Abstract
The basal ganglia (BG) have received much attention during the last 3 decades mainly because of their clinical relevance. Our understanding of their structure, organisation and function in terms of chemoarchitecture, compartmentalisation, connections and receptor localisation has increased equally. Most of the research has been focused on the mammalian BG, but a considerable number of studies have been carried out in nonmammalian vertebrates, in particular reptiles and birds. The BG of the latter 2 classes of vertebrates, which together with mammals constitute the amniotic vertebrates, have been thoroughly studied by means of tract-tracing and immunohistochemical techniques. The terminology used for amniotic BG structures has frequently been adopted to indicate putative corresponding structures in the brain of anamniotes, i.e. amphibians and fishes, but data for such a comparison were, until recently, almost totally lacking. It has been proposed several times that the occurrence of well developed BG structures probably constitutes a landmark in the anamniote-amniote transition. However, our recent studies of connections, chemoarchitecture and development of the basal forebrain of amphibians have revealed that tetrapod vertebrates share a common pattern of BG organisation. This pattern includes the existence of dorsal and ventral striatopallidal systems, reciprocal connections between the striatopallidal complex and the diencephalic and mesencephalic basal plate (striatonigral and nigrostriatal projections), and descending pathways from the striatopallidal system to the midbrain tectum and reticular formation. The connectional similarities are paralleled by similarities in the distribution of chemical markers of striatal and pallidal structures such as dopamine, substance P and enkephalin, as well as by similarities in development and expression of homeobox genes. On the other hand, a major evolutionary trend is the progressive involvement of the cortex in the processing of the thalamic sensory information relayed to the BG of tetrapods. By using the comparative approach, new insights have been gained with respect to certain features of the BG of vertebrates in general, such as the segmental organisation of the midbrain dopaminergic cell groups, the occurrence of large numbers of dopaminergic cell bodies within the telencephalon itself and the variability in, among others, connectivity and chemoarchitecture. However, the intriguing question whether the basal forebrain organisation of nontetrapods differs essentially from that observed in tetrapods still needs to be answered.
Keywords: Chemoarchitecture, comparative neuroanatomy, dorsal and ventral striatopallidal systems
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- Albin R. L., Young A. B., Penney J. B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989 Oct;12(10):366–375. doi: 10.1016/0166-2236(89)90074-x. [DOI] [PubMed] [Google Scholar]
- Alexander G. E., Crutcher M. D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990 Jul;13(7):266–271. doi: 10.1016/0166-2236(90)90107-l. [DOI] [PubMed] [Google Scholar]
- Anderson K. D., Reiner A. Extensive co-occurrence of substance P and dynorphin in striatal projection neurons: an evolutionarily conserved feature of basal ganglia organization. J Comp Neurol. 1990 May 15;295(3):339–369. doi: 10.1002/cne.902950302. [DOI] [PubMed] [Google Scholar]
- Anderson K. D., Reiner A. Immunohistochemical localization of DARPP-32 in striatal projection neurons and striatal interneurons: implications for the localization of D1-like dopamine receptors on different types of striatal neurons. Brain Res. 1991 Dec 24;568(1-2):235–243. doi: 10.1016/0006-8993(91)91403-n. [DOI] [PubMed] [Google Scholar]
