Structural and functional evolution of the basal ganglia in vertebrates
Identifieur interne : 001448 ( Istex/Corpus ); précédent : 001447; suivant : 001449Structural and functional evolution of the basal ganglia in vertebrates
Auteurs : Anton Reiner ; Loreta Medina ; C. Leo VeenmanSource :
- Brain Research Reviews [ 0165-0173 ] ; 1998.
Abstract
While a basal ganglia with striatal and pallidal subdivisions is1 Although by its structure the word basal ganglia is plural, the basal ganglia is typically regarded as a single entity. Thus, in the same sense that the structurally plural `United States' is treated as a singular noun, we here treat basal ganglia as a singular noun.1 clearly present in many extant anamniote species, this basal ganglia is cell sparse and receives only a relatively modest tegmental dopaminergic input and little if any cortical input. The major basal ganglia influence on motor functions in anamniotes appears to be exerted via output circuits to the tectum. In contrast, in modern mammals, birds, and reptiles (i.e., modern amniotes), the striatal and pallidal parts of the basal ganglia are very neuron-rich, both consist of the same basic populations of neurons in all amniotes, and the striatum receives abundant tegmental dopaminergic and cortical input. The functional circuitry of the basal ganglia also seems very similar in all amniotes, since the major basal ganglia influences on motor functions appear to be exerted via output circuits to both cerebral cortex and tectum in sauropsids (i.e., birds and reptiles) and mammals. The basal ganglia, output circuits to the cortex, however, appear to be considerably more developed in mammals than in birds and reptiles. The basal ganglia, thus, appears to have undergone a major elaboration during the evolutionary transition from amphibians to reptiles. This elaboration may have enabled amniotes to learn and/or execute a more sophisticated repertoire of behaviors and movements, and this ability may have been an important element of the successful adaptation of amniotes to a fully terrestrial habitat. The mammalian lineage appears, however, to have diverged somewhat from the sauropsid lineage with respect to the emergence of the cerebral cortex as the major target of the basal ganglia circuitry devoted to executing the basal ganglia-mediated control of movement.
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DOI: 10.1016/S0165-0173(98)00016-2
Links to Exploration step
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<front><div type="abstract" xml:lang="en">While a basal ganglia with striatal and pallidal subdivisions is1 Although by its structure the word basal ganglia is plural, the basal ganglia is typically regarded as a single entity. Thus, in the same sense that the structurally plural `United States' is treated as a singular noun, we here treat basal ganglia as a singular noun.1 clearly present in many extant anamniote species, this basal ganglia is cell sparse and receives only a relatively modest tegmental dopaminergic input and little if any cortical input. The major basal ganglia influence on motor functions in anamniotes appears to be exerted via output circuits to the tectum. In contrast, in modern mammals, birds, and reptiles (i.e., modern amniotes), the striatal and pallidal parts of the basal ganglia are very neuron-rich, both consist of the same basic populations of neurons in all amniotes, and the striatum receives abundant tegmental dopaminergic and cortical input. The functional circuitry of the basal ganglia also seems very similar in all amniotes, since the major basal ganglia influences on motor functions appear to be exerted via output circuits to both cerebral cortex and tectum in sauropsids (i.e., birds and reptiles) and mammals. The basal ganglia, output circuits to the cortex, however, appear to be considerably more developed in mammals than in birds and reptiles. The basal ganglia, thus, appears to have undergone a major elaboration during the evolutionary transition from amphibians to reptiles. This elaboration may have enabled amniotes to learn and/or execute a more sophisticated repertoire of behaviors and movements, and this ability may have been an important element of the successful adaptation of amniotes to a fully terrestrial habitat. The mammalian lineage appears, however, to have diverged somewhat from the sauropsid lineage with respect to the emergence of the cerebral cortex as the major target of the basal ganglia circuitry devoted to executing the basal ganglia-mediated control of movement.</div>
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<notesStmt><note type="content">Section title: Full-length review</note>
<note type="content">Fig. 1: Circuit diagram illustrating the basic functional organization of basal ganglia circuitry in mammals [6, 105, 136]. The pluses and minuses indicate whether the specific projections of the basal ganglia circuitry are excitatory (+) or inhibitory (−). See text for more details. Abbreviations: D1—D1 type dopamine receptor; D2—D2 type dopamine receptor; ENK—enkephalinergic neurons; GPL—lateral globus pallidus; GPM—medial globus pallidus; SNr—substantia nigra pars reticulata; SP—substance P-containing neurons; STN—subthalamic nucleus; TeO—optic tectum; VA/VL—ventral anterior and ventral lateral thalamic nuclei.</note>
<note type="content">Fig. 2: Schematics of frontal sections through the basal ganglia of the right telencephalic hemisphere in representative species from the three amniote classes, a rat (mammal), a pigeon (bird), and turtle (reptile). The basal ganglia in all three consists of a striatum and a pallidum and is located in the central and/or basal telencephalon, beneath the cortical regions. See text for more details. Abbreviations: AC—anterior commissure; DVR—dorsal ventricular ridge; OC—optic chiasm.</note>
<note type="content">Fig. 3: (A and B) Photomicrographs of frontal sections through the basal ganglia of one telencephalic hemisphere in a turtle (A) and a pigeon (B) that had been immunohistochemically stained for substance P (SP). Note the intense SP immunoreactivity in the ventrolateral wall of the telencephalon that defines the region of the striatum (Str). This region is rich in SP+ immunoreactivity due to the presence of numerous SP+ neurons and their processes. (C and D) Photomicrographs of frontal sections through rostral (C) and caudal (D) levels of rat basal ganglia of one telencephalic hemisphere that were immunohistochemically stained for tyrosine hydroxylase. Tyrosine hydroxylase (TH) is the rate limiting enzyme for catecholamine synthesis, and in the basal ganglia it is mainly localized to DA+ fibers. The intense TH immunoreactivity in the dorsal striatum (Str) and the nucleus accumbens (Acc) and olfactory tubercle (TuOl) of the ventral striatum is due to the presence of numerous DA+ fibers and varicosities. Note that only light TH immunoreactivity is present in globus pallidus (GP). Medial is to the left and dorsal to the top in all four photomicrographs. Other abbreviations: Ctx—cortex; DVR—dorsal ventricular ridge. Scale bar: A–D=1 mm.</note>
