Propriospinal afferent and efferent connections of the lateral and medial areas of the dorsal horn (laminae I‐IV) in the rat lumbar spinal cord

The different subdivisions along the mediolateral extent of the superficial dorsal horn of the spinal cord are generally regarded as identical structures that execute the function of sensory information processing without any significant communication with other regions of the spinal gray matter. In contrast to this standing, here we endeavor to show that neural assemblies along the mediolateral extent of laminae I‐IV cannot be regarded as identical structures. After injecting Phaseolus vulgaris leucoagglutinin and biotinylated dextran amine into various areas of the superficial dorsal horn (laminae I‐IV) at the level of the lumbar spinal cord in rats, we have demonstrated that the medial and lateral areas of the superficial dorsal horn show the following distinct features in their propriospinal afferent and efferent connections: 1) A 300‐ to 400‐μm‐long section of the medial aspects of laminae I‐IV projects to and receives afferent fibers from a three segment long compartment of the spinal dorsal gray matter, whereas the same length of the lateral aspects of laminae I‐IV projects to and receives afferent fibers from the entire rostrocaudal extent of the lumbar spinal cord. 2) The medial aspects of laminae I‐IV project extensively to the lateral areas of the superficial dorsal horn. In contrast to this, the lateral areas of laminae I‐IV, with the exception of a few fibers at the segmental level, do not project back to the medial territories. 3) There is a substantial direct commissural connection between the lateral aspects of laminae I‐IV on the two sides of the lumbar spinal cord. The medial part of laminae I‐IV, however, does not establish any direct connection with the gray matter on the opposite side. 4) The lateral aspects of laminae I‐IV appear to be the primary source of fibers projecting to the ipsi‐ and contralateral ventral horns and supraspinal brain centers. Projecting fibers arise from the medial subdivision of laminae I‐IV in a substantially lower number. The findings indicate that the medial and lateral areas of the superficial spinal dorsal horn of rats may play different roles in sensory information processing. J. Comp. Neurol. 422:312–325, 2000. © 2000 Wiley‐Liss, Inc.

[1]  C. Woolf,et al.  Somatotopic organization of cutaneous afferent terminals and dorsal horn neuronal receptive fields in the superficial and deep laminae of the rat lumbar spinal cord , 1986, The Journal of comparative neurology.

[2]  W. Zieglgänsberger,et al.  Sequential expression of JUN B, JUN D and FOS B proteins in rat spinal neurons: Cascade of transcriptional operations during nociception , 1991, Neuroscience Letters.

[3]  C. Heizmann,et al.  Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla , 1996, Neuroscience.

[4]  G. Grant,et al.  The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord , 1984, The Journal of comparative neurology.

[5]  Maria Fitzgerald,et al.  The contralateral input to the dorsal horn of the spinal cord in the decerebrate spinal rat , 1982, Brain Research.

[6]  K. Ren,et al.  A comparative study of the calcium-binding proteins calbindin-D28K, calretinin, calmodulin and parvalbumin in the rat spinal cord , 1994, Brain Research Reviews.

[7]  P. Mason,et al.  Neurotransmitters in nociceptive modulatory circuits. , 1991, Annual review of neuroscience.

[8]  E. Perl,et al.  Reexamination of the dorsal root projection to the spinal dorsal horn including observations on the differential termination of coarse and fine fibers , 1979, The Journal of comparative neurology.

[9]  G. Grant,et al.  Laminar distribution and somatotopic organization of primary afferent fibers from hindlimb nerves in the dorsal horn. A study by transganglionic transport of horseradish peroxidase in the rat , 1986, Neuroscience.

[10]  D. Lima,et al.  The spino-latero-reticular system of the rat: Projections from the superficial dorsal horn and structural characterization of marginal neurons involved , 1991, Neuroscience.

[11]  A. Scheibel,et al.  Terminal axonal patterns in cat spinal cord. II. The dorsal horn. , 1968, Brain research.

[12]  Y. Sugiura,et al.  Ultrastructural features of functionally identified primary afferent neurons with C (unmyelinated) fibers of the guinea pig: Classification of dorsal root ganglion cell type with reference to sensory modality , 1988, The Journal of comparative neurology.

[13]  D. A. Walsh,et al.  Monoarthritis in the rat knee induces bilateral and time-dependent changes in substance P and calcitonin gene-related peptide immunoreactivity in the spinal cord , 1993, Neuroscience.

[14]  J. Szentágothai,et al.  Distribution and Connections of Afferent Fibres in the Spinal Cord , 1973 .

