Rostral Wulst in passerine birds. I. Origin, course, and terminations of an avian pyramidal tract

An avian “pyramidal tract” was defined in zebra finches and green finches by making injections of neuronal tracers into the hyperstriatum accessorium (HA) of the rostral Wulst. Extratelencephalic projections of rostral HA traveled in the septomesencephalic tract (TSM) and gave rise to nuclear‐specific terminal fields in the precerebellar medial spiriform nucleus of the posterior thalamus, the red nucleus in the mesencephalon, the medial pontine nucleus in the pons, and the subtrigeminal, external cuneate, cuneate, gracile, and inferior olivary nuclei in the medulla. Extensive but more diffuse terminal fields were also present in the stratum cellulare externum of the posterior hypothalamus, the central periaqueductal gray, the prerubral field, and the lateral and ventrolateral tegmentum of the pons and medulla. There was also a sparse projection to the dorsal thalamic nucleus intermedius ventralis anterior, which supplies the somatosensory input to the rostral Wulst, and distinct projections to the intercollicular region surrounding the central nucleus of the inferior colliculus, where they partly overlapped the projections of the dorsal column nuclei. Projections from HA to the cerebellum via the TSM are described separately. In the brainstem the ventral ramus of TSM was situated ventral to the medial lemniscus at the base of the brain, entered the spinal cord in the inner margin of the lateral funiculus, predominantly ipsilaterally, and terminated bilaterally but predominantly contralaterally in the medial part of the base of the dorsal horn of the upper six or seven cervical segments. After injections of tracers into putative targets, numerous retrogradely labeled cells were found in the rostral HA, predominantly ventrally. The results confirm the presence of a major descending fiber system in passerine birds that resembles in its brainstem course and several of its terminations the pyramidal tract of mammals. The reciprocal projections of HA with the hypothalamus suggest that rostral HA may also incorporate neuronal components that in mammals would be considered parts of prefrontal cortex. J. Comp. Neurol. 416:429–450, 2000.

[1]  R. Nudo,et al.  Descending pathways to the spinal cord: A comparative study of 22 mammals , 1988, The Journal of comparative neurology.

[2]  J. Tepper,et al.  The shell region of the nucleus ovoidalis: A subdivision of the avian auditory thalamus , 1992, The Journal of comparative neurology.

[3]  J. Wild,et al.  Organization of afferent and efferent projections of the nucleus basalis prosencephali in a passerine, Taeniopygia guttata , 1996, The Journal of comparative neurology.

[4]  J. Wild,et al.  The avian somatosensory system: connections of regions of body representation in the forebrain of the pigeon , 1987, Brain Research.

[5]  J. Dubbeldam,et al.  The central projections of the glossopharyngeal and vagus ganglia in the mallard, Anas platyrhynchos L. , 1979, The Journal of comparative neurology.

[6]  A. Reiner,et al.  Avian homologues of mammalian intralaminar, mediodorsal and midline thalamic nuclei: immunohistochemical and hodological evidence. , 1997, Brain, behavior and evolution.

[7]  E. Dietrichs,et al.  The organization of hypothalamocerebellar cortical fibers in the squirrel monkey (Saimiri sciureus) , 1986, The Journal of comparative neurology.

[8]  J. Wild The avian somatosensory system: The pathway from wing to Wulst in a passerine (Chloris chloris) , 1997, Brain Research.

[9]  J. Dubbeldam,et al.  The efferent connections of the nuclei of the descending trigeminal tract in the mallard (Anas platyrhynchos L.) , 1984, Neuroscience.

[10]  F. Magni,et al.  A direct connection between visual Wulst and Tectum opticum in the pigeon (Columba livia) demonstrated by horseradish peroxidase. , 1980, Archives italiennes de biologie.

[11]  L. Akker An anatomical outline of the spinal cord of the pigeon , 1970 .

