Brainstem Exclusive of the Pyramids Themselves, Which Were Blood-Supplied Through the Intact Basilar Artery

NOTE ON CONVERGENCE OF PYRAMIDAL AND PRIMARY AFFERENT IMPULSES IN THE SPINAL CORD OF THE CAT BY DAVID P. C. LLOYD THE ROCKEFELLER UNIVERSITY Communicated December 20, 1967 The burden of this note is to present an example of observations long since made but not previously published. The immediate stimulus for presenting them now was provided by the paper by R. Porter' in which a combination of impulses of cortical and of lingual nerve origin was shown by convergence to facilitate the response of interneurons in or near the spinal trigeminal nucleus to a level of activity greater than that of the sum of responses elicited by lingual nerve stimulation and corticospinal stimulation, respectively, in isolation. Experiments of the sort now to be described concern the convergence upon interneurons in the lumbar spinal enlargement of pyramidal tract impulses and primary afferent impulses engendered by stimulation of the seventh lumbar dorsal root. To an ex- tent these experiments are confirmatory, with respect to another location in the neuraxis, of the observations of Porter,' but they demonstrate, in addition, how one pathway by occlusion may pre-empt the interneuron from service to the other pathway. In a prior paper2 convergence at the internuncial level was im- plied by virtue of pyramidal tract facilitatory influence upon disynaptic (three- neuron-arc) reflexes in the absence of any influence upon monosynaptic (two- neuron-arc) reflexes (ref. 2, Figs. 9 and 10). Preparation and procedure were discussed in the previous publication2 and need not be restated here, except to note that the pyramidal tract impulses were "pure" because the bulbar pyramid was stimulated rostral to a lesion that sev- ered the entire brainstem exclusive of the pyramids themselves, which were blood-supplied through the intact basilar artery. Figure 1 exemplifies in a longitudinal section the sort of lesion made by a guillotine contraption. A trans- verse section through a similar lesion was depicted in Figure 1 of the previous ac- count of pyramidal activity.2 The present illustration has the advantage of showing in part the track made by the stimulating electrodes rostral to the lesion, and the level of complete transection rostral to the site of stimulation. Observations roughly comparable to some of those herein discussed have been made by Lundberg, Norrsell, and Voorhoeve3 with the exception inter alia that they stimulated the sensorimotor cortex, as did Porter.' Such stimulation gives rise to repetitive responses in the pyramidal system.4-7 Also, a single cortical stimulus evokes a blaze of activity among the cells of the reticular formation which may project to the spinal cord.4'8 Hence the importance of severing the brainstem (except for the pyramids) caudal to the site of stimulation, whether this be cortical or pyramidal, is re-emphasized. Also, if a single pyramidal volley is desired, the pyramid itself must be stimulated following complete severance of the brainstem above the site of stimulation to prevent reverberation and repetitive discharge consequent to antidromic conduction to the cortex (unlikely6), or to activation of juxtaposed corticopetal systems, viz., medial lemniscus 381 Downloaded by guest on September 27, 2021 382 PHYSIOLOGY: D. P. C. LLOYD PROC. N. A. S. FIG. 1.-Cut face of the (sagitally cut) brainstem and upper spinal cord of gross specimen from the cat. The specimen was removed at the end of the experiment, fixed, and then rapidly surface-stained, washed, and blotted before longitudinal division. The oblique rostral (right) end of the specimen defines the preexperimental complete section of the neuraxis rostral to the site of stimulation. To the left of that section a dark line extending vertically downwards from the floor of the fourth ventricle shows part of the track of the stimulating electrodes and defines their rostrocaudal location. The bared tips of the electrodes embraced the pyramidal fibers at the ventral surface. Next, further to the left, is seen the pyramidal tract-sparing lesion, made prior to experimentation, extending ventrally from the floor of the-fourth ventricle so that the pyramidal tract at the ventral surface is the only re- maining connection between the parts of the specimen (compare with Fig. 1, ref. 2). The extreme left end of the specimen was determined by postmortem severance of the spinal cord. The basilar artery supplying the pyramids was stripped away prior to staining. (likely6). One may suppose, however, as an alternative, that decortication, in combination with the pyramid-sparing lesion caudal to the site of stimulation, would serve the latter purpose while permitting stimulation, if so desired, sub- cortically.6 Figure 2 A-D presents records of the responses of an interneuron located at the base of the dorsal horn of the grey substance in the seventh lumbar segment. Record 2A contains the triple response of the interneuron to a series of nine