- Anderson S. A., Qiu M., Bulfone A., Eisenstat D. D., Meneses J., Pedersen R., Rubenstein J. L. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron. 1997 Jul;19(1):27–37. doi: 10.1016/s0896-6273(00)80345-1. [DOI] [PubMed] [Google Scholar]
- Betarbet R., Turner R., Chockkan V., DeLong M. R., Allers K. A., Walters J., Levey A. I., Greenamyre J. T. Dopaminergic neurons intrinsic to the primate striatum. J Neurosci. 1997 Sep 1;17(17):6761–6768. doi: 10.1523/JNEUROSCI.17-17-06761.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Butler A. B. The evolution of the dorsal pallium in the telencephalon of amniotes: cladistic analysis and a new hypothesis. Brain Res Brain Res Rev. 1994 Jan;19(1):66–101. doi: 10.1016/0165-0173(94)90004-3. [DOI] [PubMed] [Google Scholar]
- Chevalier G., Deniau J. M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 1990 Jul;13(7):277–280. doi: 10.1016/0166-2236(90)90109-n. [DOI] [PubMed] [Google Scholar]
- DeLong M. R. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990 Jul;13(7):281–285. doi: 10.1016/0166-2236(90)90110-v. [DOI] [PubMed] [Google Scholar]
- Dubach M., Schmidt R., Kunkel D., Bowden D. M., Martin R., German D. C. Primate neostriatal neurons containing tyrosine hydroxylase: immunohistochemical evidence. Neurosci Lett. 1987 Mar 31;75(2):205–210. doi: 10.1016/0304-3940(87)90298-9. [DOI] [PubMed] [Google Scholar]
- Ewert J. P. Neural correlates of key stimulus and releasing mechanism: a case study and two concepts. Trends Neurosci. 1997 Aug;20(8):332–339. doi: 10.1016/s0166-2236(96)01042-9. [DOI] [PubMed] [Google Scholar]
- Faull R. L., Mehler W. R. The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience. 1978;3(11):989–1002. doi: 10.1016/0306-4522(78)90119-7. [DOI] [PubMed] [Google Scholar]
- Figueredo-Cardenas G., Medina L., Reiner A. Calretinin is largely localized to a unique population of striatal interneurons in rats. Brain Res. 1996 Feb 12;709(1):145–150. doi: 10.1016/0006-8993(95)01392-x. [DOI] [PubMed] [Google Scholar]
- Figueredo-Cardenas G., Morello M., Sancesario G., Bernardi G., Reiner A. Colocalization of somatostatin, neuropeptide Y, neuronal nitric oxide synthase and NADPH-diaphorase in striatal interneurons in rats. Brain Res. 1996 Oct 7;735(2):317–324. doi: 10.1016/0006-8993(96)00801-3. [DOI] [PubMed] [Google Scholar]
- Fritzsch B. Fast axonal diffusion of 3000 molecular weight dextran amines. J Neurosci Methods. 1993 Oct;50(1):95–103. doi: 10.1016/0165-0270(93)90060-5. [DOI] [PubMed] [Google Scholar]
- Glover J. C., Petursdottir G., Jansen J. K. Fluorescent dextran-amines used as axonal tracers in the nervous system of the chicken embryo. J Neurosci Methods. 1986 Nov;18(3):243–254. doi: 10.1016/0165-0270(86)90011-7. [DOI] [PubMed] [Google Scholar]
- Gonzalez A., Russchen F. T., Lohman A. H. Afferent connections of the striatum and the nucleus accumbens in the lizard Gekko gecko. Brain Behav Evol. 1990;36(1):39–58. doi: 10.1159/000115296. [DOI] [PubMed] [Google Scholar]
- Gonzalez A., Smeets W. J. Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. J Comp Neurol. 1991 Jan 15;303(3):457–477. doi: 10.1002/cne.903030311. [DOI] [PubMed] [Google Scholar]
- González A., Muñoz A., Muñoz M., Marín O., Arévalo R., Porteros A., Alonso J. R. Nitric oxide synthase in the brain of a urodele amphibian (Pleurodeles waltl) and its relation to catecholaminergic neuronal structures. Brain Res. 1996 Jul 15;727(1-2):49–64. doi: 10.1016/0006-8993(96)00354-x. [DOI] [PubMed] [Google Scholar]
