Skip to main content
SpringerLink
Log in

Brain stem afferents to the anterior dorsal ventricular ridge in a lizard (Varanus exanthematicus)

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

The anterior dorsal ventricular ridge (ADVR), a large intraventricular protrusion in the reptilian forebrain, receives information from many different sensory modalities and in turn, projects massively onto the striatum. The ADVR possesses functional similarities to the mammalian isocortex and may perform complex sensory integrations. The ADVR in lizards is composed of three longitudinal zones which receive visual, somatosensory and acustic information, respectively. These projections are relayed via thalamic nuclei. Previous retrograde tracer studies also suggested brain stem projections to the ADVR arising in the midbrain reticular formation and in certain monoaminergic brain stem nuclei (substantia nigra, locus coeruleus and nucleus raphes superior). In the present study the powerful retrograde fluorescent tracer. ‘Fast Blue’ was applied as a slow-release gel to the ADVR of the savanna monitor lizard, Varanus exanthematicus. Thalamic projections were confirmed and various direct brain stem projections to the ADVR were demonstrated. Brain stem afferents to the ADVR were found from the laminar nucleus of the torus semicircularis (possibly comparable to the mammalian periaqueductal gray), from the midbrain reticular formation, from the substantia nigra (pars compacta and reticulata) and the adjacent ventral tegmental area, from the nucleus raphes superior, from the locus coeruleus, from the parabrachial region, from the nucleus of the lateral lemniscus and even from the most caudal part of the brain stem (a few neurons in the nucleus of the solitary tract and lateral reticular formation, possibly comparable to the mammalian A2 and A1 groups, respectively). These data strongly suggest direct ADVR projections from the parabrachial region (related to visceral and taste information) as well as distinct catecholaminergic (presumably dopaminergic: substantia nigra, ventral tegmental area and, noradrenergic: locus coeruleus, respectively) and serotonergic projections (nucleus raphes superior).

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Balaban CD, Ulinski PS (1981) Organization of thalamic afferents to anterior dorsal ventricular ridge in turtles. I. Projections of thalamic nuclei. J Comp Neurol 200:95–129

    Google Scholar 

  • Belekhova MG, Kenigfest NB (1983) A study of the hippocampal mediodorsal cortex connections in lizards by means of horseradish peroxidase axonal transport. Neurophysiology (Kiev) 15:145–152

    Google Scholar 

  • Belekhova MG, Zharskaja VD, Khachunts AS, Gaidaenko GV, Tumanova NL (1985) Connections of the mesencephalic, thalamic and telencephalic auditory centers in turtles. Some structural bases for audiosomatic interrelations. J Hirnforsch 26:127–152

    Google Scholar 

  • Bentivoglio M, Macchi G, Rossini P, Tempesta E (1978) Brain stem neurons projecting to neocortex: a HRP study in the cat. Exp Brain Res 31:489–498

    Google Scholar 

  • Björklund A, Lindvall O (1984) Dopamine-containing systems in the CNS. In: Björklund A, Hökfelt T (eds) Handbook of Chemical Neuroanatomy, vol 2: Classical Transmitters in the CNS. Elsevier, Amsterdam, pp 55–122

    Google Scholar 

  • Bruce LL, Butler AB (1984a) Telencephalic connections in lizards. I. Projections to cortex. J Comp Neurol 229:585–601

    Google Scholar 

  • Bruce LL, Butler AB (1984b) Telencephalic connections in lizards. II. Projections to anterior dorsal ventricular ridge. J Comp Neurol 229:602–615

    Google Scholar 

  • Carpenter MB (1981) Anatomy of the corpus striatum and brain stem integrating systems. In: Brooks VB (ed) Handbook of Physiology-The Nervous System, Vol II (Motor Control). Am Physiol Soc, Bethesda, pp 947–995

    Google Scholar 

  • Desan PH (1985) Afferent connections of the cerebral cortex of the turtle (Pseudemys scripta elegans). Soc Neurosci Abst 11:1310

    Google Scholar 

  • Divac I (1975) Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Res 93:385–398

    Google Scholar 

  • Fulwiler CE, Saper CB (1984) Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat. Brain Rev Rev 7:229–259

    Google Scholar 

  • Graybiel AM, Ragsdale CW (1983) Biochemical anatomy of the striatum. In: Emson PC (ed) Chemical Neuroanatomy. Raven Press, New York, pp 427–504

    Google Scholar 

  • Griffin G, Watkins LR, Mayer DJ (1979) HRP pellets and slowrelease gels: two new techniques for greater localization and sensitivity. Brain Res 168:595–601

    Google Scholar 

  • Hohmann CF, Carroll PT, Ebner FF (1983) Acetylcholine levels and choline acetyltransferase activity in turtle cortex. Brain Res 258:120–122

    Google Scholar 

  • Hoogland PV (1977) Efferent connections of the striatum in Tupinambis nigropunctatus. J Morphol 152:229–246

