Topographical distribution of dorsal and median raphe neurons projecting to motor, Sensorimotor, and visual cortical Areas in the rat
Abstract
Abstract The present study was conducted to examine the spatial organization of dorsal (DR) and median (MR) raphe neurons that project to rostrocaudally aligned areas of the rat cerebral cortex. An additional goal was to determine if individual DR cells that send efferents to forelimb sensorimotor or visual regions of the neocortex also send axon collaterals to forelimb (crus II) or visual (paraflocculus) areas of the cerebellum. Long‐Evans hooded rats received unilateral pressure injections of horseradish peroxidase (HRP) in either motor n = 4) or sensorimotor (n = 5) or visual (n = 4) cortex to determine the intranuclear location of DR and MR neurons that project to specific neocortical regions. Coronal sections (40‐100 μm) through the pons and midbrain were examined by light microscopy after the tetramethyl benzidine reaction and neutral red counterstaining were carried out. The locations of retrogradely labeled cells were recorded relative to a threedimensional biological coordinate system maintained by a computer linked to the light microscope. For double labeling studies, unilateral injections of fast blue and nuclear yellow were made in paired motor (sensorimotor cortex and crus II of the lateral cerebellum) or visual (cortical area 17 and paraflocculus) areas of the CNS. Coronal tissue sections (35 μm) were collected on coverslips and examined on a Leitz fluorescence microscope (wavelength = 365 nm). DR neurons labeled from cerebrocortical injections of HRP were concentrated in the rostral two‐thirds of the nucleus. HRP‐filled neurons were distributed such that individual groups of neurons projecting to motor, sensorimotor, or visual cortex were aligned in a partially overlapping, rostral to caudal array. In the dorsoventral dimension, retrogradely labeled cells were clustered in three distinct groupings such that neurons projecting to the motor, sensorimotor, and visual areas were concentrated in dorsal, intermediate, and ventral portions of the DR nucleus, respectively. For all cases, the majority of HRP‐filled cells were positioned along the midline or displaced to the side of the nucleus that was ipsilateral to the cortical injection site. A small number of retrogradely labeled neurons were observed in the MR following injections in the motor cortex. Computer‐assisted reconstruction of th z neuroanatomical data facilitated the visualization of spatial relationships between groups of DR neocortical projection neurons. Twenty to 30% of the cells labeled in the DR after paired injections of fast blue and nuclear yellow in sensorimotor or visual areas of the neocortex and cerebellum were doubled labeled indicating that individual DR neurons can send axon collaterals to functionally analogous regions of the CNS. Overall, the results indicate that, within the DR, a topographic ordering exists with respect to rostrocaudally aligned terminal fields in the neocortex. In addition, a portion of the DR cerebrocortical projection neurons also send axon collaterals to specific regions of the cerebellar cortex. The intranuclear organization observed in this study suggests that neuronal activity in distinct regions of the DR nucleus may independently influence discrete populations of cerebrocortical cells. Furthermore, the possibility must now be considered that a substantial number of single DR neurons provide a common input via axon collerals to portions of the neocortical and cerebellar circuitry that receive afferent information related to the same sensory or motor function.
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Most subcortical-projecting neurons were located in the dorsal DRN, whereas most cortical-projecting neurons were located in the ventral DRN.
“Consistent with previous reports (Ren et al., 2018; Waterhouse et al., 1986), we found that most subcortical-projecting neurons were located in the dorsal DRN, whereas most cortical-projecting neurons were located in the ventral DRN.”