- González A., Smeets W. J. Noradrenaline in the brain of the South African clawed frog Xenopus laevis: a study with antibodies against noradrenaline and dopamine-beta-hydroxylase. J Comp Neurol. 1993 May 15;331(3):363–374. doi: 10.1002/cne.903310306. [DOI] [PubMed] [Google Scholar]
- Goodman I., Zacny J., Osman A., Azzaro A., Donovan C. Dopaminergic nature of feeding-induced behavioral stereotypies in stressed pigeons. Pharmacol Biochem Behav. 1983 Feb;18(2):153–158. doi: 10.1016/0091-3057(83)90355-6. [DOI] [PubMed] [Google Scholar]
- Graybiel A. M. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci. 1990 Jul;13(7):244–254. doi: 10.1016/0166-2236(90)90104-i. [DOI] [PubMed] [Google Scholar]
- Greengard P., Nairn A. C., Girault J. A., Ouimet C. C., Snyder G. L., Fisone G., Allen P. B., Fienberg A., Nishi A. The DARPP-32/protein phosphatase-1 cascade: a model for signal integration. Brain Res Brain Res Rev. 1998 May;26(2-3):274–284. doi: 10.1016/s0165-0173(97)00057-x. [DOI] [PubMed] [Google Scholar]
- Groenewegen H. J., Berendse H. W., Haber S. N. Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience. 1993 Nov;57(1):113–142. doi: 10.1016/0306-4522(93)90115-v. [DOI] [PubMed] [Google Scholar]
- Groenewegen H. J., Berendse H. W. The specificity of the 'nonspecific' midline and intralaminar thalamic nuclei. Trends Neurosci. 1994 Feb;17(2):52–57. doi: 10.1016/0166-2236(94)90074-4. [DOI] [PubMed] [Google Scholar]
- Haber S. N., Groenewegen H. J. Interrelationship of the distribution of neuropeptides and tyrosine hydroxylase immunoreactivity in the human substantia Nigra. J Comp Neurol. 1989 Dec 1;290(1):53–68. doi: 10.1002/cne.902900105. [DOI] [PubMed] [Google Scholar]
- Haber S., Elde R. The distribution of enkephalin immunoreactive fibers and terminals in the monkey central nervous system: an immunohistochemical study. Neuroscience. 1982 May;7(5):1049–1095. doi: 10.1016/0306-4522(82)91118-6. [DOI] [PubMed] [Google Scholar]
- Hemmings H. C., Jr, Greengard P. DARPP-32, a dopamine- and adenosine 3':5'-monophosphate-regulated phosphoprotein: regional, tissue, and phylogenetic distribution. J Neurosci. 1986 May;6(5):1469–1481. doi: 10.1523/JNEUROSCI.06-05-01469.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Henselmans J. M., Hoogland P. V., Stoof J. C. Differences in the regulation of acetylcholine release upon D2 dopamine and N-methyl-D-aspartate receptor activation between the striatal complex of reptiles and the neostriatum of rats. Brain Res. 1991 Dec 6;566(1-2):8–12. doi: 10.1016/0006-8993(91)91674-p. [DOI] [PubMed] [Google Scholar]
- Hoogland P. V., Vermeulen-VanderZee E. Distribution of choline acetyltransferase immunoreactivity in the telencephalon of the lizard Gekko gecko. Brain Behav Evol. 1990;36(6):378–390. doi: 10.1159/000115320. [DOI] [PubMed] [Google Scholar]
- Ikemoto K., Nagatsu I., Kitahama K., Jouvet A., Nishimura A., Nishi K., Maeda T., Arai R. A dopamine-synthesizing cell group demonstrated in the human basal forebrain by dual labeling immunohistochemical technique of tyrosine hydroxylase and aromatic L-amino acid decarboxylase. Neurosci Lett. 1998 Feb 27;243(1-3):129–132. doi: 10.1016/s0304-3940(98)00103-7. [DOI] [PubMed] [Google Scholar]
- Inglis W. L., Winn P. The pedunculopontine tegmental nucleus: where the striatum meets the reticular formation. Prog Neurobiol. 1995 Sep;47(1):1–29. doi: 10.1016/0301-0082(95)00013-l. [DOI] [PubMed] [Google Scholar]