<note type="content">Fig. 4: (A and B) Photomicrographs of frontal sections through the lateral pallidal segment of one telencephalic hemisphere in rat (i.e., globus pallidus or GP) immunohistochemically labeled for enkephalin (ENK) (A) and the medial pallidal segment of one telencephalic hemisphere in rat (i.e., entopeduncular nucleus or EP) immunohistochemically stained for SP (B). Note the intense ENK+ and SP+ innervation in the GP and EP, respectively. (C and D) Photomicrographs of adjacent, frontal sections through the ventral tegmental area (VTA) and substantia nigra (SN) on one side of the midbrain in rat, immunohistochemically stained for either tyrosine hydroxylase (TH) (C), the rate limiting enzyme of catecholamine synthesis that is uniquely abundant in DA+ neurons and processes, or SP (D), respectively. Note the densely-packed DA+ cells in the VTA and SN pars compacta (SNc) (C), and the dense SP+ innervation in the SN pars reticulata (SNr) (D). The VTA and SNc show a somewhat more moderate SP+ innervation. (E) Photomicrograph of a frontal section through the VTA and SN on one side of the midbrain in a crocodile that was immunohistochemically stained for TH. Note that the DA+ cells in the crocodile SN (E) are more widely dispersed than in the rat SN (C). Medial is to the left and dorsal to the top in (A–E). (F) Photomicrograph of a frontal section through the VTA and SN of both sides of the tegmentum in a pigeon with a unilateral knife cut on the left side of the fiber bundle carrying basal ganglia descending fibers to the tegmentum. This section has been immunohistochemically stained for SP. Note the marked decrease in SP+ innervation in the VTA and SN on the basal ganglia-deafferented side (arrow), compared to the normal, strong SP+ innervation observed on the contralateral, intact side. Dorsal is to the top in (F). Scale bars: A–E=200 μm (scale in E); F=1 mm.</note>
<note type="content">Fig. 5: Schematics of frontal sections through the basal ganglia of the right telencephalic hemisphere in representative species from three anamniote classes, a frog (amphibia), a lungfish (a crossopterygian bony fish), a shark (cartilaginous fish), and a polypterid ray-finned fish (an actinopterygian bony fish). The basal ganglia in all three groups with an evaginated telencephalon (frog, lungfish and shark) consists of a striatum and a pallidum and is located in the basal telencephalon, beneath the cortical regions. While a striatum is evident in the ventral uneverted part of the telencephalon in ray-finned fish, a pallidum is not well-defined. Medial is to the left and dorsal to the top in all schematized sections. See text for more details.</note>
<note type="content">Fig. 6: (A) Low magnification photomicrograph of a frontal section through the basal part of one telencephalic hemisphere of a frog, immunohistochemically stained for ENK. Note the intense ENK immunoreactivity in the basal telencephalon, which includes the striatal (Str) part of the basal ganglia. (B and D) High magnification photomicrographs of frontal sections through the basal ganglia of one telencephalic hemisphere in frog, immunohistochemically stained for either ENK (B) or SP (D). Note the presence of ENK+ and SP+ perikarya and processes in the striatum (Str), and the dense innervation. (C) Photomicrograph of a frontal section through the posterior tubercle region (PT) on the right side of the midbrain of a frog, immunohistochemically stained for TH to visualize DA+ neurons. The DA+ neurons of the PT are the major source of the DA+ innervation of the striatum in amphibians, and are comparable to the DA+ neurons of the amniote ventral tegmental area and substantia nigra. Abbreviations: PT—posterior tubercle; Sep—septum. Scale bar: A=200 μm; B–D=100 μm (scale in B).</note>
<note type="content">Fig. 7: (A) Photomicrograph of a frontal section through both telencephalic hemispheres of an African lungfish, immunohistochemically stained for SP. Note the intense SP immunoreactivity in the basal lateral telencephalon due to the presence of numerous SP+ cells and processes, which serves to identify the striatal part of the basal ganglia. (B) Photomicrograph of a frontal section through the midbrain tegmentum of an African lungfish that was immunohistochemically stained for SP. Note the intense SP+ innervation in the regions comparable to the amniote ventral tegmental area and substantia nigra (VTA/SN). This prominent SP+ innervation seems to arise from SP+ neurons of the striatum. Abbreviations: P—pallium; Str—striatum; SN—substantia nigra; VTA—ventral tegmental area. Scale bar: A=500 μm; B=100 μm.</note>
<note type="content">Fig. 8: Cladogram depicting the evolutionary history of the striatal (STR) and pallidal (PALL) parts of the basal ganglia. The demonstrated presence (+) or absence (−) of a striatum and pallidum is depicted for the major vertebrate groups. Neither a striatum nor a pallidum has unequivocally been shown to be absent in any vertebrate group, though the presence of a pallidum is uncertain (?) in ray-finned fish, and the presence of both is uncertain in hagfish. Batoids is a collective term for skates and rays, and the abbreviation `amphib' denotes amphibians. The most likely interpretation of the data shown is that a striatum was present as of the common ancestor of jawed and jawless vertebrates, and a pallidum was present at least as early as the common ancestor of bony and cartilaginous fish.</note>
<note type="content">Fig. 9: (A) Schematic sagittal view of a generalized amniote basal ganglia and tegmentum showing the neuronal populations of the striatum and pallidum that are common to all amniotes and their chemical characteristics. (B) Schematic sagittal section of a generalized anamniote basal ganglia and tegmentum showing the neuronal populations of the striatum and pallidum that appear to be common to all anamniotes and their known chemical characteristics. Dynorphin has not been demonstrated in striatal projection neurons in anamniote striatum, and SS/NPY-containing interneurons and GABA/LANT6/parvalbumin-containing interneurons have not been found in anamniote striatum. CHAT+ interneurons also have not been commonly observed in anamniote striatum. NOS+ neurons have, however, been observed in amphibian striatum and in bony fish ventral striatum. Abbreviations: CHAT—choline acetyltransferase; DYN—dynorphin; ENK—enkephalin; NOS—nitric oxide synthase; NPY—neuropeptide Y; PARV—parvalbumin; SP—substance P; SS—somatostatin; VTA/SN—ventral tegmental area and substantia nigra.</note>