From Molecular and anatomical organization of the dorsal raphe nucleus (2019) · cites this paper as Waterhouse et al., 1986
Cites
Dahlstroem, A., & Fuxé, K. (1964) · PubMed · Cited by 5,143 · see citing works
Mesulam, M. M. (1978) · Journal of Histochemistry & Cytochemistry · doi:10.1177/26.2.24068 · Cited by 4,303 · see citing works
Steinbusch, H. W. M. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90146-9 · Cited by 2,415 · see citing works
Azmitia, E. C., & Segal, M. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901790311 · Cited by 1,908 · see citing works
Ascending Monoamine Neurons to the Telencephalon and Diencephalon
Andén, N. ‐., Dahlström, A. B., Fuxé, K., Larsson, K., Olson, L., & Ungerstedt, U. (1966) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1966.tb03318.x · Cited by 1,214 · see citing works
Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas
Krieg, W. J. S. (1946) · The Journal of Comparative Neurology · doi:10.1002/cne.900840205 · Cited by 1,018 · see citing works
Organization of motor and somatosensory neocortex in the albino rat
Hall, R. D., & Lindholm, E. P. (1974) · Brain Research · doi:10.1016/0006-8993(74)90076-6 · Cited by 897 · see citing works
Serotonin neurons of the midbrain raphe: Ascending projections
Moore, R. Y., Halaris, A. E., & Jones, B. E. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901800302 · Cited by 803 · see citing works
Conrad, L. C. A., Leonard, C. M., & Pfaff, D. W. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901560205 · Cited by 683 · see citing works
Mesulam, M. ‐. (1976) · Journal of Histochemistry & Cytochemistry · doi:10.1177/24.12.63512 · Cited by 659 · see citing works
The organization of afferent projections to the midbrain periaqueductal gray of the rat
Beitz, A. J. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90157-9 · Cited by 544 · see citing works
Serotonin nerve terminals in adult rat neocortex
Descarries, L., Beaudet, A., & Watkins, K. C. (1975) · Brain Research · doi:10.1016/0006-8993(75)90158-4 · Cited by 508 · see citing works
The serotonin innervation of the cerebral cortex in the rat—an immunohistochemical analysis
Lidov, H. G. W., Grzanna, R., & Molliver, M. E. (1980) · Neuroscience · doi:10.1016/0306-4522(80)90099-8 · Cited by 417 · see citing works
Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique
Aghajanian, G. K., & Wang, R. Y. (1977) · Brain Research · doi:10.1016/0006-8993(77)90291-8 · Cited by 380 · see citing works
Sawchenko, P. E., Swanson, L. W., Steinbusch, H. W. M., & Verhofstad, A. A. J. (1983) · Brain Research · doi:10.1016/0006-8993(83)90945-9 · Cited by 380 · see citing works
Descarries, L., Watkins, K. C., Garcia, S., & Beaudet, A. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902070305 · Cited by 380 · see citing works
Immunohistochemical study of the development of serotonergic neurons in the rat CNS
Lidov, H. G. W., & Molliver, M. E. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90164-2 · Cited by 376 · see citing works
Arnsten, A. F. T., & Goldman-Rakic, P. S. (1984) · Brain Research · doi:10.1016/0006-8993(84)90351-2 · Cited by 333 · see citing works
Köhler, C., & Steinbusch, H. W. M. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90054-9 · Cited by 330 · see citing works
Pickel, V. M., JOH, T. H., & Reis, D. J. (1977) · Brain Research · doi:10.1016/0006-8993(77)90515-7 · Cited by 274 · see citing works
Baraban, J. M., & Aghajanian, G. K. (1981) · Brain Research · doi:10.1016/0006-8993(81)90646-6 · Cited by 259 · see citing works
Locus coeruleus projections to cortex: Topography, morphology and collateralization
Loughlin, S. E., Foote, S. L., & Fallon, J. H. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90142-3 · Cited by 212 · see citing works
Belin, M., Aguera, M., Tappaz, M., McRae‐Degueurce, A., Bobillier, P., & Pujol, J. F. (1979) · Brain Research · doi:10.1016/0006-8993(79)90107-0 · Cited by 205 · see citing works
Köhler, C., Chan‐Palay, V., & Steinbusch, H. W. M. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902090109 · Cited by 188 · see citing works
Jacobs, B. L., Foote, S. L., & Bloom, F. E. (1978) · Brain Research · doi:10.1016/0006-8993(78)90779-5 · Cited by 184 · see citing works
The distribution of neocortical projection neurons in the locus coeruleus
Waterhouse, B. D., Lin, C.-S., Burne, R. A., & Woodward, D. J. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902170406 · Cited by 180 · see citing works
Self-citationMonoamine innervation of the forebrain: Collateralization
Fallon, J. H., & Loughlin, S. E. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90143-5 · Cited by 170 · see citing works
Afferents to the periaqueductal gray in the rat. A horseradish peroxidase study
Marchand, J. E., & Hagino, N. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90049-0 · Cited by 166 · see citing works
Serotonin nerve terminals in the locus coeruleus of adult rat: A radioautographic study
Léger, L., & Descarries, L. (1978) · Brain Research · doi:10.1016/0006-8993(78)90791-6 · Cited by 163 · see citing works
Björklund, A., FALCK, B., & Stenevi, U. (1971) · Brain Research · doi:10.1016/0006-8993(71)90324-6 · Cited by 154 · see citing works
Occurrence of dopamine-containing neurons in the midbrain raphe nuclei of the rat