- Johnson M. D., Ma P. M. Localization of NADPH diaphorase activity in monoaminergic neurons of the rat brain. J Comp Neurol. 1993 Jun 22;332(4):391–406. doi: 10.1002/cne.903320402. [DOI] [PubMed] [Google Scholar]
- Kawaguchi Y., Wilson C. J., Augood S. J., Emson P. C. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 1995 Dec;18(12):527–535. doi: 10.1016/0166-2236(95)98374-8. [DOI] [PubMed] [Google Scholar]
- Marín O., González A., Smeets W. J. Anatomical substrate of amphibian basal ganglia involvement in visuomotor behaviour. Eur J Neurosci. 1997 Oct;9(10):2100–2109. doi: 10.1111/j.1460-9568.1997.tb01377.x. [DOI] [PubMed] [Google Scholar]
- Marín O., González A., Smeets W. J. Basal ganglia organization in amphibians: afferent connections to the striatum and the nucleus accumbens. J Comp Neurol. 1997 Feb 3;378(1):16–49. doi: 10.1002/(sici)1096-9861(19970203)378:1<16::aid-cne2>3.0.co;2-n. [DOI] [PubMed] [Google Scholar]
- Marín O., González A., Smeets W. J. Basal ganglia organization in amphibians: efferent connections of the striatum and the nucleus accumbens. J Comp Neurol. 1997 Mar 31;380(1):23–50. [PubMed] [Google Scholar]
- Marín O., Smeets W. J., González A. Basal ganglia organization in amphibians: chemoarchitecture. J Comp Neurol. 1998 Mar 16;392(3):285–312. [PubMed] [Google Scholar]
- Marín O., Smeets W. J., González A. Basal ganglia organization in amphibians: evidence for a common pattern in tetrapods. Prog Neurobiol. 1998 Jul;55(4):363–397. doi: 10.1016/s0301-0082(98)00008-2. [DOI] [PubMed] [Google Scholar]
- Marín O., Smeets W. J., González A. Evolution of the basal ganglia in tetrapods: a new perspective based on recent studies in amphibians. Trends Neurosci. 1998 Nov;21(11):487–494. doi: 10.1016/s0166-2236(98)01297-1. [DOI] [PubMed] [Google Scholar]
- Marín O., Smeets W. J., Muñoz M., Sanchez-Camacho C., Peña J. J., Lopez J. M., González A. Cholinergic and catecholaminergic neurons relay striatal information to the optic tectum in amphibians. Eur J Morphol. 1999 Apr;37(2-3):155–159. doi: 10.1076/ejom.37.2.155.4749. [DOI] [PubMed] [Google Scholar]
- McDonald R. J., White N. M. A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci. 1993 Feb;107(1):3–22. doi: 10.1037//0735-7044.107.1.3. [DOI] [PubMed] [Google Scholar]
- Medina L., Reiner A. Distribution of choline acetyltransferase immunoreactivity in the pigeon brain. J Comp Neurol. 1994 Apr 22;342(4):497–537. doi: 10.1002/cne.903420403. [DOI] [PubMed] [Google Scholar]
- Medina L., Reiner A. Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implications for the evolution of basal ganglia. Brain Behav Evol. 1995;46(4-5):235–258. doi: 10.1159/000113277. [DOI] [PubMed] [Google Scholar]
- Medina L., Reiner A. The efferent projections of the dorsal and ventral pallidal parts of the pigeon basal ganglia, studied with biotinylated dextran amine. Neuroscience. 1997 Dec;81(3):773–802. doi: 10.1016/s0306-4522(97)00204-2. [DOI] [PubMed] [Google Scholar]
- Medina L., Smeets W. J. Comparative aspects of the basal ganglia-tectal pathways in reptiles. J Comp Neurol. 1991 Jun 22;308(4):614–629. doi: 10.1002/cne.903080408. [DOI] [PubMed] [Google Scholar]
- Medina L., Smeets W. J., Hoogland P. V., Puelles L. Distribution of choline acetyltransferase immunoreactivity in the brain of the lizard Gallotia galloti. J Comp Neurol. 1993 May 8;331(2):261–285. doi: 10.1002/cne.903310209. [DOI] [PubMed] [Google Scholar]
- Meredith G. E., Smeets W. J. Immunocytochemical analysis of the dopamine system in the forebrain and midbrain of Raja radiata: evidence for a substantia nigra and ventral tegmental area in cartilaginous fish. J Comp Neurol. 1987 Nov 22;265(4):530–548. doi: 10.1002/cne.902650407. [DOI] [PubMed] [Google Scholar]
