and Holmes’ silver stain for the impregnation of axons (7)) respectively. Standard statistical methods have been used in the analysis of data (11). Relevant mean values are expressed together with the standard deviation. Results
In the first series of experiments the site of peripheral stimulation was always the same, namely the ipsilateral upper lip. The patterns of the potentials evoked by both electrical and mechanical stimulation of the skin were investigated in a series of paralIe1 planes, 1 mm apart, throughout the rostrocaudal extent of the trigeminal nuclear complex. Potentials Evoked Within the Trigeminal NmEear Complex. The wave form of the potentials evoked within the trigeminal nuclear complex by electrical stimulation of the skin was essentially unchanged at various levels within the brain stem. It consisted of a synchronous diphasic, or sometimes triphasic, initially positive presynaptic component followed by
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a postsynaptic negative wave lasting several milliseconds. The presynaptic nature of the early spike sequence was demonstrated by the fact that it was unaffected by repetitive stimulation at a frequency of 7.50 to 1000 per second, whereas the late negative wave was very much depressed by such stimuli. Further, the early spike sequence was relatively insensitive to anoxia, or a marked reduction in blood pressure, while the negative wave was eliminated in such circumstances. The potential evoked within the nuclear complex by mechanical stimulation was less well defined, because a less synchronous and more complex afferent volley was initiated at the site of stimulation. Temporal dispersion of the volley arriving in the brain stem resulted in a poorly defined presynaptic complex, although this could usually be recognized. Further, the postsynaptic component was smaller in amplitude and of longer duration. In spite of these differences in the potentials evoked by electrical and mechanical stimulation of the skin, the amplitudes of the postsynaptic components in the present experiments ran parallel, the recording site of the maximal responses always coinciding. This relationship between the potentials evoked by the two forms of stimulation in a single penetration are illustrated in Fig. 1. For the electrical stimulation the intensity used was only sufficient to activate the rapidly conducting fibers (3) and did not activate the smaller, slowly conducting fibers. However, mechanical stimulation of skin activated much finer fibers in addition to these large fibers ( 16). Thus the parallelism between the potential evoked by the two forms of peripheral stimulation occurred only for the rapidly conducting fibers. While both stimuli were always used in each experiment, because of the synchrony of the afferent volley evoked by electrical stimulation most of the measurements discussed in the remainder of the paper concern the latter form of stimulation and in fact give information concerning the projection of coarse tactile fibers. However information concerning the projection of the finest tactile fibers was not investigated in the present experiments. When electrical stimulation of the skin was used the action potential was directly initiated in the axon proximal to the receptor terminal; it was not initiated by activation of the receptor (3). Late&es of PBotentials Evoked by Electrical Stim2ation of tke Skin. The latencies of the components of the evoked potential varied slightly in each experiment, owing to differences in the lengths of the peripheral conducting pathway, but changes within each animal were quite uniform.
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Potentials evoked by electrical stimulation of the ipsilateral upper lip were recorded throughout the greater part of the nuclear complex. The latencies of both the pre- and postsynaptic components of this potential were significantly longer in the caudal part of the spinal nucleus than in the region of the main sensory nucleus. This rostrocaudal increase in
FIG. 1. Close correspondence between amplitudes of postsynaptic potentials evoked within n. tractus spinalis caudalis, when the same region of skin was stimulated electrically (closed circles) and also mechanically (open circles). Ordinate is amplitude of wave expressed as percentage of maximal amplitude recorded. Negative potentials are plotted above and positive potentials below x-axis. Abscissa is stereotaxic reading along axis of electrode penetration. Inset on left indicates actual position of electrode within nucleus.
latency was not graded but occurred fairly abruptly over a distance of about 2 mm in the region of the obex. Anterior and posterior to this transition region the latencies were constant. These latency changes, observed in a single experiment, are illustrated in Fig. 2. The latencies of the onset and the peak of the negative portion of the presynaptic complex, and the latency of the peak of the postsynaptic negative wave are shown. .The onset of the negativity of the presynaptic spike approximated to the average arrival time of the action potentials of the presynaptic fibers. In addition to an increase in latency, caudal to the obex
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there was also an increased temporal dispersion of the components of the evoked potential. In Table 1 the values of latencies in all experiments in which the ipsilateral upper lip was stimulated are summarized. Estimated conduction velocities are also stated. No allowance was made for delay in the initiation of propagated action potentials at the stimulus site.
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-6
-8
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FIG. 2. Graph indicating latency changes of components of potentials evoked in trigeminal nuclear complex on stimulating ipsilateral upper lip electrically. Ordinate, latency in msec; abscissa, stereotaxic plane in mm; level of obex is indicated. Presynaptic complex: half closed circles, latency of onset of negativity; closed circles, Postsynaptic complex: open circles, latency of latency of peak of negative spike. peak of negative wave. TABLE 1 LATENCIES OF COMPONENTS OF THE EVOKED POTENTIAL IN DIFFERENT REGIONS OF THE TRIGEMINAL NUCLEAR COMPLEX, AND ESTIMATED CONDUCTION VELOCITIES ALONG THE PRESYNAPTIC PATHWAY Recording Parameter
Number of experiments
Latency of presynaptic spike Onset of negativity Peak of negative spike Latency Peak Mean
of postsynaptic wave of negative wave conduction
a N.V.Sp.0. b N.V.Sp.C.
velocity = nucleus = nucleus
N.V.Sp.0.a (msec)
N.V.Sp.C.” (msec)
7 7
1.00 & 0.15 1.15 + 0.15
1.50 If: 0.15 1.80 & 0.15
7
1.90 f
2.75 -c 0.35
2 tractus tractus
spinalis spinalis
Site
oralis (10). caudalis.
0.15
73 m/set
48 m/set
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Similar abrupt changes in the latencies of the components of the evoked potentials were observed on stimulating all other cutaneous regions of the face investigated. Pattern of Evoked Potentials in a Transverse Plane. Figure 3 illustrates the evoked potentials recorded with a series of penetrations in a
FIG. 3. Evoked entry of sensory lateral upper lip. are shown.