Ochi, J., & Shimizu, K. (1978) · Neuroscience Letters · doi:10.1016/0304-3940(78)90142-8 · Cited by 127 · see citing works
Steinbusch, H. W. M., van der Kooy, D., Verhofstad, A. A. J., & Pellegrino, A. (1980) · Neuroscience Letters · doi:10.1016/0304-3940(80)90184-6 · Cited by 126 · see citing works
de Olmos, J. S., & Heimer, L. (1980) · Neuroscience Letters · doi:10.1016/0304-3940(80)90247-5 · Cited by 118 · see citing works
van der Kooy, D., & Kuypers, H. G. J. M. (1979) · Science · doi:10.1126/science.441742 · Cited by 104 · see citing works
NAGATSU, I., INAGAKI, S., KONDO, Y., KARASAWA, N., & NAGATSU, T. (1979) · ACTA HISTOCHEMICA ET CYTOCHEMICA · doi:10.1267/ahc.12.20 · Cited by 98 · see citing works
Horseradish peroxidase tracing of the lateral habenular-midbrain raphe nuclei connections in the rat
Pasquier, D. A., Anderson, C. D., Forbes, W. B., et al. (1976) · Brain Research Bulletin · doi:10.1016/0361-9230(76)90114-3 · Cited by 82 · see citing works
Nucleus raphe dorsalis: A morphometric golgi study in rats of three age groups
Díaz-Cintra, S. Y., Cintra, L., Kemper, T. L., Resnick, O., & Morgane, P. J. (1981) · Brain Research · doi:10.1016/0006-8993(81)90675-2 · Cited by 71 · see citing works
Bowker, R. M., Westlund, K. N., & Coulter, J. D. (1981) · Neuroscience Letters · doi:10.1016/0304-3940(81)90160-9 · Cited by 66 · see citing works
Gamrani, H., Calas, A., Belin, M., et al. (1979) · Neuroscience Letters · doi:10.1016/0304-3940(79)91527-1 · Cited by 62 · see citing works
Response properties of neurons in the visual cortex of the rat
Burne, R. A., Parnavelas, J. G., & Lin, C.-S. (1984) · Experimental Brain Research · doi:10.1007/bf00238168 · Cited by 56 · see citing works
Agnati, L. F., Fuxé, K., Hökfelt, T. G. M., Benfenati, F., Calzà, L., Johansson, O., & Mey, J. D. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90119-8 · Cited by 25 · see citing works
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A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat
Vertes, R. P. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903130409 · Cited by 842 · see citing works
The human raphe nuclei and the serotonergic system
Hornung, J.-P. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2003.10.002 · Cited by 742 · see citing works
Neural circuits mediating stress
López, J. F., Akil, H., & Watson, S. J. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00266-8 · Cited by 373 · see citing works
Top-Down Control of Motor Cortex Ensembles by Dorsomedial Prefrontal Cortex
Narayanan, N. S., & Laubach, M. (2006) · Neuron · doi:10.1016/j.neuron.2006.10.021 · Cited by 311 · see citing works
Muzerelle, A., Scotto-Lomassese, S., Bernard, J. F., Soiza-Reilly, M., & Gaspar, P. (2016) · Brain Structure and Function · doi:10.1007/s00429-014-0924-4 · Cited by 303 · see citing works
Molecular and anatomical organization of the dorsal raphe nucleus
Huang, K. W., Ochandarena, N. E., Philson, A. C., Hyun, M., Birnbaum, J. E., Cicconet, M., & Sabatini, B. L. (2019) · eLife · doi:10.7554/elife.46464 · Cited by 267 · see citing works
Waselus, M., Valentino, R. J., & Van Bockstaele, E. J. (2011) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2011.05.011 · Cited by 142 · see citing works
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Fox, J. H., & Lowry, C. A. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00169 · Cited by 93 · see citing works
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Hornung, J.-P. (2010) · Handbook of Behavioral Neuroscience · doi:10.1016/s1569-7339(10)70071-0 · Cited by 45 · see citing works
Herrero, M. T., Insausti, R., & Gonzalo, L. M. (1991) · Brain Research · doi:10.1016/0006-8993(91)90029-u · Cited by 33 · see citing works
Lee, S.-B., Lee, H. S., & Waterhouse, B. D. (2008) · Brain Research · doi:10.1016/j.brainres.2008.04.003 · Cited by 27 · see citing works
Self-citation
- Authors
- Waterhouse, B. D., Mihailoff, G. A., Baack, J. C., & Woodward, D. J.
- Affiliations
- University of Texas Health Science Center at Dallas (US)
- ORCID
- Waterhouse, Barry D.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 1986-07-22
- Volume
- 249
- Issue
- 4
- Pages
- 460-476
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2170771167
- Cited by
- 136
- References
- 41
- Citations by year
- 2026: 1 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 4 · 2020: 6 · 2019: 4 · 2018: 3 · 2017: 2 · 2016: 3 · 2015: 5 · 2014: 4 · 2013: 5 · 2012: 6
- FWCI
- 0.82
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Drug Abuse (DA-02338)
- National Institute of Neurological Disorders and Stroke (NS-12644, NS-18081)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
- Keywords
- dorsal raphe nucleus, median raphe nucleus, raphe neurons, topographic organization, motor cortex, sensorimotor cortex, visual cortex, cerebellar Crus II, paraflocculus, axon collaterals, retrograde tracing, horseradish peroxidase, Fast Blue, thalamic nuclei
- MeSH terms
- Animals, Brain Mapping, Cell Count, Cerebral Cortex, Efferent Pathways, Fluorescent Dyes, Motor Cortex, Neurons, Raphe Nuclei, Rats, Inbred Strains, Somatosensory Cortex, Stereotaxic Techniques, Visual Cortex, Rats
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