- Márin O., Smeets W. J., González A. Basal ganglia organization in amphibians: development of striatal and nucleus accumbens connections with emphasis on the catecholaminergic inputs. J Comp Neurol. 1997 Jul 7;383(3):349–369. doi: 10.1002/(sici)1096-9861(19970707)383:3<349::aid-cne6>3.0.co;2-3. [DOI] [PubMed] [Google Scholar]
- Northcutt R. G., Reiner A., Karten H. J. Immunohistochemical study of the telencephalon of the spiny dogfish, Squalus acanthias. J Comp Neurol. 1988 Nov 8;277(2):250–267. doi: 10.1002/cne.902770207. [DOI] [PubMed] [Google Scholar]
- Parent A., Côté P. Y., Lavoie B. Chemical anatomy of primate basal ganglia. Prog Neurobiol. 1995 Jun;46(2-3):131–197. [PubMed] [Google Scholar]
- Parent A., Hazrati L. N. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev. 1995 Jan;20(1):91–127. doi: 10.1016/0165-0173(94)00007-c. [DOI] [PubMed] [Google Scholar]
- Parent A., Hazrati L. N. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res Brain Res Rev. 1995 Jan;20(1):128–154. doi: 10.1016/0165-0173(94)00008-d. [DOI] [PubMed] [Google Scholar]
- Pombal M. A., El Manira A., Grillner S. Afferents of the lamprey striatum with special reference to the dopaminergic system: a combined tracing and immunohistochemical study. J Comp Neurol. 1997 Sep 15;386(1):71–91. [PubMed] [Google Scholar]
- Puelles L., Kuwana E., Puelles E., Rubenstein J. L. Comparison of the mammalian and avian telencephalon from the perspective of gene expression data. Eur J Morphol. 1999 Apr;37(2-3):139–150. doi: 10.1076/ejom.37.2.139.4756. [DOI] [PubMed] [Google Scholar]
- Puelles L., Rubenstein J. L. Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci. 1993 Nov;16(11):472–479. doi: 10.1016/0166-2236(93)90080-6. [DOI] [PubMed] [Google Scholar]
- Redgrave P., Marrow L., Dean P. Topographical organization of the nigrotectal projection in rat: evidence for segregated channels. Neuroscience. 1992 Oct;50(3):571–595. doi: 10.1016/0306-4522(92)90448-b. [DOI] [PubMed] [Google Scholar]
- Redgrave P., Prescott T. J., Gurney K. The basal ganglia: a vertebrate solution to the selection problem? Neuroscience. 1999;89(4):1009–1023. doi: 10.1016/s0306-4522(98)00319-4. [DOI] [PubMed] [Google Scholar]
- Reiner A., Anderson K. D. The patterns of neurotransmitter and neuropeptide co-occurrence among striatal projection neurons: conclusions based on recent findings. Brain Res Brain Res Rev. 1990 Sep-Dec;15(3):251–265. doi: 10.1016/0165-0173(90)90003-7. [DOI] [PubMed] [Google Scholar]
- Reiner A., Medina L., Haber S. N. The distribution of dynorphinergic terminals in striatal target regions in comparison to the distribution of substance P-containing and enkephalinergic terminals in monkeys and humans. Neuroscience. 1999;88(3):775–793. doi: 10.1016/s0306-4522(98)00254-1. [DOI] [PubMed] [Google Scholar]
- Reiner A., Medina L., Veenman C. L. Structural and functional evolution of the basal ganglia in vertebrates. Brain Res Brain Res Rev. 1998 Dec;28(3):235–285. doi: 10.1016/s0165-0173(98)00016-2. [DOI] [PubMed] [Google Scholar]
- Russchen F. T., Smeets W. J., Hoogland P. V. Histochemical identification of pallidal and striatal structures in the lizard Gekko gecko: evidence for compartmentalization. J Comp Neurol. 1987 Feb 15;256(3):329–341. doi: 10.1002/cne.902560303. [DOI] [PubMed] [Google Scholar]
- Rye D. B., Saper C. B., Lee H. J., Wainer B. H. Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol. 1987 May 22;259(4):483–528. doi: 10.1002/cne.902590403. [DOI] [PubMed] [Google Scholar]