stimuli to the bulbar pyramids. The smaller deflections are the recorded stimulus artifacts; the larger (ca. 2 mv in amplitude), the responses of the interneuron. In record 2B the same interneuron is seen to respond thrice, at rela- tively high frequency, to a volley of impulses engendered in the seventh lumbar dorsal root. To obtain record 2C, the dorsal root and pyramidal tract stimuli were combined in the exact time relationship, each to the other, as obtained in records 2A and B. The three internuncial discharges characteristic of response by this neuron to the dorsal root stimulation take place as did they in Figure 2B, but response to the series of pyramidal volleys has been occluded by the sequelae of dorsal root stimulation. When the dorsal root stimulation is shifted in time relative to the pyramidal tract stimulation, as in Figure 2D, so that the impingement upon the interneuron of impulses generated as a consequence of dorsal root stimulation falls during the peak of excitation mediated through the pyramidal system, a sharp burst of responses (four) at very high frequency occurs as a result of excitatory convergence. In Figure 2D, the first of the responses expected to result from the fact of pyramidal tract stimulation occurs at its appropriate time, in the circumstance, prior to the dorsal root stimulation (compare the initial discharge in records 2A and 2D). The recordings in Figure 2 lead to discourse on several aspects of internuncial activity not altogether novel, but nonetheless worthy of statement in brief. Downloaded by guest on September 27, 2021 VOL. 59, 1968 PHYSIOLOGY: D. P. C. LLOYD 383 (1) Direct evidence is presented in place of inference2 concerning convergent impingement upon spinal interneurons of activity engendered by pyramidal (sensu strict.) and primary afferent impulses. (2) The results of this and of a former paper2 are consistent with the view expressed by Porter' that convergence (i.e., the site of integration) between FIG. 2.-Responses of an interneuron situated at the base of the dorsal horn in the seventh lumbar segment of the spinal cord elicited by: (A) Nine stimuli to the bulbar pyramid. (B) Single stimulus to the seventh lumbar dorsal root (the initial triphasic response denotes the primary afferent volley ini- tiated by such stimulation). (C and D) Combined stimulation of pyramidal tract and dorsal root at two different time relations one to the other. corticospinal and reflex systems (in the cat!) is at the internuncial level rather than at the motoneuron (final common path). (3) The responses depicted in Figure 2 are typical of a variety of interneurons in that they can respond repetitively, at a high frequency, for a shorter or longer period of time, to a given excitatory input without evidence of inter- current depression only to become immediately thereafter unresponsive. This is putative evidence for occlusion presumably through operation of the subnormal process. (4) Since, in record 2C, the interneuron, having fired to the dorsal root stimulation, will not continue to fire in response to the pyramidal impulses, there is indication that failure to continue responding for an additional period of time (as in Fig. 2B) to impulse impingement of dorsal root origin alone is not merely the result of waning afferent impulse excitation. In the circumstance the response of the interneuron should be considered a self-limiting process. In other words the cause, with respect to this interneuron and by reason of simi- larity of behavior to many other interneurons, is considered to be postsynaptic rather than presynaptic. (5) To invoke inhibition as a participant in the foregoing result is unnecessary and would be lavish use of hypothesis. (6) Finally, concerning occlusion, as herein defined by example, one is at liberty to speculate that it is merely an inconsequential consequence of massive synchronous stimulation, rather than a salient aspect of normal integrative activity. This is neither to deny utility for purpose of analysis of neuronal activity nor, in fact, to deny its existence as a manifestation of normal integrative mechanism in action. Downloaded by guest on September 27, 2021 384 PHYSIOLOGY: D. P. C. LLOYD PROC. N. A. S. ' Porter, R., "Cortical actions on hypoglossal motoneurones in cats: A proposed role for a common internuncial cell," J. Physiol., 193, 295-308 (1967). 2 Lloyd, D. P. C., "The spinal mechanism of the pyramidal system in cats," J. Neurophysiol., 4, 525-546 (1941). 3 Lundberg, A., V. Norrsell, and P. Voorhoeve, "Pyramidal effects on lumbosacral inter- neurones activated by somatic afferents," Acta Physiol. Scand., 56, 220-229 (1962). 4Lloyd, D. P. C., unpublished observations (1940). 6 Patton, H. D., and V. E. Amassian, "Single and multiple unit analysis of cortical stage of pyramidal tract activation," J. Neurophysiol., 17, 345-363 (1954). 6 Patton, H. D., and V. E. Amassian, "The pyramidal tract: its excitation and functions," in Handbook of Physiology-Neurophysiology, ed.

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