<note type="content">Fig. 10: Schematics of frontal sections through the tegmental dopaminergic cell field of the right side of the midbrain in representative species from three amniote classes, a rat (mammal), a pigeon (bird), and a turtle (reptile), and three anamniote classes, a shark (cartilaginous fish), a polypterid ray-finned fish (bony fish), and a frog (amphibia). In all groups, tegmental dopaminergic neurons projecting to the striatum are present. See text for more details. Medial is to the left and dorsal to the top in all schematically rendered sections. Abbreviations: nIII—oculomotor nerve; OC—optic chiasm; OM—oculomotor nucleus; PT—posterior tubercle; SN—substantia nigra; TeO—optic tectum; VTA—ventral tegmental area.</note>
<note type="content">Fig. 11: Schematics of sagittal sections through the tegmental dopaminergic cell field of representative species from three amniote classes, a rat (mammal), a pigeon (bird), and a lizard (reptile), and three anamniote classes, a shark (cartilaginous fish), a ray-finned fish (bony fish), and a frog (amphibia). In all groups, tegmental dopaminergic neurons projecting to the striatum are present and span one or more caudal diencephalic and/or midbrain neuromeres. Diencephalic and midbrain neuromeres are identified as in Refs. [337, 338]. See text for more details. Abbreviations: Cb—cerebellum; Is—isthmic neuromere; M—mesencephalic neuromere; OC—optic chiasm; P1—first prosomere; P2—second prosomere; P3—third prosomere; SN—substantia nigra; TEL—telencephalon; VTA—ventral tegmental area.</note>
<note type="content">Fig. 12: Schematic illustrations of transverse sections through the right hemisphere of pigeon telencephalon showing the location of the striatum and its major sources of cortical input. The striatum is shaded in black and it receives input from the striped area along the outer rind of the pallium. This pallial region includes the hyperstriatum accessorium (HA) region of the Wulst, the pallium externum (PE) of the dorsolateral pallium, and the archistriatum (ARCH) of the posterior basal pallium. The sections are in a rostrocaudal series (A–C), and medial is to the left and dorsal to the top in all three. Other abbreviations: Dien—diencephalon; DVR—dorsal ventricular ridge; Hp—hippocampal complex; PP—paleostriatum primitivum; S—septum.</note>
<note type="content">Fig. 13: Schematics of sagittal sections through the brains of a mammal and a sauropsid (i.e., bird or reptile), showing the basic connections involved in the output circuitry of the basal ganglia to the telencephalic `cortex' in either amniote group. While data is only available for the above pallido-thalamo-cortical circuitry in mammals and birds, we hypothesize that similar circuitry may be present in reptiles. Abbreviations: DTZ—avian and reptilian dorsal thalamic zone; GPL—lateral pallidal segment; GPM—medial pallidal segment; INTR—mammalian midline-intralaminar nuclei; NCP—nucleus of the posterior commissure in reptiles and mammals, and lateral spiriform nucleus in birds; OC—optic chiasm; SP—substance P-containing neurons; VA/VL—ventral anterior/ventral lateral thalamic nuclei of mammals; VIA—ventrointermediate thalamic area of birds; VTA/SN—ventral tegmental area and substantia nigra.</note>
<note type="content">Fig. 14: Schematics of hypothesized sagittal sections through the brain of an early amphibian and the brain of an early reptile, showing the evolutionary change that occurred in the basic inputs to the striatal part of the basal ganglia at the anamniote–amniote transition. The conclusions are inferred from the phyletic distribution of basal ganglia traits in living vertebrate species. The basal ganglia in the anamniotes ancestral to amniotes likely received sensory input via the dorsal thalamus (DORSAL THAL), and must have been reciprocally connected with the DA+ neurons of the posterior tubercle region (PT), which is comparable to the amniote ventral tegmental area and substantia nigra (VTA/SN). The cortical input and dorsal thalamic intralaminar input to the striatum were likely to be absent or sparse in ancestral anamniotes and have evolved in ancestral amniotes. Other abbreviations: Mot—motor thalamus; PRET—pretectum; PT—posterior tubercle; Sen—sensory thalamus.</note>
<note type="content">Fig. 15: Schematics of sagittal sections through the brains of a mammal and a sauropsid (i.e., bird or reptile), showing the basic connections involved in the output circuitry of the basal ganglia to the midbrain tectum in either amniote group. Data are available to support the above circuitry in mammals, birds and reptiles. See text for further details. Abbreviations: DTZ—avian and reptilian dorsal thalamic zone; ENK—enkephalinergic neurons; GPL—lateral pallidal segment; GPM—medial pallidal segment; INTR—mammalian midline-intralaminar nuclei; NCP—nucleus of the posterior commissure in reptiles and mammals, and lateral spiriform nucleus in birds; OC—optic chiasm; SP—substance P-containing neurons; VA/VL—ventral anterior/ventral lateral thalamic area of mammals; VIA—ventrointermediate thalamic area of birds; VTA/SN—ventral tegmental area and substantia nigra.</note>
<note type="content">Fig. 16: Schematic illustrations of transverse sections through the pigeon diencephalon (A), pretectum (B), and midbrain (C) of the right side of the brain illustrating the output fibers of the avian pallidum within the ansa lenticularis (AL) and its major projection targets, the anterior nucleus of the ansa lenticularis (ALa), the ventrointermediate thalamic area (VIA), the dorsointermediate posterior thalamic area (DIP), the posterior nucleus of the ansa lenticularis (ALp), the lateral spiriform nucleus (SpL), and the reticulata part of the substantia nigra (SN). All pallidal projection targets are stippled, while the AL itself is crosshatched. The numbers below each drawing represent the anterior–posterior level of the section in the stereotaxic coordinates of the atlas of the pigeon brain by Karten and Hodos [201]. Medial is to the left and dorsal to the top in all schematized sections. Other abbreviations: APH—parahippocampal area; Cb—cerebellum; CO—optic chiasm; CPi—piriform cortex; DTZ—dorsal thalamic zone; EW—nucleus of Edinger–Westphal; FPL—lateral forebrain bundle; GCt—central gray; GLv—ventral geniculate nucleus; Hb—habenula; Hp—hippocampus; Hy—hypothalamus; Imc—nucleus isthmi pars magnocellularis; IP—interpeduncular nucleus; Ipc—nucleus isthmi pars parvocellularis; MLd—nucleus mesencephali lateralis pars dorsalis; nBOR—nucleus of the basal optic root; OM—oculomotor nucleus; PL—lateral pontine nucleus; PT—nucleus pretectalis; QF—quintofrontal tract; RSd—dorsal thalamic reticular nucleus; Rt—nucleus rotundus; SGC—stratum griseum centrale of the tectum; SGF—stratum griseum et fibrosum of the tectum; SO—stratum opticum of the tectum; SP—nucleus subpretectalis; SpM—medial spiriform nucleus; Tn—taenia; TO—optic tract; TU—tuberal region of hypothalamus; V—ventricle; VTA—ventral tegmental area.</note>