potentials recorded in a plane of penetrations just trigeminal root into pons. Site of electrical stimulation Position of spinal tract is indicated. Time and voltage
caudal to was ipsicalibration
plane just caudal to the entry of the sensory root of the trigeminal. This plane passed through the nucleus tractus spinalis oralis. Again the site of cutaneous electrical stimulation was the ipsilateral upper lip. The amplitude of the negative spike of the presynaptic component was maximal within the middle part of the spinal tract, and that of the negative postsynaptic component within the nucleus. However, both components were recorded with diminished amplitude over a much wider area. Much of this extension resulted from field spread, as is evident with the medial
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recording of the presynaptic component, and the dorsal and lateral recording of the negative postsynaptic wave. However, ventral and medial to the nucleus a sharp reversal of the polarity of the recorded postsynaptic potential was regularly recorded. Thus the activated neural elements within the nucleus were not randomly arranged but were sufficiently oriented for the source of current flowing into the region of depolarized elements to be evident in field records. In this region which acted as a source of current the outflow of axons of second order trigeminal neurons was readily identified in silver impregnated sections. The evoked field potentials observed in a transverse plane through the nucleus tractus spinalis caudalis differed in latency, as already described, but the pattern of these potentials was similar to that observed more rostrally. However, one difference observed was that in this plane the current source extended somewhat more laterally below the nucleus probably indicating rotation of the outflow of axons which now sweep somewhat more ventrally before passing medially to join the medial lemniscus on the opposite side of the brain stem. Again this fiber pathway is recognized in silver stained sections at this level of the brain stem. Changes in Amplitude of Evoked Potential Along Rostrocaudul Axis. In each experiment the limits of the trigeminal complex were investigated by recording the potentials evoked in 8 or 10 planes at l-mm intervals. By plotting the maximal amplitudes of the pre- and postsynaptic components of the evoked potential observed in each plane, the distribution and extent of activity in this axis were determined. In Fig. 4 the maximum amplitude of the negative spike in the presynaptic component has been plotted for successive planes in a series of experiments, the ipsilateral upper lip being the stimulus site. The anatomical levels of the penetrating planes were determined by serial section of the brain stem which was essential in order to compare different experiments. The maximal amplitude in each plane of this presynaptic component was uniformly recorded just caudal to the level of entry of the sensory root and fell off gradually in both the rostra1 and caudal directions. Similar estimates of the amplitude of the postsynaptic negative wave along the rostrocaudal axis were made. In Fig. 5 the maximum amplitude of this wave in each plane has been plotted against its anatomical position within the brain stem for five experiments. The distribution contrasted sharply with that of the presynaptic component. The graph illustrates that within the trigeminal nuclear complex a maximal nuclear response occurred just posterior to the trigeminal motor nucleus. More
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posteriorly in the region of the obex there was a marked reduction in amplitude of the nuclear response. Caudal to the obex at the rostra1 end of the pyramidal decussation, however, a second region of marked nuclear activity was recorded. The observed reduction in nuclear activity in the region of the obex
FIG. 4. Graph illustrating rostrocaudal extent of tract activity. Ordinate shows amplitude of presynaptic negative spike expressed as percentage of maximum value recorded in the experiment. At each level the maximum presynaptic response recorded in that plane is plotted. Abscissa shows anatomical level of successive penetrations. Results were obtained from five separate experiments, the electrical stimulus site being the ipsilateral upper lip.
was not an artifact. The order of examining successive planes was deliberately made random in all experiments to avoid any gradual changes in the recorded activity of successive rostrocaudal planes ‘which might occur with time. In spite of this, the bimodal activity was observed in Further it was observed in the distribution of all ten experiments. activity for all four peripheral points stimulated although the plane of minimum activity depended entirely on the peripheral site stimulated. Within a given experiment the planes of minimum activity for the two peripheral regions stimulated, usually differed by as much as 2 mm or more. The pre- and postsynaptic components of the evoked potential were differentially affected, the presynaptic component having a quite large amplitude when the postsynaptic component was minimal. This is seen on comparing Figs. 4 and 5. Finally the potentials evoked in the two regions of increased activity differed, as has been previously men-
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tioned; latencies of both pre- and postsynaptic components were constant within the limits of either the anterior or posterior nuclear region, but in the caudal region all latencies were significantly greater, as is shown in Table 1. The two regions of maximal activity were found to occur within particular components of the nuclear complex. The peak of the rostra1 region of activity occurred within the nucleus tractus spinalis oralis (10, 13), and extended into the posterior region of the main sensory nucleus. The peak of the caudal activity in all experiments fell within the nucleus
0 LiiEEkN t
OBEX
’
I
FIG. 5. Graph illustrating rostrocaudal extent of nuclear activity recorded on five cats. Stimulus (electrical) site was the ipsilateral upper lip. Ordinate shows amplitude of postsynaptic negative wave expressed as a percentage of maximum value recorded in experiment. Within each transverse plane, amplitude of maximum response in that plane has been plotted. Abscissa shows rostrocaudal anatomical level of recording. The bimodal distribution of activity is illustrated. Traces above the graph are typical records obtained in the two regions of activity.
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tractus spinalis caudalis and the intervening low amplitude segment was in the nucleus tractus spinalis interpolaris. When the peripheral stimulus was mechanical, nuclear evoked activity was more restricted than was observed with electrical stimulation. Evoked activity occurred in the region of the peak observed with electrical stimulation, the two regions being quite separated and no activity being recorded in the nucleus tractus spinalis interpolaris. Somdotopk Arrangement Within the Spinal Tract. Similar patterns of activity within the brain stem were observed on stimulating skin areas other than the ipsilateral upper lip. Rostrocaudal latency changes were similar, the rostrocaudal change in the amplitude of the negative presynaptic spike was unimodal, and two regions of increased nuclear activity were observed within the nucleus tractus spinalis oralis and nucleus tractus spinalis caudalis respectively. However, the regions of maximal activity within these subnuclei depended on the stimulus site. In these experiments the projections of two peripheral regions of the face were always simultaneously mapped. In all, four peripheral regions were investigated, these being shown in Fig. 6. By suitable pairing of the cutaneous regions stimulated in the six animals used, three full maps for each point were obtained, each of which was paired with the map from one of the three other points. This comparison of projection patterns within animals was essential as the differences in the patterns was not large and could have been obscured by small errors in localization of recording sites in different experiments. At all levels in the spinal tract there was a dorsoventral somatotopic lamination, Fibers of the ophthalmic division were localized in the most ventral part of the tract, those from the maxillary division were largely distributed in the middle third of the tract and fibers of the mandibular division were largely within the dorsal part of the tract. Considerable overlap of recorded activity occurred as is seen in Fig. 6, but the regions of maximum activity always retained this relationship. In this figure, the results obtained in four experiments in a penetration of the spinal tract in a plane just rostra1 to the entry of the glossopharyngeal nerve into the brain stem are illustrated. In experiments B, C, and D, the region of activity on stimulating the upper lip is shown to be constant; the relation of the activity induced on stimulating the other regions is demonstrated by comparison with this common region of activity. The rostrocaudal extension of this presynaptic activity was not correlated with the divisional lamination of the tract. Thus the most caudal
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activity recorded in the first cervical segment occurred on stimulating the preauricular region, situated within the cutaneous distribution of the mandibular division of the trigeminal nerve. Stimulation of the supraorbital region evoked activity extending to the caudal extent of the pyramidal decussation and stimulation of the perioral region evoked presynaptic activity extending to the rostra1 limit of the pyramidal decussation. Somatotop’c Ovganiz’ation Within the Trigeminal Nuclear Complex. Along the rostrocaudal axis all four peripheral points stimulated had a bimodal representation within the trigeminal nuclear complex. One peak of activity was always recorded rostra1 to the obex within the
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I 4
I
3I
1
I 2
1
I I
,
4 0
FIG. 6. Distribution of presynaptic activity along a dorsoventral penetration of of electrode penetration is shown spinal tract for different stimulus sites. Position in left upper corner. The inset illustrates four ipsilateral regions stimulated electrically. In the graphs, ordinate shows amplitude of presynaptic negative spike in mv, plotted against abscissa, the recording site within the tract in mm along electrode path. In each graph the potentials evoked from two peripheral regions have been plotted.
