Summary
Previous studies in the rat have demonstrated that corresponding peripheral tactile and somatosensory cortical inputs converge within the granule cell layer of various cerebellar lobules and further that descending corticopontine projections from the forelimb sensory cortex (FLSCx) partially overlap with the projection zones of ascending basilar pontine afferents from nucleus cuneatus (NC). The present study employed anatomical and electrophysiological procedures to determine whether cortical and dorsal column nuclear afferent projections converge on pontine neurons that, in turn, provide mossy fiber input to the granule cell layer of the paramedian lobule (PML), i. e., that portion of the rodent cerebellum shown to receive forelimb peripheral inputs. The combination of the orthograde and retrograde axonal transport of horseradish peroxidase (HRP) conjugated to wheat germ agglutinin (WGA) was used light microscopically to demonstrate that orthogradely labeled projections from injections of the FLSCx and NC converged with ponto-paramedian projection neurons that were retrogradely labeled from injections of the PML. These studies were also repeated in conjunction with ablations of either the FLSCx or NC which resulted in the ultrastructural identification of degenerating, as well as WGA-HRP labeled axonal boutons of these pontine afferent projections thus confirming that such projections actually formed synaptic contacts with the retrogradely labeled pontoparamedian projection neurons. Single unit recording analyses of neurons in the ventromedial region of the basilar pons following combined electrical stimulation of various regions of the sensorimotor cortex and the contralateral body surface indicated that approximately 40% of all cells recorded responded to electrical stimulation of corresponding regions of the cortex and periphery, particularly the FLSCx and the forepaw. Natural cutaneous stimuli applied to the forepaw that also elicited responses in these same groups of basilar pontine neurons and were associated with relatively small receptive fields. Taken together, these observations indicate that the previously observed convergence of peripheral and somatosensory cortical inputs within the granule cell layer of the cerebellar cortex may be at least partially organized at the level of the basilar pons.
Similar content being viewed by others
References
Allen GI, Tsukahara N (1974) Cerebrocerebellar communication systems. Physiol Rev 54: 957–1006
Asanuma H, Arnold AP (1975) Noxious effects of excessive currents used for intracortical microstimulation. Brain Res 96: 103–107
Bower JM, Beerman DH, Gibson JM, Shambes GM, Welker W (1981) Principles of organization of a cerebro-cerebellar circuit. Micromapping the projections from cerebral (SI) to cerebellar (granule cell layer) tactile areas of rats. Brain Behav Evol 18: 1–18
Burne RA, Eriksson MA, Saint-Cyr JA, Woodward DJ (1978) The organization of the pontine projection to lateral cerebellar areas in the rat: dual zones in the pons. Brain Res 139: 340–347
Donoghue JP, Kerman KL, Ebner FF (1979) Evidence for two organizational plans within the somatic sensory-motor cortex of the rat. J Comp Neurol 183: 647–664
Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212: 76–88
Dykes RW, Rasmusson DD, Sretavan D, Rehman NB (1982) Submodality segregation and receptive-field sequences in cuneate, gracile, and external cuneate nuclei of the cat. J Neurophysiol 47: 389–416
Enger M, Brodal P (1985) Organization of corticopontocerebellar connections to the paramedian lobule in the cat. Anat Embryol 172: 227–238
Feldman SG, Kruger L (1980) An axonal transport study of the ascending projection of medial lemniscal neurons in the rat. J Comp Neurol 192: 427–454
Fink RP, Heimer L (1967) Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res 4: 369–374
Hall RD, Lindholm EP (1974) Organization of motor and somatosensory neocortex in the albino rat. Brain Res 66: 23–38
Joseph JW, Shambes GM, Gibson JM, Welker W (1978) Tactile projections to granule cells in caudal vermis of the rat's cerebellum. Brain Behav Evol 15: 141–149
Kassel J, Shambes GM, Welker W (1984) Fractured cutaneous projections to the granule cell layer of the posterior cerebellar hemisphere of the domestic cat. J Comp Neurol 225: 458–468