<note type="content">Fig. 17: Schematics of hypothesized sagittal sections through the brains of an early amphibian and an early reptile, showing the change that occurred in the basic output circuitry of the basal ganglia at the anamniote–amniote transition. The conclusions are inferred from the phyletic distribution of basal ganglia traits in living vertebrate species. The basal ganglia pathways to the tectum via the pretectum and via the ventral tegmental area/substantia nigra (VTA/SN) were likely to have been present in ancestral tetrapods, and were retained in the ancestral amniotes, as well as in living amphibians, reptiles and birds. In addition to the projections to the pretectum and tegmentum, the basal ganglia of ancestral tetrapods probably projected to the subthalamus, as they appear to in modern amphibians and amniotes. A basal ganglia pathway to a somatosensory/somatomotor cortical area via the dorsal thalamus (DORSAL THAL) seems to have evolved during the anamniote–amniote transition. Abbreviations: Mot—motor thalamus; PRET—pretectum; PT—posterior tubercle; Sen—sensory thalamus.</note>
<note type="content">Fig. 18: Circuit diagram of the functional organization of the basal ganglia in birds. The pluses and minuses indicate whether the specific projections of the basal ganglia circuitry use an excitatory (+) or inhibitory (−) neurotransmitter. The characteristic transmitter used by the neuron type of each connection is also shown. In mammals and birds, the striatal and pallidal output circuitry appears organized into direct SP+ striatal outputs to pallidal neurons promoting movement and ENK+ striatal outputs to pallidal neurons inhibiting unwanted movement. The latter pallidal neurons have direct outputs to the targets of the SP+ striatal neurons (i.e., GPM, SNr and SpL) and indirect outputs to these same targets via ALa (i.e., the subthalamic nucleus of birds). Because neurons of the ENK+ pathway indirectly project to the same targets as neurons of SP+ pathways, the ENK pathway has been called the indirect pathway in mammals. In mammals, SP+ neurons target two populations of pallidal type neurons (GPM and SNr), while in birds three are targeted (GPM, SNr and SpL). It is not yet certain, however, for birds whether ALa projections and GPL type pallidal projection neurons (i.e., receiving ENK input) specifically target GPM type neurons (i.e., receiving SP input) within the pallidum. See text for more details. Abbreviations: ALa—anterior nucleus of the ansa lenticularis; GLUT—glutamate; GPL—lateral globus pallidus; GPM—medial globus pallidus; SNr—substantia nigra pars reticulata; SpL—nucleus spiriformis lateralis; TeO—optic tectum; VIA—ventrointermediate thalamic area.</note>
<note type="content">Fig. 19: Schematics of sagittal sections through the brains of an adult rat and chicken illustrating the comparable location of the subthalamic nucleus of mammals (STN) and its homologue in birds, the anterior nucleus of the ansa lenticularis (ALa). The location of various forebrain and midbrain cell groups is shown with respect to the neuromeric boundaries identified in Refs. [337, 338]. The line of separation between the alar and basal plate is also shown. In this framework, the forebrain is divided into six prosomeres (p1–6) and one mesomere (m), with the first prosomere (p1) abutting the rostral part of the mesomere. Other abbreviations: ac—anterior commissure; Cb—cerebellum; CC—corpus callosum; DORSAL THAL—dorsal thalamus; FR—fasciculus retroflexus; Hb—habenula; IC—inferior colliculus; IIIm—oculomotor nerve; IP—interpeduncular nucleus; IVm—trochlear nerve; mam—mammillary region; oc—optic chiasm; OB—olfactory bulb; pc—posterior commissure; pt—pretectum; rm—retromammillary region; SC—superior colliculus; Sep—septum; TeO—optic tectum; Tu—tuberal hypothalamic region; VEN THAL—ventral thalamus; VMH—ventromedial hypothalamus.</note>
<note type="content">Fig. 20: Schematics of sagittal sections through the brains of a late sauropsid (e.g., bird) and an early mammal, showing the evolutionary changes in the major output circuitry of the basal ganglia that occurred during the sauropsid–mammal transition. The conclusions are inferred from the phyletic distribution of basal ganglia traits in living vertebrate species. The basal ganglia pathways to the tectum via the pretectum and via the ventral tegmental area/substantia nigra (VTA/SN) were likely present in ancestral tetrapods, and were retained in the ancestral amniotes, as well as living reptiles and birds. The circuit to the pretectum appears to have been de-emphasized in the mammalian lineage, while the pallido-thalamic-motor cortex circuit appears to have been elaborated. The latter circuit is present in birds and we believe is likely to have been present in ancestral reptiles as well. Abbreviations: DORSAL THAL—dorsal thalamus; GPL—lateral pallidal segment; GPM—medial pallidal segment; Mot—motor thalamus; PRET—pretectum; Sen—sensory thalamus.</note>
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<author xml:id="author-3"><persName><forename type="first">C.Leo</forename>
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<abstract xml:lang="en"><p>While a basal ganglia with striatal and pallidal subdivisions is1 Although by its structure the word basal ganglia is plural, the basal ganglia is typically regarded as a single entity. Thus, in the same sense that the structurally plural `United States' is treated as a singular noun, we here treat basal ganglia as a singular noun.1 clearly present in many extant anamniote species, this basal ganglia is cell sparse and receives only a relatively modest tegmental dopaminergic input and little if any cortical input. The major basal ganglia influence on motor functions in anamniotes appears to be exerted via output circuits to the tectum. In contrast, in modern mammals, birds, and reptiles (i.e., modern amniotes), the striatal and pallidal parts of the basal ganglia are very neuron-rich, both consist of the same basic populations of neurons in all amniotes, and the striatum receives abundant tegmental dopaminergic and cortical input. The functional circuitry of the basal ganglia also seems very similar in all amniotes, since the major basal ganglia influences on motor functions appear to be exerted via output circuits to both cerebral cortex and tectum in sauropsids (i.e., birds and reptiles) and mammals. The basal ganglia, output circuits to the cortex, however, appear to be considerably more developed in mammals than in birds and reptiles. The basal ganglia, thus, appears to have undergone a major elaboration during the evolutionary transition from amphibians to reptiles. This elaboration may have enabled amniotes to learn and/or execute a more sophisticated repertoire of behaviors and movements, and this ability may have been an important element of the successful adaptation of amniotes to a fully terrestrial habitat. The mammalian lineage appears, however, to have diverged somewhat from the sauropsid lineage with respect to the emergence of the cerebral cortex as the major target of the basal ganglia circuitry devoted to executing the basal ganglia-mediated control of movement.</p>
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<item><term>Striatum</term>