[15]  D. Lima,et al.  Periterminal synaptic organization of primary afferents in laminae I and IIo of the rat spinal cord, as shown after anterograde HRP labelling , 1993, Journal of neurocytology.

[16]  D. Menétrey,et al.  Calbindin‐D28K (CaBP28k)‐like Immunoreactivity in Ascending Projections , 1992, The European journal of neuroscience.

[17]  D. Lima,et al.  Morphological types of spinomesencephalic neurons in the marginal zone (Lamina I) of the rat spinal cord, as shown after retrograde labelling with cholera toxin subunit B , 1989, The Journal of comparative neurology.

[18]  M. P. Witter,et al.  Multiple anterograde tracing, combining Phaseolus vulgaris leucoagglutinin with rhodamine- and biotin-conjugated dextran amine , 1994, Journal of Neuroscience Methods.

[19]  C J Hodge,et al.  Primate spinothalamic pathways: I. A quantitative study of the cells of origin of the spinothalamic pathway , 1989, The Journal of comparative neurology.

[20]  J. Szentágothai Neuronal and synaptic arrangement in the substantia gelatinosa rolandi , 1964, The Journal of comparative neurology.

[21]  S. Granum The spinothalamic system of the rat. I. Locations of cells of origin , 1986, The Journal of comparative neurology.

[22]  G. Grant,et al.  Cutaneous projections from the rat hindlimb foot to the substantia gelatinosa of the spinal cord studied by transganglionic transport of WGA‐HRP conjugate , 1985, The Journal of comparative neurology.

[23]  M. Zimmermann,et al.  c-JUN-like immunoreactivity in the CNS of the adult rat: Basal and transynaptically induced expression of an immediate-early gene , 1991, Neuroscience.

[24]  G. Aston-Jones,et al.  Axonal collateral-collateral transport of tract tracers in brain neurons: false anterograde labelling and useful tool , 1997, Neuroscience.

[25]  R. Traub,et al.  Unilateral hindpaw inflammation produces a bilateral increase in NADPH-diaphorase histochemical staining in the rat lumbar spinal cord , 1992, Neuroscience.

[26]  M. Ghatei,et al.  Calcitonin gene-related peptide immunoreactivity in the spinal cord of man and of eight other species , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  K. Westlund,et al.  Immunohistochemical localization of seven different peptides in the human spinal cord , 1989, The Journal of comparative neurology.

[28]  F. Wouterlood,et al.  Double-label immunocytochemistry: combination of anterograde neuroanatomical tracing with Phaseolus vulgaris leucoagglutinin and enzyme immunocytochemistry of target neurons. , 1987, Journal of Histochemistry and Cytochemistry.

[29]  M B Hancock,et al.  Visualization of peptide-immunoreactive processes on serotonin-immunoreactive cells using two-color immunoperoxidase staining. , 1984, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[30]  Y. Smith,et al.  Differential synaptic innervation of striatofugal neurones projecting to the internal or external segments of the globus pallidus by thalamic afferents in the squirrel monkey , 1996, The Journal of comparative neurology.

[31]  Edward L. White,et al.  The identification of thalamocortical axon terminals in barrels of mouse Sml cortex using immunohistochemistry of anterogradely transported lectin (Phaseolus vulgaris-leucoagglutinin) , 1985, Brain Research.

[32]  J. Szentágothai PROPRIOSPINAL PATHWAYS AND THEIR SYNAPSES. , 1964, Progress in brain research.

[33]  A I Basbaum,et al.  Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. , 1984, Annual review of neuroscience.

[34]  R. Dubner,et al.  Neurochemistry and neural circuitry in the dorsal horn. , 1986, Progress in brain research.

[35]  M. Geffard,et al.  Serotonergic innervation of the dorsal horn of rat spinal cord: light and electron microscopic immunocytochemical study , 1991, Journal of neurocytology.

[36]  Walle J. H. Nauta,et al.  Light microscopic evidence of striatal input to intrapallidal neurons of cholinergic cell group Ch4 in the rat: a study employing the anterograde tracerPhaseolus vulgaris leucoagglutinin (PHA-L) , 1986, Brain Research.

[37]  William D. Willis,et al.  The cells of origin of the primate spinothalamic tract , 1979, The Journal of comparative neurology.

[38]  P. Wall,et al.  The distribution of nine peptides in rat spinal cord with special emphasis on the substantia gelatinosa and on the area around the central canal (laminaX) , 1981, The Journal of comparative neurology.

[39]  D. Lima,et al.  The spinothalamic system of the rat: Structural types of retrogradely labelled neurons in the marginal zone (lamina I) , 1988, Neuroscience.