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nucleus tractus spinalis oralis, or the caudal part of the main sensory nucleus and the second posteriorly within the nucleus tractus spinalis caudalis. This representation and its extent is best shown in Figs. 7, 8, and 9, in which the activity on stimulating pairs of peripheral points
FIG. 7. Graphs illustrating relation of rostrocaudal extent of activity evoked on stimulating two separate peripheral cutaneous regions. Stimulus sites were ipsilateral upper lip (closed circles) and supraorbital skin (open circles), respectively. Upper graph, distribution of nuclear graph, distribution of presynaptic activity ; lower activity. Abscissa is stereotaxic plane of penetration, inset illustrating this on the brain stem. Ordinates are amplitudes of pre- and postsynaptic negative components in mv, respectively. In both regions of increased nuclear activity, the peak for the supraorbital site was more posterior than that evoked by stimulating the upper lip.
have been plotted. The maximal amplitudes and both pre- and postsynaptic potentials evoked on stimulating the different peripheral points (with equal stimulus intensities) was related to the stimulus site, being greatest when the perioral region was stimulated, somewhat less for the supraorbital region, and quite small for the preauricular region. These differences probably reflected the density of fibers projecting from the stimulus site to the nucleus. From the figures it is seenthe relations of regions of maximum evoked activity for the different peripheral points was similar in both nucleus tractus spinalis oralis and nucleus tractus spinalis caudalis. The two
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perioral sites were represented within the nuclei at the same rostrocaudal levels. Both peaks of activity for the supraorbital stimulus site were caudal to those for the perioral region and the preauricular projection was still further caudal. Finally there was a well-defined pattern of representation of these peripheral points within transverse stereotaxic planes in the regions of activity. The arrangement in both regions was similar as is illustrated
FIG. 8. Graphs similar to Fig. 7, illustrating relation of rostrocaudal extent of evoked activity within trigeminal complex, on stimulating skin of ipsilateral lower lip (closed circles) and supraorbital regions (open circles), respectively.
in Figs. 10 and 11. In these figures two transverse planes are considered, one passing through the nucleus tractus spinalis oralis and the second through the nucleus tractus spinalis caudalis. Because of the rostrocaudal separation of peaks of activity, the peak of activity for one of the stimulus sites only in any combination is represented. In both planes it is seen that maximal nuclear activity was evoked by stimulation of the ipsilateral lower lip more dorsally and medially than that evoked by stimulation of the upper lip. Similarly it was shown that the peak of activity ventral
evoked by stimulation of the supraorbital region was lateral and to that evoked from the upper lip; and finally that the peak of
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activity evoked from the preauricular region was dorsal and lateral to the upper lip representation. Figure 12 summarizes some of these relations. It illustrates the rostrocaudal and mediolateral relations of the regions to which the four peripheral points projected. In addition there was a dorsoventral lamination, essentially according to peripheral divisions, as in the spina tract, The mandibular projection was most dorsal and the ophthalmic division most ventral.
FIG. 9. Graphs sirnilalto Fig. 7, illustrating relation of rostrocaudal extent of evoked activity within trigeminal complex, on stimulating skin of ipsilateral upper lip (closed circles) and preauricular regions (open circles). While amplitudes of potentials evoked on stimuIating preauricular region were small, peaks of activity were readiIy measured. At stereotaxic plane -6, no evoked nuclear activity was recorded. The two peaks of nuclear activity evoked by stimulating preauricular skin were well posterior to those of activity evoked on stimulating upper lip.
In all experiments the peak of nuclear activity evoked by tactile stimulation of the skin coincided with the peaks of nuclear activity by electrical stimulation of the skin. Discussion
Representation of Single Cutaneous Facial Region Within Trigeminal
Cmnplex. The findings in the present experiments of a dual tactile repre-
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sentation within the brain-stem trigeminal complex may be adequately explained in terms of the known structural organization. Windle (15) demonstrated a deep nonbifurcating bundle of finer fibers in the descending tract. Sjijqvist (12) by analyzing the fiber spectrum at different levels in the tract, demonstrated that most of the coarse superficial fibers terminate rostra1 to the obex and that the fine deeper fibers extend down into the cervical cord. This has been confirmed recently by Astrom (1)
FIG. 10. Graphs indicating amplitude of postsynaptic wave along three penetrations through n. tractus spinalis oralis, scale along abscissa and along inset of brain stem corresponding. Negative potentials plotted above baseline of each. Potentials evoked on stimulating upper lip (closed circles) and lower lip (open circles). Maximum negative potential on stimulating lower lip was dorsomedial to that evoked on stimulating upper lip. Sharp reversal of sign of potential ventromedially for both peripheral stimulus sites is also seen.
in the mouse. These two fiber bundles would provide the anatomical basis for the present observations concerning the functional discontinuity in the region of the obex. The abrupt increase in the latency of the presynaptic complex posterior to the obex may be accounted for by this reduction in the predominant fiber diameter of the spinal tract at this level. The two separate regions of nuclear activity evoked by tactile or electrical stimulation of a peripheral cutaneous area appear to have been mediated by these separate presynaptic pathways. That these two regions
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of activity occurred within the nucleus tractus spinalis caudalis and nucleus tractus spinalis oralis respectively, supports Olszewski’s suggestion that the spinal trigeminal complex is not a functional unit, but rather that three functional units, corresponding to the anatomical subdivisions, are included within it. The secondary trigeminal pathways arising from these separate nuclear regions and activated by tactile stimulation were
FIG. 11. Graphs indicating amplitude of postsynaptic wave along four penetrations through n. tractus spinalis caudalis, on stimulating electrically the ipsilateral upper (closed circles) and lower lips (open circles), respectively.
not investigated in the present experiments. However, the termination of most of these secondary fibers in the ventrobasal thalamic complex has been demonstrated by both histological methods (12, 13, 14) and electrophysiological methods (2, 9). It is probable that the region of nuclear activity evoked in the rostra1 part of the nuclear complex is homologous to the medial lemniscal projection, and the caudal region to the spinothalamic relay in the dorsal horn of the spinal cord. However, the active component corresponding to that observed in the external cuneate nucleus (spinocerebellar relay) has not been identified within the trigeminal complex.