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<head><ce:dochead><ce:textfn>Full-length review</ce:textfn>
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<ce:textfn>Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee—Memphis, 855 Monroe Avenue, Memphis, TN 38163, USA</ce:textfn>
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<ce:textfn>Department of Morphological Sciences, Facultad de Medicina, Universidad de Murcia, Campus de Espinardo, Murcia 30100, Spain</ce:textfn>
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<ce:abstract-sec><ce:simple-para>While a basal ganglia with striatal and pallidal subdivisions is<ce:footnote id="FN1"><ce:label>1</ce:label>
<ce:note-para>Although by its structure the word basal ganglia is plural, the basal ganglia is typically regarded as a single entity. Thus, in the same sense that the structurally plural `United States' is treated as a singular noun, we here treat basal ganglia as a singular noun.</ce:note-para>
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clearly present in many extant anamniote species, this basal ganglia is cell sparse and receives only a relatively modest tegmental dopaminergic input and little if any cortical input. The major basal ganglia influence on motor functions in anamniotes appears to be exerted via output circuits to the tectum. In contrast, in modern mammals, birds, and reptiles (i.e., modern amniotes), the striatal and pallidal parts of the basal ganglia are very neuron-rich, both consist of the same basic populations of neurons in all amniotes, and the striatum receives abundant tegmental dopaminergic and cortical input. The functional circuitry of the basal ganglia also seems very similar in all amniotes, since the major basal ganglia influences on motor functions appear to be exerted via output circuits to both cerebral cortex and tectum in sauropsids (i.e., birds and reptiles) and mammals. The basal ganglia, output circuits to the cortex, however, appear to be considerably more developed in mammals than in birds and reptiles. The basal ganglia, thus, appears to have undergone a major elaboration during the evolutionary transition from amphibians to reptiles. This elaboration may have enabled amniotes to learn and/or execute a more sophisticated repertoire of behaviors and movements, and this ability may have been an important element of the successful adaptation of amniotes to a fully terrestrial habitat. The mammalian lineage appears, however, to have diverged somewhat from the sauropsid lineage with respect to the emergence of the cerebral cortex as the major target of the basal ganglia circuitry devoted to executing the basal ganglia-mediated control of movement.</ce:simple-para>
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<ce:keywords class="keyword"><ce:section-title>Keywords</ce:section-title>
<ce:keyword><ce:text>Striatum</ce:text>
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<ce:keyword><ce:text>Pallidum</ce:text>
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<ce:keyword><ce:text>Substantia nigra</ce:text>
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<ce:keyword><ce:text>Segmental development</ce:text>
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<ce:keyword><ce:text>Evolution</ce:text>
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<abstract lang="en">While a basal ganglia with striatal and pallidal subdivisions is1 Although by its structure the word basal ganglia is plural, the basal ganglia is typically regarded as a single entity. Thus, in the same sense that the structurally plural `United States' is treated as a singular noun, we here treat basal ganglia as a singular noun.1 clearly present in many extant anamniote species, this basal ganglia is cell sparse and receives only a relatively modest tegmental dopaminergic input and little if any cortical input. The major basal ganglia influence on motor functions in anamniotes appears to be exerted via output circuits to the tectum. In contrast, in modern mammals, birds, and reptiles (i.e., modern amniotes), the striatal and pallidal parts of the basal ganglia are very neuron-rich, both consist of the same basic populations of neurons in all amniotes, and the striatum receives abundant tegmental dopaminergic and cortical input. The functional circuitry of the basal ganglia also seems very similar in all amniotes, since the major basal ganglia influences on motor functions appear to be exerted via output circuits to both cerebral cortex and tectum in sauropsids (i.e., birds and reptiles) and mammals. The basal ganglia, output circuits to the cortex, however, appear to be considerably more developed in mammals than in birds and reptiles. The basal ganglia, thus, appears to have undergone a major elaboration during the evolutionary transition from amphibians to reptiles. This elaboration may have enabled amniotes to learn and/or execute a more sophisticated repertoire of behaviors and movements, and this ability may have been an important element of the successful adaptation of amniotes to a fully terrestrial habitat. The mammalian lineage appears, however, to have diverged somewhat from the sauropsid lineage with respect to the emergence of the cerebral cortex as the major target of the basal ganglia circuitry devoted to executing the basal ganglia-mediated control of movement.</abstract>
<note type="content">Section title: Full-length review</note>
<note type="content">Fig. 1: Circuit diagram illustrating the basic functional organization of basal ganglia circuitry in mammals [6, 105, 136]. The pluses and minuses indicate whether the specific projections of the basal ganglia circuitry are excitatory (+) or inhibitory (−). See text for more details. Abbreviations: D1—D1 type dopamine receptor; D2—D2 type dopamine receptor; ENK—enkephalinergic neurons; GPL—lateral globus pallidus; GPM—medial globus pallidus; SNr—substantia nigra pars reticulata; SP—substance P-containing neurons; STN—subthalamic nucleus; TeO—optic tectum; VA/VL—ventral anterior and ventral lateral thalamic nuclei.</note>
<note type="content">Fig. 2: Schematics of frontal sections through the basal ganglia of the right telencephalic hemisphere in representative species from the three amniote classes, a rat (mammal), a pigeon (bird), and turtle (reptile). The basal ganglia in all three consists of a striatum and a pallidum and is located in the central and/or basal telencephalon, beneath the cortical regions. See text for more details. Abbreviations: AC—anterior commissure; DVR—dorsal ventricular ridge; OC—optic chiasm.</note>