Kosinski RJ, Azizi SA, Border BG, Mihailoff GA (1986a) Origin and ultrastructural identification of dorsal column nuclear synaptic terminals in the basilar pontine gray of rats. J Comp Neurol 253: 92–104
Kosinski RJ, Azizi SA, Mihailoff GA (1986b) Anatomical and electrophysiological evidence for the convergence of somatosensory cortical and peripheral inputs onto components of the pontocerebellar system in the rat. Neurosci Abstr 26: S344
Kosinski RJ, Neafsey EJ, Castro AJ (1986c) A comparative topographical analysis of dorsal column nuclear and cerebral cortical projections to the basilar pontine gray in rats. J Comp Neurol 244: 163–173
Kosinski RJ, Mihailoff GA (1988) A double retrograde fluorescent tracing of dorsal column nuclear projections to the basilar pontine nuclei, thalamus, and superior colliculus in the rat. Neurosci Lett 85: 40–46
Lund RD, Webster KE (1967) Thalamic afferents from the dorsal column nuclei: an experimental anatomical study in the rat. J Comp Neurol 130: 301–212
Massopust LC, Hauge DH, Ferneding JC, Doubek WG, Taylor JJ (1985) Projection systems and terminal localization of dorsal column afferents: an autoradiographic and horseradish peroxidase study in the rat. J Comp Neurol 237: 533–544
Mihailoff GA, McArdle CB (1981) The cytoarchitecture, cytology and synaptic organization of the basilar pontine nuclei in the rat. II. Electron microscopic studies. J Comp Neurol 195: 203–219
Mihailoff GA, Burne RA, Azizi SA, Norell G, Woodward DJ (1981a) The pontocerebellar system in the rat: an HRP study. II. Hemispheral components. J Comp Neurol 197: 559–557
Mihailoff GA, McArdle CB, Adams CE (1981b) The cytoarchitecture, cytology and synaptic organization of the basilar pontine nuclei in the rat. I. Nissl and Golgi studies. J Comp Neurol 195: 181–201
Mihailoff GA, Watt CB, Burne RA (1981c) Evidence suggesting that both the corticopontine and cerebellopontine systems are each composed of two separate neuronal populations: an electron microscopic and horseradish peroxidase study in the rat. J Comp Neurol 197: 221–242
Neafsey EJ, Sievert C (1982) A second forelimb motor area exists in rat frontal cortex. Brain Res 232: 151–156
Peschanski M, Ralston HJ (1985) Light and electron microscopic evidence of transneuronal labeling with WGA-HRP to trace somatosensory pathways to the thalamus. J Comp Neurol 236: 29–41
Potter RF, Ruegg DG, Wiesendanger M (1978) Responses of neurons of the pontine nuclei to stimulation of the sensorimotor, visual and auditory cortex of rats. Brain Res Bull 3: 15–19
Ramón y Cajal S (1909) Histologie du system nerveux de l'homme et des vertebres, Vol 1. Maloine, Paris
Ruegg DJ, Seguin JJ, Wiesendanger M (1977) Effects of electrical stimulation of somatosensory and motor areas of the cerebral cortex on neurones of the pontine nuclei in squirrel monkeys. Neuroscience 2: 923–927
Ruegg DJ, Wiesendanger M (1975) Corticofugal effects from sensorimotor area I and somatosensory area II on neurones of the pontine nuclei in the cat. J Physiol (Lond) 247: 745–757
Rye DB, Saper CB, Wainer BH (1984) Stabilization of the tetramethylbenzidine (TMB) reaction product: application for retrograde and anterograde tracing and combination with immunohistochemistry. J Histochem Cytochem 32: 1145–1153
Shambes GM, Gibson JM, Welker W (1978) Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behav Evol 15: 94–140
Spreafico R, De Biasi S, Frassomi C, Battoglea G (1985) Transneuronal transport of wheatgerm agglutinin conjugated with horseradish peroxidase in the somatosensory system of the rat: a light and electron microscopic study. Somatosens Res 2: 119–137
Swenson RS, Kosinski RJ, Castro AJ (1984) Topography of spinal, dorsal column nuclear and spinal trigeminal projections to the pontine gray in rats. J Comp Neurol 222: 301–311
Welker W, Shambes GM (1985) Tactile cutaneous representation in cerebellar granule cell layer of opossum, Didelphis virginiana. Brain Behav Evol 27: 57–79
Wise SP, Jones EG (1977) Calls of origin and terminal distribution of descending projections of the rat somatic sensory cortex. J Comp Neurol 175: 129–158
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kosinski, R.J., Azizi, S.A. & Mihailoff, G.A. Convergence of cortico- and cuneopontine projections onto components of the pontocerebellar system in the rat: an anatomical and electrophysiological study. Exp Brain Res 71, 541–556 (1988). https://doi.org/10.1007/BF00248746
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00248746