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Somatotofk Organization Within Trigemid Complex. There has been general agreement in the previous anatomical and electrophysiological investigations concerning the dorsoventral representation of the peripheral divisions in the spinal tract nuclei of the trigeminal nerve. The present experiments confirmed this lamination throughout the length of the complex, with the mandibular division being dorsal, the ophthalmic division ventral, and the maxillary division between these. Tactile representation of the face along the rostrocaudal axis of the complex, however, has not been clearly defined. Most recent work (6, 9)
FIG. 12. Dorsal view of right half of cat’s brain stem, illustrating somatotopic organization of trigeminal complex. The regions of maximal nuclear activity, rostra1 and caudal to the obex, are shown for four ipsilateral sites of mechanical (and electrical) stimulation of skin. Stimulus sites are shown in inset, Fig. 6. Abbreviations: C, cuneate nucleus; C,, first cervical nerve; G, gracile nucleus; Inf Coll, inferior colliculus; IX, glossopharyngeal nerve. Sites x, n, o, and s indicate upper lip, lower lip, supraorbital region, and cheek.
has been concentrated on determining the caudal extent of activity evoked by stimulation of different regions of the face. Using this criterion, McKinley and Magoun (9) and Harrison and Corbin (6) suggested a divisional representation, the ophthalmic division projecting most caudally and the mandibular division rostrally within the spinal trigeminal complex. The present experiments do not support this view, since, while stimulation of skin in the supraorbital region did evoke maximal activity posterior to that evoked by stimulation of the upper and lower lips, the activity evoked by stimulation of skin in the preauricular area (mandibular division) was the most caudally recorded. Thus the restrocaudal projection of the regions of the face investigated in the present experiments correlates best with the distance of the site of stimulation from the oral cavity. Dejerine
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(4) has previously suggestedsuch a somatotopic organization of the spinal trigeminal complex. The somatotopic organization of the second, rostra1 region of nuclear activity has not been previously investigated, but the present observations suggestan arrangement identical to that observed in the nucleus tractus spinalis caudalis. One problem which arises from the present findings concerns the main sensory nucleus. In our experiments, no peripheral stimulus site has its peak of evoked nuclear activity rostra1 to the caudal limit of the motor nucleus. However, the activity evoked usually extended well into the main sensory nucleus. The junction of the nucleus tractus spinalis oralis and the main sensory nucleus is difficult to define in the cat, but it would appear that if these peaks of activity did fall within the main sensory nucleus it was only in the most caudal part. It seemsprobable that intraoral structures innervated by the trigeminal nerve have their rostra1 representation more anteriorly within the main sensory nucleus.
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3. 4. 5. 6. 7. 8. 9. 10. 11.
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References .&STRBM, K. E., On the central course of afferent fibers in the trigeminal, facial, glossopharyngeal and vagal nerves and their nuclei in the mouse. Acta pkysiol. stand., suppl. 106: 209-320, 195’2. BERRY, C. M., F. D. ANDERSON,and D. C. BROOKS, Ascending pathways of the trigeminal nerve in the cat. J. Neurophysiol. 19: 144-153, 1956. DARIAN-SM~ITR, I., Activity of single neurones in the main sensory nucleus of the cat’s trigeminal nerve elicited by graded peripheral stimulation. J. Physiol., Lond. (in press) 1960. DEJI~~NE, J., “Semiologie des affections due systeme nerveux.” Paris, Masson et Cie., pp. 836-839, 1914. EINARSON, L. A method for progressive selective staining of Nissl and nuclear substances in nerve cells. Am. J. Path. 8: 295-307, 1932. HARRISON,F., and C. B. CORBIN, Oscillographic studies on the spinal tract of the fifth cranial nerve. J. Neurophysiol. 5: 465-482, 1942. HOLMES, W., “Recent advances in clinical pathology.” Pp. 404405, S. C. Dyke, Ed., London. J. & A. Churchill, 1947. Hunu, D. H., Tungsten micro-electrodes for recording from single units. Science, 125: 549-550, 1957. MCKINLEY, W. A., and H. W. MAGOWN, The bulbar projection of the trigeminal nerve. Am. J. Physiol. 197: 217-224, 1942. OLSZEWSKI, J., On the anatomical and functional organization of the spinal trigeminal nucleus. J. Camp. New. 92: 401-413, 1950. QUENOUILLE, M. H., “Associated Measurements.” London, Butterworth, 1952. SJBQVIST, O., Studies on pain conduction in the trigeminal nerve. Acta psych&. new. stand., suppl. 17: l-139, 1938.
TRIGEMINAL
13.
TORVIK,
J. Anat. 14. 1.5.
16.
A., The 100:
ascending 1-13,
fibers
from
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the main
trigeminal
sensory
nucleus.
Am.
1957.
A. E., The origin, of the trigeminal nerve in WINDLE, W. F., Non-bifurcating New. 40: 229-240, 1926. ZOTTEPMAN, Y., Touch, pain cutaneous sensory nerves.
WALKER,
SOMATOTOPIC
course and terminations of the secondary primates. J. Comp. New. 71: 59-89, 1939. nerve fibers of the trigeminal nerve. and tickling: an electrophysiological J. Physiol., Land. 96: l-28, 1939.
pathways J. Camp.
investigation
on
NEUROLOGY
Somatotopic
2, 290-309
(1960)
Organization Within the Brain-Stem Trigeminal Complex of the Cat I. DARIAN-SMITH
Department
of Physiology,
AND
University Received
of
February
G.