    Google Scholar 

  • Hoogland PV (1981) Spinothalamic projections in a lizard, Varanus exanthematicus: an HRP study. J Comp Neurol 198:7–12

    Google Scholar 

  • Jones BE, Yang T-Z (1985) The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat. J Comp Neurol 242:56–92

    Google Scholar 

  • Källén B (1951) On the ontogeny of the reptilian forebrain. Nuclear structures and ventricular sulci. J Comp Neurol 36:143–192

    Google Scholar 

  • Kievit J, Kuypers HGJM (1975) Subcortical afferents to the frontal lobe in the rhesus monkey studied by means of retrograde horseradish peroxidase transport. Brain Res 85:261–266

    Google Scholar 

  • Kimura H, McGeer PL, Peng JH, McGeer EG (1981) The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat. J Comp Neurol 200:151–201

    Google Scholar 

  • Kuypers HGJM, Huisman AM (1984) Fluorescent neuronal tracers. In: Federoff S (ed) Labeling Methods Applicable to the Study of Neuronal Pathways. Adv Cell Neurobiol, vol 5. Academic Press, New York, pp 307–340

    Google Scholar 

  • Lasiter PS, Glanzman DL, Mensah PA (1982) Direct connectivity between pontine taste areas and gustatory neocortex in rat. Brain Res 234:111–121

    Google Scholar 

  • Lindvall O, Björklund A (1978) Organization of catecholamine neurons in the rat central nervous system. In: Iversen LL, Iversen SD, Snyder SH (eds) Chemical Pathways in the Brain. Hb Psychopharmacol, vol 9. Plenum Press, New York, pp 139–231

    Google Scholar 

  • Lohman AHM, van Woerden-Verkley I (1978) Ascending connections to the forebrain in the tegu lizard. J Comp Neurol 182:555–594

    Google Scholar 

  • Loughlin SE, Fallon JH (1984) Substantia nigra and ventral tegmental area projections to cortex: topography and collateralization. Neuroscience 11:425–435

    Google Scholar 

  • Markowitsch HJ, Irle E (1981) Widespread cortical projections of the ventral tegmental area and of other brain stem structures in the cat. Exp Brain Res 41:233–246

    Google Scholar 

  • Mesulam M-M, Mufson EJ, Levey AI, Wainer BH (1983) Cholinergic innervation of cortex by basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata) and hypothalamus in the rhesus monkey. J Comp Neurol 214:170–197

    Google Scholar 

  • Mufson EJ, Desan PH, Mesulam M-M, Wainer BH, Levey AI (1984) Choline aceyltransferase-like immunoreactivity in the forebrain of the red-eared pond turtle (Pseudemys scripta elegans). Brain Res 323:103–108

    Google Scholar 

  • Nauta WJH, Karten HJ (1970) A general profile of the vertebrate brain, with sidelights on the ancestry of cerebral cortex. In: Schmitt FO (ed) The Neurosciences: Second Study Program. Rockefeller University Press, New York, pp 7–26

    Google Scholar 

  • Nieuwenhuys R (1985) Chemoarchitecture of the Brain. Springer Verlag, Berlin Heidelberg New York

    Google Scholar 

  • Norgren R (1984) Taste: central neural mechanisms. In: Darian-Smith I (ed) Hb Physiology. The Nervous System, Vol III (Sensory Processes). Am Physiol Soc, Bethesda, pp 1087–1128

    Google Scholar 

  • Northcutt RG (1978) Forebrain and midbrain organization in lizards and its phylogenetic significance. In: Greenberg N, MacLean PD (eds) Behavior and Neurology of Lizards, Nat Inst Mental Health, Rockville, Md, pp 11–64

    Google Scholar 

  • Northeutt RG (1981) Evolution of the telencephalon in nonmammals. Ann Rev Neurosci 4:301–350

    Google Scholar 

  • Northcutt RG (1984) Evolution of the vertebrate central nervous system: patterns and processes. Am Zool 24:701–716

    Google Scholar 

  • Oades RD, Halliday GM (1987) Ventral tegmental (A10)system: neurobiology. 1. Anatomy and connectivity. Brain Res Rev 12:117–165

    Google Scholar 

  • Ouimet CC, Patrick RL, Ebner FF (1985) The projection of three extrathalamic cell groups to the cerebral cortex of the turtle Pseudemys. J Comp Neurol 237:77–84

    Google Scholar 

  • Parent A (1979) Monoaminergic systems of the brain. In: Gans C, Northcutt RG, Ulinski P (eds) Biology of the Reptilia, vol 10: Neurology B. Academic Press, London, pp 247–285

    Google Scholar 

  • Parent A, Poitras D, Dubé L (1984) Comparative anatomy of central monoaminergic systems. In: Björklund A, Hökfelt T (eds) Handbook of Chemical Neuroanatomy, vol 2: Classical Transmitters in the CNS. Elsevier, Amsterdam, pp 409–439