<note type="content">Fig. 3: (A and B) Photomicrographs of frontal sections through the basal ganglia of one telencephalic hemisphere in a turtle (A) and a pigeon (B) that had been immunohistochemically stained for substance P (SP). Note the intense SP immunoreactivity in the ventrolateral wall of the telencephalon that defines the region of the striatum (Str). This region is rich in SP+ immunoreactivity due to the presence of numerous SP+ neurons and their processes. (C and D) Photomicrographs of frontal sections through rostral (C) and caudal (D) levels of rat basal ganglia of one telencephalic hemisphere that were immunohistochemically stained for tyrosine hydroxylase. Tyrosine hydroxylase (TH) is the rate limiting enzyme for catecholamine synthesis, and in the basal ganglia it is mainly localized to DA+ fibers. The intense TH immunoreactivity in the dorsal striatum (Str) and the nucleus accumbens (Acc) and olfactory tubercle (TuOl) of the ventral striatum is due to the presence of numerous DA+ fibers and varicosities. Note that only light TH immunoreactivity is present in globus pallidus (GP). Medial is to the left and dorsal to the top in all four photomicrographs. Other abbreviations: Ctx—cortex; DVR—dorsal ventricular ridge. Scale bar: A–D=1 mm.</note>
<note type="content">Fig. 4: (A and B) Photomicrographs of frontal sections through the lateral pallidal segment of one telencephalic hemisphere in rat (i.e., globus pallidus or GP) immunohistochemically labeled for enkephalin (ENK) (A) and the medial pallidal segment of one telencephalic hemisphere in rat (i.e., entopeduncular nucleus or EP) immunohistochemically stained for SP (B). Note the intense ENK+ and SP+ innervation in the GP and EP, respectively. (C and D) Photomicrographs of adjacent, frontal sections through the ventral tegmental area (VTA) and substantia nigra (SN) on one side of the midbrain in rat, immunohistochemically stained for either tyrosine hydroxylase (TH) (C), the rate limiting enzyme of catecholamine synthesis that is uniquely abundant in DA+ neurons and processes, or SP (D), respectively. Note the densely-packed DA+ cells in the VTA and SN pars compacta (SNc) (C), and the dense SP+ innervation in the SN pars reticulata (SNr) (D). The VTA and SNc show a somewhat more moderate SP+ innervation. (E) Photomicrograph of a frontal section through the VTA and SN on one side of the midbrain in a crocodile that was immunohistochemically stained for TH. Note that the DA+ cells in the crocodile SN (E) are more widely dispersed than in the rat SN (C). Medial is to the left and dorsal to the top in (A–E). (F) Photomicrograph of a frontal section through the VTA and SN of both sides of the tegmentum in a pigeon with a unilateral knife cut on the left side of the fiber bundle carrying basal ganglia descending fibers to the tegmentum. This section has been immunohistochemically stained for SP. Note the marked decrease in SP+ innervation in the VTA and SN on the basal ganglia-deafferented side (arrow), compared to the normal, strong SP+ innervation observed on the contralateral, intact side. Dorsal is to the top in (F). Scale bars: A–E=200 μm (scale in E); F=1 mm.</note>
<note type="content">Fig. 5: Schematics of frontal sections through the basal ganglia of the right telencephalic hemisphere in representative species from three anamniote classes, a frog (amphibia), a lungfish (a crossopterygian bony fish), a shark (cartilaginous fish), and a polypterid ray-finned fish (an actinopterygian bony fish). The basal ganglia in all three groups with an evaginated telencephalon (frog, lungfish and shark) consists of a striatum and a pallidum and is located in the basal telencephalon, beneath the cortical regions. While a striatum is evident in the ventral uneverted part of the telencephalon in ray-finned fish, a pallidum is not well-defined. Medial is to the left and dorsal to the top in all schematized sections. See text for more details.</note>
<note type="content">Fig. 6: (A) Low magnification photomicrograph of a frontal section through the basal part of one telencephalic hemisphere of a frog, immunohistochemically stained for ENK. Note the intense ENK immunoreactivity in the basal telencephalon, which includes the striatal (Str) part of the basal ganglia. (B and D) High magnification photomicrographs of frontal sections through the basal ganglia of one telencephalic hemisphere in frog, immunohistochemically stained for either ENK (B) or SP (D). Note the presence of ENK+ and SP+ perikarya and processes in the striatum (Str), and the dense innervation. (C) Photomicrograph of a frontal section through the posterior tubercle region (PT) on the right side of the midbrain of a frog, immunohistochemically stained for TH to visualize DA+ neurons. The DA+ neurons of the PT are the major source of the DA+ innervation of the striatum in amphibians, and are comparable to the DA+ neurons of the amniote ventral tegmental area and substantia nigra. Abbreviations: PT—posterior tubercle; Sep—septum. Scale bar: A=200 μm; B–D=100 μm (scale in B).</note>
<note type="content">Fig. 7: (A) Photomicrograph of a frontal section through both telencephalic hemispheres of an African lungfish, immunohistochemically stained for SP. Note the intense SP immunoreactivity in the basal lateral telencephalon due to the presence of numerous SP+ cells and processes, which serves to identify the striatal part of the basal ganglia. (B) Photomicrograph of a frontal section through the midbrain tegmentum of an African lungfish that was immunohistochemically stained for SP. Note the intense SP+ innervation in the regions comparable to the amniote ventral tegmental area and substantia nigra (VTA/SN). This prominent SP+ innervation seems to arise from SP+ neurons of the striatum. Abbreviations: P—pallium; Str—striatum; SN—substantia nigra; VTA—ventral tegmental area. Scale bar: A=500 μm; B=100 μm.</note>
<note type="content">Fig. 8: Cladogram depicting the evolutionary history of the striatal (STR) and pallidal (PALL) parts of the basal ganglia. The demonstrated presence (+) or absence (−) of a striatum and pallidum is depicted for the major vertebrate groups. Neither a striatum nor a pallidum has unequivocally been shown to be absent in any vertebrate group, though the presence of a pallidum is uncertain (?) in ray-finned fish, and the presence of both is uncertain in hagfish. Batoids is a collective term for skates and rays, and the abbreviation `amphib' denotes amphibians. The most likely interpretation of the data shown is that a striatum was present as of the common ancestor of jawed and jawless vertebrates, and a pallidum was present at least as early as the common ancestor of bony and cartilaginous fish.</note>
<note type="content">Fig. 9: (A) Schematic sagittal view of a generalized amniote basal ganglia and tegmentum showing the neuronal populations of the striatum and pallidum that are common to all amniotes and their chemical characteristics. (B) Schematic sagittal section of a generalized anamniote basal ganglia and tegmentum showing the neuronal populations of the striatum and pallidum that appear to be common to all anamniotes and their known chemical characteristics. Dynorphin has not been demonstrated in striatal projection neurons in anamniote striatum, and SS/NPY-containing interneurons and GABA/LANT6/parvalbumin-containing interneurons have not been found in anamniote striatum. CHAT+ interneurons also have not been commonly observed in anamniote striatum. NOS+ neurons have, however, been observed in amphibian striatum and in bony fish ventral striatum. Abbreviations: CHAT—choline acetyltransferase; DYN—dynorphin; ENK—enkephalin; NOS—nitric oxide synthase; NPY—neuropeptide Y; PARV—parvalbumin; SP—substance P; SS—somatostatin; VTA/SN—ventral tegmental area and substantia nigra.</note>