Sydney,
MAYDAYS Sydney,
N.S.W.,
Australia
IS, 1960
Potentials evoked by mechanical and electrical stimulation of the skin of the cat’s face were recorded throughout the extent of the brain-stem nuclear complex of the trigeminal nerve. A synchronous presynaptic component and a negative postsynaptic component were identified in the potential evoked within the nucleus. The sites of maximal postsynaptic activity evoked by both mechanical and electrical stimulation of the same peripheral area were identical in all experiments. Along the rostrocaudal axis the presynaptic spike evoked from a fixed area of skin had a single peak of activity rostra1 to the obex. The postsynaptic negative wave, however, had two maxima along this axis, occurring in the rostra1 part of the nucleus tractus spinalis oralis and in the ‘nucleus tractus spinalis caudalis, respectively. Little or no activity was recorded in the intervening nucleus tractus spinalis interpolaris. The positions of the peaks of postsynaptic activity within the respective nuclei were dependent on the site of cutaneous stimulation. Stimulation of the ipsilateral upper or lower lip evoked maximal activity in the most rostra1 part of these two nuclei. Stimulation of the supraorbital skin evoked maximal activity 1 to 2 mm caudal to this, and stimulation of preauricular skin evoked activity still more caudally. The projection was more closely correlated with the distance of the stimulus site from the mouth, than with the division of the nerve supplying this site. On the other hand, there was dorsoventral lamination of the regions of activity within both the spinal tract and the nuclei which was closely related to the distribution of the divisions of the nerve. Stimulation of skin supplied by the ophthalmic division evoked maximal activity in the ventral third of the tract and nuclei, while stimulation of skin supplied by the mandibular division evoked maximal activity in the most dorsal third of these structures. Introduction
Recently Olszewski (10) and Astriim (1) have emphasized the nonuniform structure of the spinal trigeminal complex. Using cytoarchitectural 1 Aided by a grant from the National Health and Medical Research Council, Australia. Dr. Darian-Smith is a Senior Research Fellow, National Health and Medical Research Council, Australia. The authors thank Professors P. 0. Bishop and P. I. Korner for constructive criticism. 290
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criteria Olszewski divided the spinal nuclear component into three nuclei: the nucleus tractus spinalis caudalis, the nucleus tractus spinalis interpolaris, and the nucleus tractus spinalis oralis. Previous investigations of somatotopic organization within the spinal trigeminal complex have not taken into account this structural nonuniformity. While there has been general agreement concerning the representation of the face in the caudal part of the spinal nucleus (6, 9) the nature of the somatotopic organization has been incompletely defined. In the present experiments tactile representation of the face within the spinal trigeminal tract, the spinal trigeminal nuclei, and the main sensory nucleus have been investigated, using the evoked potential technique. The representation of different regions of the face within this brain-stem structure has been mapped, and this somatotopic organization related to the different structural components. A well-defined correlation between the tactile representation of the face within the spinal trigeminal complex and the structural subdivisions of the latter has been established. Methods Adult cats lightly anesthetized with intravenous sodium pentobarbital were used for all experiments. Flaxedil (4-5 mg) was given intravenously every 20 to 25 minutes and respiration maintained with a pump. Respiratory pulsation of the brain stem was reduced by decreasing the respiratory excursion, to one-third of the normal value, increasing its rate to 26 per minute and the administration of 90 per cent oxygen. Details of this procedure are described elsewhere (3 ) . The head of the animal was fixed in a stereotaxik apparatus, bilateral occipital craniotomy performed, and the dura overlying the cerebellum and brain stem removed. Removal of the dura was done after a mineral oil pool (at 38” C) had been constructed using the scalp flaps. Tungsten microelectrodes (8) with a tip diameter of 1 to 2 p and resistance to direct current of 1 to 5 megohms were used for all recording. Penetrations were made at an angle of 30” to the Horsley-Clarke vertical in order to reach the upper pons and midbrain under the sloping tentorium cerebelli. The reference lead was a flat platinum plate in close contact with the scalp flaps. Amplification was attained using a capacitycoupled amplifier with a time constant of SO msec, and responses were recorded by means of a Grass kymograph camera attached to a doublebeam oscilloscope. In all records an upward deflection indicated a negative change in potential at the electrode tip.
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The skin of the face was stimulated electrically, using a bipolar electrode (interpolar distance, 2 mm), the stimulus duration being 100 usec and the voltage 60 to 90. Also mechanical stimulation of the skin within 3 mm of the electrodes was obtained by pulsing a dynamic earphone, to the diaphragm of which was attached a short glass rod with a rounded tip about 1 mm in diameter. Axial movement of the probe when in contact with the skin was approximately 0.25 mm. The duration of the pulse was 1 msec. In each experiment the potentials evoked in the brain stem were mapped in 8 or 10 transverse planes, at l-mm intervals, with electrode penetrations at 0.7 mm intervals in the transverse plane. Records were taken at 0.25 mm intervals during each penetration. As the full recording period was 6 to 8 hours, care was taken that the animal’s condition did not deteriorate during this period. Hourly blood pressure recordings were taken. In no experiment in the present series did the mean blood pressure fall below 110 mm Hg. The mean blood pressure during the whole recording period for all experiments was 130 t 15 mm Hg. Very little change occurred during the course of the experiments. Serial paraffin sections were made of all brain stems after each experiment. The plane of section was transverse to the brain stem and inclined so as to be paralle1 to the penetrations of the electrode. Sections were cut at 20 p, and every fifth section mounted. Alternate mounted sections were stained using Einarson’s gallocyanin method (5) and Holmes’ silver stain for the impregnation of axons (7)) respectively. Standard statistical methods have been used in the analysis of data (11). Relevant mean values are expressed together with the standard deviation. Results
In the first series of experiments the site of peripheral stimulation was always the same, namely the ipsilateral upper lip. The patterns of the potentials evoked by both electrical and mechanical stimulation of the skin were investigated in a series of paralIe1 planes, 1 mm apart, throughout the rostrocaudal extent of the trigeminal nuclear complex. Potentials Evoked Within the Trigeminal NmEear Complex. The wave form of the potentials evoked within the trigeminal nuclear complex by electrical stimulation of the skin was essentially unchanged at various levels within the brain stem. It consisted of a synchronous diphasic, or sometimes triphasic, initially positive presynaptic component followed by
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a postsynaptic negative wave lasting several milliseconds. The presynaptic nature of the early spike sequence was demonstrated by the fact that it was unaffected by repetitive stimulation at a frequency of 7.50 to 1000 per second, whereas the late negative wave was very much depressed by such stimuli. Further, the early spike sequence was relatively insensitive to anoxia, or a marked reduction in blood pressure, while the negative wave was eliminated in such circumstances. The potential evoked within the nuclear complex by mechanical stimulation was less well defined, because a less synchronous and more complex afferent volley was initiated at the site of stimulation. Temporal dispersion of the volley arriving in the brain stem resulted in a poorly defined presynaptic complex, although this could usually be recognized. Further, the postsynaptic component was smaller in amplitude and of longer duration. In spite of these differences in the potentials evoked by electrical and mechanical stimulation of the skin, the amplitudes of the postsynaptic components in the present experiments ran parallel, the recording site of the maximal responses always coinciding. This relationship between the potentials evoked by the two forms of stimulation in a single penetration are illustrated in Fig. 1. For the electrical stimulation the intensity used was only sufficient to activate the rapidly conducting fibers (3) and did not activate the smaller, slowly conducting fibers. However, mechanical stimulation of skin activated much finer fibers in addition to these large fibers ( 16). Thus the parallelism between the potential evoked by the two forms of peripheral stimulation occurred only for the rapidly conducting fibers. While both stimuli were always used in each experiment, because of the synchrony of the afferent volley evoked by electrical stimulation most of the measurements discussed in the remainder of the paper concern the latter form of stimulation and in fact give information concerning the projection of coarse tactile fibers. However information concerning the projection of the finest tactile fibers was not investigated in the present experiments. When electrical stimulation of the skin was used the action potential was directly initiated in the axon proximal to the receptor terminal; it was not initiated by activation of the receptor (3). Late&es of PBotentials Evoked by Electrical Stim2ation of tke Skin. The latencies of the components of the evoked potential varied slightly in each experiment, owing to differences in the lengths of the peripheral conducting pathway, but changes within each animal were quite uniform.