[40]  J. Sandkühler,et al.  Characteristics of propriospinal modulation of nociceptive lumbar spinal dorsal horn neurons in the cat , 1993, Neuroscience.

[41]  M. Devor,et al.  Mapping and plasticity of acid phosphatase afferents in the rat dorsal horn , 1980, Brain Research.

[42]  S. P. Hunt,et al.  Changing patterns of c-fos induction in spinal neurons following thermal cutaneous stimulation in the rat , 1990, Neuroscience.

[43]  E. Perl Afferent basis of nociception and pain: evidence from the characteristics of sensory receptors and their projections to the spinal dorsal horn. , 1980, Research publications - Association for Research in Nervous and Mental Disease.

[44]  M. Tohyama,et al.  Vasoactive intestinal polypeptide (VIP)-containing neurons in the spinal cord of the rat and their projections , 1983, Neuroscience Letters.

[45]  D. Lima,et al.  Structural types of marginal (lamina I) neurons projecting to the dorsal reticular nucleus of the medulla oblongata , 1990, Neuroscience.

[46]  N. Rajakumar,et al.  Biotinylated dextran: a versatile anterograde and retrograde neuronal tracer , 1993, Brain Research.

[47]  K. D. Cliffer,et al.  PHA-L can be transported anterogradely through fibers of passage , 1988, Brain Research.

[48]  J. Seckl,et al.  Increased expression of preprotachykinin, calcitonin gene-related peptide, but not vasoactive intestinal peptide messenger RNA in dorsal root ganglia during the development of adjuvant monoarthritis in the rat. , 1992, Brain research. Molecular brain research.

[49]  K. Ren,et al.  Descending modulation of Fos expression after persistent peripheral inflammation , 1996, Neuroreport.

[50]  J. Wu,et al.  Distribution, ontogeny and projections of cholecystokinin-8, vasoactive intestinal polypeptide and γ-aminobutyrate-containing neuron systems in the rat spinal cord: An immunohistochemical analysis , 1985, Neuroscience.

[51]  R. Petralia,et al.  Light and electron microscopic immunocytochemical localization of AMPA‐selective glutamate receptors in the rat spinal cord , 1994, The Journal of comparative neurology.

[52]  A. Duggan,et al.  Bilaterally enhanced dorsal horn postsynaptic currents in a rat model of peripheral mononeuropathy , 1996, Neuroscience Letters.

[53]  J. Beal,et al.  Quantitative and neurogenic analysis of neurons with supraspinal projections in the superficial dorsal horn of the rat lumbar spinal cord , 1997, The Journal of comparative neurology.

[54]  T. Freund,et al.  Calcium‐binding proteins, parvalbumin‐ and calbindin‐D 28k‐immunoreactive neurons in the rat spinal cord and dorsal root ganglia: A light and electron microscopic study , 1990, The Journal of comparative neurology.

[55]  J E Swett,et al.  The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord , 1985, The Journal of comparative neurology.

[56]  Perl Er Afferent basis of nociception and pain: evidence from the characteristics of sensory receptors and their projections to the spinal dorsal horn. , 1980 .

[57]  W D Willis,et al.  The pain system. The neural basis of nociceptive transmission in the mammalian nervous system. , 1985, Pain and headache.

[58]  A. Reiner,et al.  Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies , 1992, Journal of Neuroscience Methods.

[59]  J. Beal,et al.  Quantitative and neurogenic analysis of the total population and subpopulations of neurons defined by axon projection in the superficial dorsal horn of the rat lumbar spinal cord , 1997, The Journal of comparative neurology.

[60]  D. Menétrey,et al.  Spinal neurons reaching the lateral reticular nucleus as studied in the rat by retrograde transport of horseradish peroxidase , 1983, The Journal of comparative neurology.

[61]  D. Lima,et al.  Neurons in the substantia gelatinosa rolandi (lamina II) project to the caudal ventrolateral reticular formation of the medulla oblongata in the rat , 1991, Neuroscience Letters.

[62]  W. Willis,et al.  Neural changes in acute arthritis in monkeys. III. Changes in substance P, calcitonin gene-related peptide and glutamate in the dorsal horn of the spinal cord , 1992, Brain Research Reviews.

[63]  H. Groenewegen,et al.  Neuroanatomical tracing by use of Phaseolus vulgaris-leucoagglutinin (PHA-L): electron microscopy of PHA-L-filled neuronal somata, dendrites, axons and axon terminals , 1985, Brain Research.