<note type="content">Fig. 10: Schematics of frontal sections through the tegmental dopaminergic cell field of the right side of the midbrain in representative species from three amniote classes, a rat (mammal), a pigeon (bird), and a turtle (reptile), and three anamniote classes, a shark (cartilaginous fish), a polypterid ray-finned fish (bony fish), and a frog (amphibia). In all groups, tegmental dopaminergic neurons projecting to the striatum are present. See text for more details. Medial is to the left and dorsal to the top in all schematically rendered sections. Abbreviations: nIII—oculomotor nerve; OC—optic chiasm; OM—oculomotor nucleus; PT—posterior tubercle; SN—substantia nigra; TeO—optic tectum; VTA—ventral tegmental area.</note>
<note type="content">Fig. 11: Schematics of sagittal sections through the tegmental dopaminergic cell field of representative species from three amniote classes, a rat (mammal), a pigeon (bird), and a lizard (reptile), and three anamniote classes, a shark (cartilaginous fish), a ray-finned fish (bony fish), and a frog (amphibia). In all groups, tegmental dopaminergic neurons projecting to the striatum are present and span one or more caudal diencephalic and/or midbrain neuromeres. Diencephalic and midbrain neuromeres are identified as in Refs. [337, 338]. See text for more details. Abbreviations: Cb—cerebellum; Is—isthmic neuromere; M—mesencephalic neuromere; OC—optic chiasm; P1—first prosomere; P2—second prosomere; P3—third prosomere; SN—substantia nigra; TEL—telencephalon; VTA—ventral tegmental area.</note>
<note type="content">Fig. 12: Schematic illustrations of transverse sections through the right hemisphere of pigeon telencephalon showing the location of the striatum and its major sources of cortical input. The striatum is shaded in black and it receives input from the striped area along the outer rind of the pallium. This pallial region includes the hyperstriatum accessorium (HA) region of the Wulst, the pallium externum (PE) of the dorsolateral pallium, and the archistriatum (ARCH) of the posterior basal pallium. The sections are in a rostrocaudal series (A–C), and medial is to the left and dorsal to the top in all three. Other abbreviations: Dien—diencephalon; DVR—dorsal ventricular ridge; Hp—hippocampal complex; PP—paleostriatum primitivum; S—septum.</note>
<note type="content">Fig. 13: Schematics of sagittal sections through the brains of a mammal and a sauropsid (i.e., bird or reptile), showing the basic connections involved in the output circuitry of the basal ganglia to the telencephalic `cortex' in either amniote group. While data is only available for the above pallido-thalamo-cortical circuitry in mammals and birds, we hypothesize that similar circuitry may be present in reptiles. Abbreviations: DTZ—avian and reptilian dorsal thalamic zone; GPL—lateral pallidal segment; GPM—medial pallidal segment; INTR—mammalian midline-intralaminar nuclei; NCP—nucleus of the posterior commissure in reptiles and mammals, and lateral spiriform nucleus in birds; OC—optic chiasm; SP—substance P-containing neurons; VA/VL—ventral anterior/ventral lateral thalamic nuclei of mammals; VIA—ventrointermediate thalamic area of birds; VTA/SN—ventral tegmental area and substantia nigra.</note>
<note type="content">Fig. 14: Schematics of hypothesized sagittal sections through the brain of an early amphibian and the brain of an early reptile, showing the evolutionary change that occurred in the basic inputs to the striatal part of the basal ganglia at the anamniote–amniote transition. The conclusions are inferred from the phyletic distribution of basal ganglia traits in living vertebrate species. The basal ganglia in the anamniotes ancestral to amniotes likely received sensory input via the dorsal thalamus (DORSAL THAL), and must have been reciprocally connected with the DA+ neurons of the posterior tubercle region (PT), which is comparable to the amniote ventral tegmental area and substantia nigra (VTA/SN). The cortical input and dorsal thalamic intralaminar input to the striatum were likely to be absent or sparse in ancestral anamniotes and have evolved in ancestral amniotes. Other abbreviations: Mot—motor thalamus; PRET—pretectum; PT—posterior tubercle; Sen—sensory thalamus.</note>
<note type="content">Fig. 15: Schematics of sagittal sections through the brains of a mammal and a sauropsid (i.e., bird or reptile), showing the basic connections involved in the output circuitry of the basal ganglia to the midbrain tectum in either amniote group. Data are available to support the above circuitry in mammals, birds and reptiles. See text for further details. Abbreviations: DTZ—avian and reptilian dorsal thalamic zone; ENK—enkephalinergic neurons; GPL—lateral pallidal segment; GPM—medial pallidal segment; INTR—mammalian midline-intralaminar nuclei; NCP—nucleus of the posterior commissure in reptiles and mammals, and lateral spiriform nucleus in birds; OC—optic chiasm; SP—substance P-containing neurons; VA/VL—ventral anterior/ventral lateral thalamic area of mammals; VIA—ventrointermediate thalamic area of birds; VTA/SN—ventral tegmental area and substantia nigra.</note>
<note type="content">Fig. 16: Schematic illustrations of transverse sections through the pigeon diencephalon (A), pretectum (B), and midbrain (C) of the right side of the brain illustrating the output fibers of the avian pallidum within the ansa lenticularis (AL) and its major projection targets, the anterior nucleus of the ansa lenticularis (ALa), the ventrointermediate thalamic area (VIA), the dorsointermediate posterior thalamic area (DIP), the posterior nucleus of the ansa lenticularis (ALp), the lateral spiriform nucleus (SpL), and the reticulata part of the substantia nigra (SN). All pallidal projection targets are stippled, while the AL itself is crosshatched. The numbers below each drawing represent the anterior–posterior level of the section in the stereotaxic coordinates of the atlas of the pigeon brain by Karten and Hodos [201]. Medial is to the left and dorsal to the top in all schematized sections. Other abbreviations: APH—parahippocampal area; Cb—cerebellum; CO—optic chiasm; CPi—piriform cortex; DTZ—dorsal thalamic zone; EW—nucleus of Edinger–Westphal; FPL—lateral forebrain bundle; GCt—central gray; GLv—ventral geniculate nucleus; Hb—habenula; Hp—hippocampus; Hy—hypothalamus; Imc—nucleus isthmi pars magnocellularis; IP—interpeduncular nucleus; Ipc—nucleus isthmi pars parvocellularis; MLd—nucleus mesencephali lateralis pars dorsalis; nBOR—nucleus of the basal optic root; OM—oculomotor nucleus; PL—lateral pontine nucleus; PT—nucleus pretectalis; QF—quintofrontal tract; RSd—dorsal thalamic reticular nucleus; Rt—nucleus rotundus; SGC—stratum griseum centrale of the tectum; SGF—stratum griseum et fibrosum of the tectum; SO—stratum opticum of the tectum; SP—nucleus subpretectalis; SpM—medial spiriform nucleus; Tn—taenia; TO—optic tract; TU—tuberal region of hypothalamus; V—ventricle; VTA—ventral tegmental area.</note>