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Potentials evoked by electrical stimulation of the ipsilateral upper lip were recorded throughout the greater part of the nuclear complex. The latencies of both the pre- and postsynaptic components of this potential were significantly longer in the caudal part of the spinal nucleus than in the region of the main sensory nucleus. This rostrocaudal increase in
FIG. 1. Close correspondence between amplitudes of postsynaptic potentials evoked within n. tractus spinalis caudalis, when the same region of skin was stimulated electrically (closed circles) and also mechanically (open circles). Ordinate is amplitude of wave expressed as percentage of maximal amplitude recorded. Negative potentials are plotted above and positive potentials below x-axis. Abscissa is stereotaxic reading along axis of electrode penetration. Inset on left indicates actual position of electrode within nucleus.
latency was not graded but occurred fairly abruptly over a distance of about 2 mm in the region of the obex. Anterior and posterior to this transition region the latencies were constant. These latency changes, observed in a single experiment, are illustrated in Fig. 2. The latencies of the onset and the peak of the negative portion of the presynaptic complex, and the latency of the peak of the postsynaptic negative wave are shown. .The onset of the negativity of the presynaptic spike approximated to the average arrival time of the action potentials of the presynaptic fibers. In addition to an increase in latency, caudal to the obex
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there was also an increased temporal dispersion of the components of the evoked potential. In Table 1 the values of latencies in all experiments in which the ipsilateral upper lip was stimulated are summarized. Estimated conduction velocities are also stated. No allowance was made for delay in the initiation of propagated action potentials at the stimulus site.
o---o--+--o--+-4’ 1.5: ,
=
=
l
=-=*s
2
I
=
=
=
=
4-y
0
-I
-2
-3
-4
-6
-8
-10
FIG. 2. Graph indicating latency changes of components of potentials evoked in trigeminal nuclear complex on stimulating ipsilateral upper lip electrically. Ordinate, latency in msec; abscissa, stereotaxic plane in mm; level of obex is indicated. Presynaptic complex: half closed circles, latency of onset of negativity; closed circles, Postsynaptic complex: open circles, latency of latency of peak of negative spike. peak of negative wave. TABLE 1 LATENCIES OF COMPONENTS OF THE EVOKED POTENTIAL IN DIFFERENT REGIONS OF THE TRIGEMINAL NUCLEAR COMPLEX, AND ESTIMATED CONDUCTION VELOCITIES ALONG THE PRESYNAPTIC PATHWAY Recording Parameter
Number of experiments
Latency of presynaptic spike Onset of negativity Peak of negative spike Latency Peak Mean
of postsynaptic wave of negative wave conduction
a N.V.Sp.0. b N.V.Sp.C.
velocity = nucleus = nucleus
N.V.Sp.0.a (msec)
N.V.Sp.C.” (msec)
7 7
1.00 & 0.15 1.15 + 0.15
1.50 If: 0.15 1.80 & 0.15
7
1.90 f
2.75 -c 0.35
2 tractus tractus
spinalis spinalis
Site
oralis (10). caudalis.
0.15
73 m/set
48 m/set
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Similar abrupt changes in the latencies of the components of the evoked potentials were observed on stimulating all other cutaneous regions of the face investigated. Pattern of Evoked Potentials in a Transverse Plane. Figure 3 illustrates the evoked potentials recorded with a series of penetrations in a
FIG. 3. Evoked entry of sensory lateral upper lip. are shown.
potentials recorded in a plane of penetrations just trigeminal root into pons. Site of electrical stimulation Position of spinal tract is indicated. Time and voltage
caudal to was ipsicalibration
plane just caudal to the entry of the sensory root of the trigeminal. This plane passed through the nucleus tractus spinalis oralis. Again the site of cutaneous electrical stimulation was the ipsilateral upper lip. The amplitude of the negative spike of the presynaptic component was maximal within the middle part of the spinal tract, and that of the negative postsynaptic component within the nucleus. However, both components were recorded with diminished amplitude over a much wider area. Much of this extension resulted from field spread, as is evident with the medial
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recording of the presynaptic component, and the dorsal and lateral recording of the negative postsynaptic wave. However, ventral and medial to the nucleus a sharp reversal of the polarity of the recorded postsynaptic potential was regularly recorded. Thus the activated neural elements within the nucleus were not randomly arranged but were sufficiently oriented for the source of current flowing into the region of depolarized elements to be evident in field records. In this region which acted as a source of current the outflow of axons of second order trigeminal neurons was readily identified in silver impregnated sections. The evoked field potentials observed in a transverse plane through the nucleus tractus spinalis caudalis differed in latency, as already described, but the pattern of these potentials was similar to that observed more rostrally. However, one difference observed was that in this plane the current source extended somewhat more laterally below the nucleus probably indicating rotation of the outflow of axons which now sweep somewhat more ventrally before passing medially to join the medial lemniscus on the opposite side of the brain stem. Again this fiber pathway is recognized in silver stained sections at this level of the brain stem. Changes in Amplitude of Evoked Potential Along Rostrocaudul Axis. In each experiment the limits of the trigeminal complex were investigated by recording the potentials evoked in 8 or 10 planes at l-mm intervals. By plotting the maximal amplitudes of the pre- and postsynaptic components of the evoked potential observed in each plane, the distribution and extent of activity in this axis were determined. In Fig. 4 the maximum amplitude of the negative spike in the presynaptic component has been plotted for successive planes in a series of experiments, the ipsilateral upper lip being the stimulus site. The anatomical levels of the penetrating planes were determined by serial section of the brain stem which was essential in order to compare different experiments. The maximal amplitude in each plane of this presynaptic component was uniformly recorded just caudal to the level of entry of the sensory root and fell off gradually in both the rostra1 and caudal directions. Similar estimates of the amplitude of the postsynaptic negative wave along the rostrocaudal axis were made. In Fig. 5 the maximum amplitude of this wave in each plane has been plotted against its anatomical position within the brain stem for five experiments. The distribution contrasted sharply with that of the presynaptic component. The graph illustrates that within the trigeminal nuclear complex a maximal nuclear response occurred just posterior to the trigeminal motor nucleus. More
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posteriorly in the region of the obex there was a marked reduction in amplitude of the nuclear response. Caudal to the obex at the rostra1 end of the pyramidal decussation, however, a second region of marked nuclear activity was recorded. The observed reduction in nuclear activity in the region of the obex
FIG. 4. Graph illustrating rostrocaudal extent of tract activity. Ordinate shows amplitude of presynaptic negative spike expressed as percentage of maximum value recorded in the experiment. At each level the maximum presynaptic response recorded in that plane is plotted. Abscissa shows anatomical level of successive penetrations. Results were obtained from five separate experiments, the electrical stimulus site being the ipsilateral upper lip.