    Google Scholar 

  • Porrino LJ, Goldman-Rakic PS (1982) Brainstem innervation of prefrontal and anterior cingulate cortex in the rhesus monkey revealed by retrograde transport of HRP. J Comp Neurol 205:63–76

    Google Scholar 

  • Pritz MB (1980) Parallels in the organization of auditory and visual systems in crocodiles. In: Ebbesson SOE (ed) Comparative Neurology of the telencephalon. Plenum Press, New York, pp 331–342

    Google Scholar 

  • Pritz MB, Northcutt RG (1980) Anatomical evidence for an ascending somatosensory pathway to the telencephalon in crocodile, Caiman corocilus. Exp Brain Res 40:342–345

    Google Scholar 

  • Pritz MB, Stritzel ME (1985) Thalamic projections to the noncortical telencephalon in a reptile. Soc Neurosci Abstr 11:1309

    Google Scholar 

  • Ricardo JA, Koh ET (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res 153:1–26

    Google Scholar 

  • Smeets WJAJ, Hoogland PV, Voorn P (1986) The distribution of dopamine immunoreactivity in the forebrain and midbrain of the lizard Gekko gecko: an immunohistochemical study with antibodies against dopamine. J Comp Neurol 253:46–60

    Google Scholar 

  • Steinbusch HWM, Nieuwenhuys R (1983) The raphe nuclci of the rat brain stem: a cytoarchitectonic and immunohistochemical study. In: Emson PC (ed) Chemical Neuroanatomy. Raven Press, New York, pp 131–207

    Google Scholar 

  • ten Donkelaar HJ, de Boer-van Huizen R (1981) Ascending projections of the brain stem reticular formation in a nonmammalian vertebrate (the lizard Varanus exanthematicus), with notes on the afferent connections of the forebrain. J Comp Neurol 200:501–528

    Google Scholar 

  • ten Donkelaar HJ, de Boer-van Huizen R (1984) Ascending and descending axon collaterals efferent from the brain stem reticular formation. A retrograde fluorescent tracer study in the lizard, Varanus exanthematicus. Brain Res 32:184–188

    Google Scholar 

  • ten Donkelaar HJ, Bangma GC, de Boer-van Huizen R (1985) The fasciculus longitudinalis medialis in the lizard Varanus exanthematicus. 2. Vestibular and internuclear components. Anat Embryol 172:205–215

    Google Scholar 

  • ten Donkelaar HJ, Bangma GC, Barbas-Henry HA, de Boer-van Huizen R, Wolters JG (1987) The brain stem in a lizard Varanus exanthematicus. Adv Anat Embryol Cell Biol, Vol 107. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Ueda S, Takeushi Y, Sano Y (1983) Immunohistochemical demonstration of serotonin neurons in the central nervous system of the turtle Clemmys japonica. Anat Embryol 108:1–19

    Google Scholar 

  • Ulinski PS (1983) Dorsal Ventricular Ridge: A Treatise on Forebrain Organization in Reptiles and Birds. Wiley, New York

    Google Scholar 

  • Voneida TJ, Sligar CM (1979) Efferent projections of the dorsal ventricular ridge and the striatum in the tegu lizard, Tupinambis nigropunctatus. J Comp Neurol 186:43–64

    Google Scholar 

  • Wolters JG, ten Donkelaar HJ, Verhofstad AAJ (1984) Distribution of catecholamines in the brain stem and spinal cord of the lizard Varanus exanthematicus: an immunohistochemical study based on the use of antibodies to tyrosine hydroxylase. Neuroscience 13:469–493

    Google Scholar 

  • Wolters JG, ten Donkelaar HJ, Steinbusch HWM, Verhofstad AAJ (1985) Distribution of serotonin in the brain stem and spinal cord of the lizard Varanus exanthematcus: an immunohistochemical study. Neuroscience 14:169–193

    Google Scholar 

  • Wolters JG, ten Donkelaar HJ, Verhofstad AAJ (1986a) Distribution of some peptides (substance P, Leu enkephalin, Met enkephalin) in the brain stem and spinal cord of a lizard, Varanus exanthematicus. Neuroscience 18:917–946

    Google Scholar 

  • Wolters JG, de Boer-van Huizen R, ten Donkelaar HJ, Leenen L (1986b) Collateralization of descending pathways from the brainstem to the spinal cord in a lizard, Varanus exanthematicus. J Comp Neurol 251:317–333

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Embryology, University of Nijmegen, The Netherlands

    H. J. ten Donkelaar & R. de Boer-van Huizen

Authors
  1. H. J. ten Donkelaar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. de Boer-van Huizen
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

ten Donkelaar, H.J., de Boer-van Huizen, R. Brain stem afferents to the anterior dorsal ventricular ridge in a lizard (Varanus exanthematicus). Anat Embryol 177, 465–475 (1988). https://doi.org/10.1007/BF00304745

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00304745

Key words

Search

Navigation