<note type="content">Fig. 17: Schematics of hypothesized sagittal sections through the brains of an early amphibian and an early reptile, showing the change that occurred in the basic output circuitry of the basal ganglia at the anamniote–amniote transition. The conclusions are inferred from the phyletic distribution of basal ganglia traits in living vertebrate species. The basal ganglia pathways to the tectum via the pretectum and via the ventral tegmental area/substantia nigra (VTA/SN) were likely to have been present in ancestral tetrapods, and were retained in the ancestral amniotes, as well as in living amphibians, reptiles and birds. In addition to the projections to the pretectum and tegmentum, the basal ganglia of ancestral tetrapods probably projected to the subthalamus, as they appear to in modern amphibians and amniotes. A basal ganglia pathway to a somatosensory/somatomotor cortical area via the dorsal thalamus (DORSAL THAL) seems to have evolved during the anamniote–amniote transition. Abbreviations: Mot—motor thalamus; PRET—pretectum; PT—posterior tubercle; Sen—sensory thalamus.</note>
<note type="content">Fig. 18: Circuit diagram of the functional organization of the basal ganglia in birds. The pluses and minuses indicate whether the specific projections of the basal ganglia circuitry use an excitatory (+) or inhibitory (−) neurotransmitter. The characteristic transmitter used by the neuron type of each connection is also shown. In mammals and birds, the striatal and pallidal output circuitry appears organized into direct SP+ striatal outputs to pallidal neurons promoting movement and ENK+ striatal outputs to pallidal neurons inhibiting unwanted movement. The latter pallidal neurons have direct outputs to the targets of the SP+ striatal neurons (i.e., GPM, SNr and SpL) and indirect outputs to these same targets via ALa (i.e., the subthalamic nucleus of birds). Because neurons of the ENK+ pathway indirectly project to the same targets as neurons of SP+ pathways, the ENK pathway has been called the indirect pathway in mammals. In mammals, SP+ neurons target two populations of pallidal type neurons (GPM and SNr), while in birds three are targeted (GPM, SNr and SpL). It is not yet certain, however, for birds whether ALa projections and GPL type pallidal projection neurons (i.e., receiving ENK input) specifically target GPM type neurons (i.e., receiving SP input) within the pallidum. See text for more details. Abbreviations: ALa—anterior nucleus of the ansa lenticularis; GLUT—glutamate; GPL—lateral globus pallidus; GPM—medial globus pallidus; SNr—substantia nigra pars reticulata; SpL—nucleus spiriformis lateralis; TeO—optic tectum; VIA—ventrointermediate thalamic area.</note>
<note type="content">Fig. 19: Schematics of sagittal sections through the brains of an adult rat and chicken illustrating the comparable location of the subthalamic nucleus of mammals (STN) and its homologue in birds, the anterior nucleus of the ansa lenticularis (ALa). The location of various forebrain and midbrain cell groups is shown with respect to the neuromeric boundaries identified in Refs. [337, 338]. The line of separation between the alar and basal plate is also shown. In this framework, the forebrain is divided into six prosomeres (p1–6) and one mesomere (m), with the first prosomere (p1) abutting the rostral part of the mesomere. Other abbreviations: ac—anterior commissure; Cb—cerebellum; CC—corpus callosum; DORSAL THAL—dorsal thalamus; FR—fasciculus retroflexus; Hb—habenula; IC—inferior colliculus; IIIm—oculomotor nerve; IP—interpeduncular nucleus; IVm—trochlear nerve; mam—mammillary region; oc—optic chiasm; OB—olfactory bulb; pc—posterior commissure; pt—pretectum; rm—retromammillary region; SC—superior colliculus; Sep—septum; TeO—optic tectum; Tu—tuberal hypothalamic region; VEN THAL—ventral thalamus; VMH—ventromedial hypothalamus.</note>
<note type="content">Fig. 20: Schematics of sagittal sections through the brains of a late sauropsid (e.g., bird) and an early mammal, showing the evolutionary changes in the major output circuitry of the basal ganglia that occurred during the sauropsid–mammal transition. The conclusions are inferred from the phyletic distribution of basal ganglia traits in living vertebrate species. The basal ganglia pathways to the tectum via the pretectum and via the ventral tegmental area/substantia nigra (VTA/SN) were likely present in ancestral tetrapods, and were retained in the ancestral amniotes, as well as living reptiles and birds. The circuit to the pretectum appears to have been de-emphasized in the mammalian lineage, while the pallido-thalamic-motor cortex circuit appears to have been elaborated. The latter circuit is present in birds and we believe is likely to have been present in ancestral reptiles as well. Abbreviations: DORSAL THAL—dorsal thalamus; GPL—lateral pallidal segment; GPM—medial pallidal segment; Mot—motor thalamus; PRET—pretectum; Sen—sensory thalamus.</note>
<subject><genre>Keywords</genre>
<topic>Striatum</topic>
<topic>Pallidum</topic>
<topic>Substantia nigra</topic>
<topic>Intralaminar nucleus</topic>
<topic>Ventral tier</topic>
<topic>Motor function</topic>
<topic>Segmental development</topic>
<topic>Evolution</topic>
<topic>Neurotransmitter</topic>
</subject>
<relatedItem type="host"><titleInfo><title>Brain Research Reviews</title>
</titleInfo>
<titleInfo type="abbreviated"><title>BRESR</title>
</titleInfo>
<genre type="journal">journal</genre>
<originInfo><dateIssued encoding="w3cdtf">199812</dateIssued>
</originInfo>
<identifier type="ISSN">0165-0173</identifier>
<identifier type="PII">S0165-0173(00)X0022-7</identifier>
<part><date>199812</date>
<detail type="volume"><number>28</number>
<caption>vol.</caption>
</detail>
<detail type="issue"><number>3</number>
<caption>no.</caption>
</detail>
<extent unit="issue pages"><start>235</start>
<end>492</end>
</extent>
<extent unit="pages"><start>235</start>
<end>285</end>
</extent>
</part>
</relatedItem>
<identifier type="istex">1394EA848F8616A1188E7035CF0E5450CB125F3C</identifier>
<identifier type="DOI">10.1016/S0165-0173(98)00016-2</identifier>
<identifier type="PII">S0165-0173(98)00016-2</identifier>
<accessCondition type="use and reproduction" contentType="copyright">©1998 Elsevier Science B.V.</accessCondition>
<recordInfo><recordContentSource>ELSEVIER</recordContentSource>
<recordOrigin>Elsevier Science B.V., ©1998</recordOrigin>
</recordInfo>
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