was not an artifact. The order of examining successive planes was deliberately made random in all experiments to avoid any gradual changes in the recorded activity of successive rostrocaudal planes ‘which might occur with time. In spite of this, the bimodal activity was observed in Further it was observed in the distribution of all ten experiments. activity for all four peripheral points stimulated although the plane of minimum activity depended entirely on the peripheral site stimulated. Within a given experiment the planes of minimum activity for the two peripheral regions stimulated, usually differed by as much as 2 mm or more. The pre- and postsynaptic components of the evoked potential were differentially affected, the presynaptic component having a quite large amplitude when the postsynaptic component was minimal. This is seen on comparing Figs. 4 and 5. Finally the potentials evoked in the two regions of increased activity differed, as has been previously men-
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tioned; latencies of both pre- and postsynaptic components were constant within the limits of either the anterior or posterior nuclear region, but in the caudal region all latencies were significantly greater, as is shown in Table 1. The two regions of maximal activity were found to occur within particular components of the nuclear complex. The peak of the rostra1 region of activity occurred within the nucleus tractus spinalis oralis (10, 13), and extended into the posterior region of the main sensory nucleus. The peak of the caudal activity in all experiments fell within the nucleus
0 LiiEEkN t
OBEX
’
I
FIG. 5. Graph illustrating rostrocaudal extent of nuclear activity recorded on five cats. Stimulus (electrical) site was the ipsilateral upper lip. Ordinate shows amplitude of postsynaptic negative wave expressed as a percentage of maximum value recorded in experiment. Within each transverse plane, amplitude of maximum response in that plane has been plotted. Abscissa shows rostrocaudal anatomical level of recording. The bimodal distribution of activity is illustrated. Traces above the graph are typical records obtained in the two regions of activity.
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tractus spinalis caudalis and the intervening low amplitude segment was in the nucleus tractus spinalis interpolaris. When the peripheral stimulus was mechanical, nuclear evoked activity was more restricted than was observed with electrical stimulation. Evoked activity occurred in the region of the peak observed with electrical stimulation, the two regions being quite separated and no activity being recorded in the nucleus tractus spinalis interpolaris. Somdotopk Arrangement Within the Spinal Tract. Similar patterns of activity within the brain stem were observed on stimulating skin areas other than the ipsilateral upper lip. Rostrocaudal latency changes were similar, the rostrocaudal change in the amplitude of the negative presynaptic spike was unimodal, and two regions of increased nuclear activity were observed within the nucleus tractus spinalis oralis and nucleus tractus spinalis caudalis respectively. However, the regions of maximal activity within these subnuclei depended on the stimulus site. In these experiments the projections of two peripheral regions of the face were always simultaneously mapped. In all, four peripheral regions were investigated, these being shown in Fig. 6. By suitable pairing of the cutaneous regions stimulated in the six animals used, three full maps for each point were obtained, each of which was paired with the map from one of the three other points. This comparison of projection patterns within animals was essential as the differences in the patterns was not large and could have been obscured by small errors in localization of recording sites in different experiments. At all levels in the spinal tract there was a dorsoventral somatotopic lamination, Fibers of the ophthalmic division were localized in the most ventral part of the tract, those from the maxillary division were largely distributed in the middle third of the tract and fibers of the mandibular division were largely within the dorsal part of the tract. Considerable overlap of recorded activity occurred as is seen in Fig. 6, but the regions of maximum activity always retained this relationship. In this figure, the results obtained in four experiments in a penetration of the spinal tract in a plane just rostra1 to the entry of the glossopharyngeal nerve into the brain stem are illustrated. In experiments B, C, and D, the region of activity on stimulating the upper lip is shown to be constant; the relation of the activity induced on stimulating the other regions is demonstrated by comparison with this common region of activity. The rostrocaudal extension of this presynaptic activity was not correlated with the divisional lamination of the tract. Thus the most caudal
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activity recorded in the first cervical segment occurred on stimulating the preauricular region, situated within the cutaneous distribution of the mandibular division of the trigeminal nerve. Stimulation of the supraorbital region evoked activity extending to the caudal extent of the pyramidal decussation and stimulation of the perioral region evoked presynaptic activity extending to the rostra1 limit of the pyramidal decussation. Somatotop’c Ovganiz’ation Within the Trigeminal Nuclear Complex. Along the rostrocaudal axis all four peripheral points stimulated had a bimodal representation within the trigeminal nuclear complex. One peak of activity was always recorded rostra1 to the obex within the
\
lDt 51
I
I 4
I
3I
1
I 2
1
I I
,
4 0
FIG. 6. Distribution of presynaptic activity along a dorsoventral penetration of of electrode penetration is shown spinal tract for different stimulus sites. Position in left upper corner. The inset illustrates four ipsilateral regions stimulated electrically. In the graphs, ordinate shows amplitude of presynaptic negative spike in mv, plotted against abscissa, the recording site within the tract in mm along electrode path. In each graph the potentials evoked from two peripheral regions have been plotted.
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nucleus tractus spinalis oralis, or the caudal part of the main sensory nucleus and the second posteriorly within the nucleus tractus spinalis caudalis. This representation and its extent is best shown in Figs. 7, 8, and 9, in which the activity on stimulating pairs of peripheral points
FIG. 7. Graphs illustrating relation of rostrocaudal extent of activity evoked on stimulating two separate peripheral cutaneous regions. Stimulus sites were ipsilateral upper lip (closed circles) and supraorbital skin (open circles), respectively. Upper graph, distribution of nuclear graph, distribution of presynaptic activity ; lower activity. Abscissa is stereotaxic plane of penetration, inset illustrating this on the brain stem. Ordinates are amplitudes of pre- and postsynaptic negative components in mv, respectively. In both regions of increased nuclear activity, the peak for the supraorbital site was more posterior than that evoked by stimulating the upper lip.
have been plotted. The maximal amplitudes and both pre- and postsynaptic potentials evoked on stimulating the different peripheral points (with equal stimulus intensities) was related to the stimulus site, being greatest when the perioral region was stimulated, somewhat less for the supraorbital region, and quite small for the preauricular region. These differences probably reflected the density of fibers projecting from the stimulus site to the nucleus. From the figures it is seenthe relations of regions of maximum evoked activity for the different peripheral points was similar in both nucleus tractus spinalis oralis and nucleus tractus spinalis caudalis. The two
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perioral sites were represented within the nuclei at the same rostrocaudal levels. Both peaks of activity for the supraorbital stimulus site were caudal to those for the perioral region and the preauricular projection was still further caudal. Finally there was a well-defined pattern of representation of these peripheral points within transverse stereotaxic planes in the regions of activity. The arrangement in both regions was similar as is illustrated
FIG. 8. Graphs similar to Fig. 7, illustrating relation of rostrocaudal extent of evoked activity within trigeminal complex, on stimulating skin of ipsilateral lower lip (closed circles) and supraorbital regions (open circles), respectively.
in Figs. 10 and 11. In these figures two transverse planes are considered, one passing through the nucleus tractus spinalis oralis and the second through the nucleus tractus spinalis caudalis. Because of the rostrocaudal separation of peaks of activity, the peak of activity for one of the stimulus sites only in any combination is represented. In both planes it is seen that maximal nuclear activity was evoked by stimulation of the ipsilateral lower lip more dorsally and medially than that evoked by stimulation of the upper lip. Similarly it was shown that the peak of activity ventral
evoked by stimulation of the supraorbital region was lateral and to that evoked from the upper lip; and finally that the peak of
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activity evoked from the preauricular region was dorsal and lateral to the upper lip representation. Figure 12 summarizes some of these relations. It illustrates the rostrocaudal and mediolateral relations of the regions to which the four peripheral points projected. In addition there was a dorsoventral lamination, essentially according to peripheral divisions, as in the spina tract, The mandibular projection was most dorsal and the ophthalmic division most ventral.