- Smeets W. J., Alonso J. R., González A. Distribution of NADPH-diaphorase and nitric oxide synthase in relation to catecholaminergic neuronal structures in the brain of the lizard Gekko gecko. J Comp Neurol. 1997 Jan 6;377(1):121–141. [PubMed] [Google Scholar]
- Smeets W. J. Comparative aspects of the distribution of substance P and dopamine immunoreactivity in the substantia nigra of amniotes. Brain Behav Evol. 1991;37(3):179–188. doi: 10.1159/000114357. [DOI] [PubMed] [Google Scholar]
- Smeets W. J., Steinbusch H. W. Distribution of noradrenaline immunoreactivity in the forebrain and midbrain of the lizard Gekko gecko. J Comp Neurol. 1989 Jul 22;285(4):453–466. doi: 10.1002/cne.902850404. [DOI] [PubMed] [Google Scholar]
- Smith Y., Bevan M. D., Shink E., Bolam J. P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience. 1998 Sep;86(2):353–387. doi: 10.1016/s0306-4522(98)00004-9. [DOI] [PubMed] [Google Scholar]
- Smith Y., Bolam J. P. Convergence of synaptic inputs from the striatum and the globus pallidus onto identified nigrocollicular cells in the rat: a double anterograde labelling study. Neuroscience. 1991;44(1):45–73. doi: 10.1016/0306-4522(91)90250-r. [DOI] [PubMed] [Google Scholar]
- Smith Y., Bolam J. P. The output neurones and the dopaminergic neurones of the substantia nigra receive a GABA-containing input from the globus pallidus in the rat. J Comp Neurol. 1990 Jun 1;296(1):47–64. doi: 10.1002/cne.902960105. [DOI] [PubMed] [Google Scholar]
- Specht L. A., Pickel V. M., Joh T. H., Reis D. J. Light-microscopic immunocytochemical localization of tyrosine hydroxylase in prenatal rat brain. I. Early ontogeny. J Comp Neurol. 1981 Jun 20;199(2):233–253. doi: 10.1002/cne.901990207. [DOI] [PubMed] [Google Scholar]
- Striedter G. F. The telencephalon of tetrapods in evolution. Brain Behav Evol. 1997;49(4):179–213. doi: 10.1159/000112991. [DOI] [PubMed] [Google Scholar]
- Takakusaki K., Shiroyama T., Yamamoto T., Kitai S. T. Cholinergic and noncholinergic tegmental pedunculopontine projection neurons in rats revealed by intracellular labeling. J Comp Neurol. 1996 Jul 29;371(3):345–361. doi: 10.1002/(SICI)1096-9861(19960729)371:3<345::AID-CNE1>3.0.CO;2-2. [DOI] [PubMed] [Google Scholar]
- Tashiro Y., Sugimoto T., Hattori T., Uemura Y., Nagatsu I., Kikuchi H., Mizuno N. Tyrosine hydroxylase-like immunoreactive neurons in the striatum of the rat. Neurosci Lett. 1989 Feb 13;97(1-2):6–10. doi: 10.1016/0304-3940(89)90130-4. [DOI] [PubMed] [Google Scholar]
- Veenman C. L., Medina L., Reiner A. Avian homologues of mammalian intralaminar, mediodorsal and midline thalamic nuclei: immunohistochemical and hodological evidence. Brain Behav Evol. 1997;49(2):78–98. doi: 10.1159/000112983. [DOI] [PubMed] [Google Scholar]
- Veenman C. L., Reiner A., Honig M. G. Biotinylated dextran amine as an anterograde tracer for single- and double-labeling studies. J Neurosci Methods. 1992 Mar;41(3):239–254. doi: 10.1016/0165-0270(92)90089-v. [DOI] [PubMed] [Google Scholar]
- Vincent S. R., Reiner P. B. The immunohistochemical localization of choline acetyltransferase in the cat brain. Brain Res Bull. 1987 Mar;18(3):371–415. doi: 10.1016/0361-9230(87)90015-3. [DOI] [PubMed] [Google Scholar]
- Wicht H., Northcutt R. G. The forebrain of the Pacific hagfish: a cladistic reconstruction of the ancestral craniate forebrain. Brain Behav Evol. 1992;40(1):25–64. doi: 10.1159/000108540. [DOI] [PubMed] [Google Scholar]
- Woolf N. J. Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol. 1991;37(6):475–524. doi: 10.1016/0301-0082(91)90006-m. [DOI] [PubMed] [Google Scholar]