FIG. 9. Graphs sirnilalto Fig. 7, illustrating relation of rostrocaudal extent of evoked activity within trigeminal complex, on stimulating skin of ipsilateral upper lip (closed circles) and preauricular regions (open circles). While amplitudes of potentials evoked on stimuIating preauricular region were small, peaks of activity were readiIy measured. At stereotaxic plane -6, no evoked nuclear activity was recorded. The two peaks of nuclear activity evoked by stimulating preauricular skin were well posterior to those of activity evoked on stimulating upper lip.
In all experiments the peak of nuclear activity evoked by tactile stimulation of the skin coincided with the peaks of nuclear activity by electrical stimulation of the skin. Discussion
Representation of Single Cutaneous Facial Region Within Trigeminal
Cmnplex. The findings in the present experiments of a dual tactile repre-
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sentation within the brain-stem trigeminal complex may be adequately explained in terms of the known structural organization. Windle (15) demonstrated a deep nonbifurcating bundle of finer fibers in the descending tract. Sjijqvist (12) by analyzing the fiber spectrum at different levels in the tract, demonstrated that most of the coarse superficial fibers terminate rostra1 to the obex and that the fine deeper fibers extend down into the cervical cord. This has been confirmed recently by Astrom (1)
FIG. 10. Graphs indicating amplitude of postsynaptic wave along three penetrations through n. tractus spinalis oralis, scale along abscissa and along inset of brain stem corresponding. Negative potentials plotted above baseline of each. Potentials evoked on stimulating upper lip (closed circles) and lower lip (open circles). Maximum negative potential on stimulating lower lip was dorsomedial to that evoked on stimulating upper lip. Sharp reversal of sign of potential ventromedially for both peripheral stimulus sites is also seen.
in the mouse. These two fiber bundles would provide the anatomical basis for the present observations concerning the functional discontinuity in the region of the obex. The abrupt increase in the latency of the presynaptic complex posterior to the obex may be accounted for by this reduction in the predominant fiber diameter of the spinal tract at this level. The two separate regions of nuclear activity evoked by tactile or electrical stimulation of a peripheral cutaneous area appear to have been mediated by these separate presynaptic pathways. That these two regions
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of activity occurred within the nucleus tractus spinalis caudalis and nucleus tractus spinalis oralis respectively, supports Olszewski’s suggestion that the spinal trigeminal complex is not a functional unit, but rather that three functional units, corresponding to the anatomical subdivisions, are included within it. The secondary trigeminal pathways arising from these separate nuclear regions and activated by tactile stimulation were
FIG. 11. Graphs indicating amplitude of postsynaptic wave along four penetrations through n. tractus spinalis caudalis, on stimulating electrically the ipsilateral upper (closed circles) and lower lips (open circles), respectively.
not investigated in the present experiments. However, the termination of most of these secondary fibers in the ventrobasal thalamic complex has been demonstrated by both histological methods (12, 13, 14) and electrophysiological methods (2, 9). It is probable that the region of nuclear activity evoked in the rostra1 part of the nuclear complex is homologous to the medial lemniscal projection, and the caudal region to the spinothalamic relay in the dorsal horn of the spinal cord. However, the active component corresponding to that observed in the external cuneate nucleus (spinocerebellar relay) has not been identified within the trigeminal complex.
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Somatotofk Organization Within Trigemid Complex. There has been general agreement in the previous anatomical and electrophysiological investigations concerning the dorsoventral representation of the peripheral divisions in the spinal tract nuclei of the trigeminal nerve. The present experiments confirmed this lamination throughout the length of the complex, with the mandibular division being dorsal, the ophthalmic division ventral, and the maxillary division between these. Tactile representation of the face along the rostrocaudal axis of the complex, however, has not been clearly defined. Most recent work (6, 9)
FIG. 12. Dorsal view of right half of cat’s brain stem, illustrating somatotopic organization of trigeminal complex. The regions of maximal nuclear activity, rostra1 and caudal to the obex, are shown for four ipsilateral sites of mechanical (and electrical) stimulation of skin. Stimulus sites are shown in inset, Fig. 6. Abbreviations: C, cuneate nucleus; C,, first cervical nerve; G, gracile nucleus; Inf Coll, inferior colliculus; IX, glossopharyngeal nerve. Sites x, n, o, and s indicate upper lip, lower lip, supraorbital region, and cheek.
has been concentrated on determining the caudal extent of activity evoked by stimulation of different regions of the face. Using this criterion, McKinley and Magoun (9) and Harrison and Corbin (6) suggested a divisional representation, the ophthalmic division projecting most caudally and the mandibular division rostrally within the spinal trigeminal complex. The present experiments do not support this view, since, while stimulation of skin in the supraorbital region did evoke maximal activity posterior to that evoked by stimulation of the upper and lower lips, the activity evoked by stimulation of skin in the preauricular area (mandibular division) was the most caudally recorded. Thus the restrocaudal projection of the regions of the face investigated in the present experiments correlates best with the distance of the site of stimulation from the oral cavity. Dejerine
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(4) has previously suggestedsuch a somatotopic organization of the spinal trigeminal complex. The somatotopic organization of the second, rostra1 region of nuclear activity has not been previously investigated, but the present observations suggestan arrangement identical to that observed in the nucleus tractus spinalis caudalis. One problem which arises from the present findings concerns the main sensory nucleus. In our experiments, no peripheral stimulus site has its peak of evoked nuclear activity rostra1 to the caudal limit of the motor nucleus. However, the activity evoked usually extended well into the main sensory nucleus. The junction of the nucleus tractus spinalis oralis and the main sensory nucleus is difficult to define in the cat, but it would appear that if these peaks of activity did fall within the main sensory nucleus it was only in the most caudal part. It seemsprobable that intraoral structures innervated by the trigeminal nerve have their rostra1 representation more anteriorly within the main sensory nucleus.
1.
2.
3. 4. 5. 6. 7. 8. 9. 10. 11.
12.
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