[12]  J. Dubbeldam,et al.  Organization and efferent connections of the archistriatum of the mallard, Anas platyrhynchos L.: An anterograde and retrograde tracing study , 1997, The Journal of comparative neurology.

[13]  A. D. Smith,et al.  A simple and rapid method for the production of cholera B-chain coupled to horseradish peroxidase for neuronal tracing , 1988, Journal of Neuroscience Methods.

[14]  M L Berk,et al.  Projections of the lateral hypothalamus and bed nucleus of the stria terminalis to the dorsal vagal complex in the pigeon , 1987, The Journal of comparative neurology.

[15]  J. Wild,et al.  Convergence of somatosensory and auditory projections in the avian torus semicircularis, including the central auditory nucleus , 1995, The Journal of comparative neurology.

[16]  C. Kappers,et al.  The comparative anatomy of the nervous system of vertebrates, including man , 1936 .

[17]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[18]  A. Revzin,et al.  A specific visual projection area in the hyperstriatum of the pigeon (Columba livia). , 1969, Brain research.

[19]  J. Steeves,et al.  Origins of brainstem‐spinal projections in the duck and goose , 1988, The Journal of comparative neurology.

[20]  J. Wild The avian somatosensory system. I. Primary spinal afferent input to the spinal cord and brainstem in the pigeon (Columba livia) , 1985, The Journal of comparative neurology.

[21]  E. Korzeniewska Multisensory convergence in the thalamus of the pigeon (Columba livia) , 1987, Neuroscience Letters.

[22]  J. Wild,et al.  Rostral wulst of passerine birds: II. Intratelencephalic projections to nuclei associated with the auditory and song systems , 1999, The Journal of comparative neurology.

[23]  J. Rio,et al.  Efferent projections of the visual Wulst upon the nucleus of the basal optic root in the pigeon , 1983, Brain Research.

[24]  O. Kalischer Das Grosshirn der Papageien : in Anatomischer und Physiologischer Beziehung , 1905 .

[25]  R. Oppenheim,et al.  Novel sources of descending input to the spinal cord of the hatchling chick , 1985, The Journal of comparative neurology.

[26]  H. Bischof,et al.  Afferent connections of the ectostriatum and visual wulst in the zebra finch (Taeniopygia guttata castanotis Gould) — an HRP study , 1982, Brain Research.

[27]  S. Hardy Anatomical data supporting the concept of prefrontal influences upon hypothalamo-medullary relays in the rat , 1994, Neuroscience Letters.

[28]  Harvey J. Karten,et al.  THE ORGANIZATION OF THE AVIAN TELENCEPHALON AND SOME SPECULATIONS ON THE PHYLOGENY OF THE AMNIOTE TELENCEPHALON * , 1969 .

[29]  A. Reiner,et al.  Evidence for a possible avian dorsal thalamic region comparable to the mammalian ventral anterior, ventral lateral, and oral ventroposterolateral nuclei , 1997, The Journal of comparative neurology.

[30]  N. J. Adamo Connections of efferent fibers from hyperstriatal areas in chicken, raven, and African lovebird , 1967 .

[31]  A. Butler,et al.  Efferent projections of the medial preoptic nucleus and medial hypothalamus in the pigeon , 1981, The Journal of comparative neurology.

[32]  C. S. S.,et al.  The Comparative Anatomy of the Nervous System of Vertebrates, including Man , 1937, Nature.

[33]  H. Karten,et al.  A direct thalamo-cerebellar pathway in pigeon and catfish , 1976, Brain Research.

[34]  G. E. Vates,et al.  Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taenopygia guttata) , 1996, The Journal of comparative neurology.

[35]  J. Pettigrew,et al.  The distribution of neurons projecting from the retina and visual cortex to the thalamus and tectum opticum of the barn owl, Tyto alba, and the burrowing owl, Speotyto cunicularia , 1981, The Journal of comparative neurology.

[36]  Harvey J. Karten,et al.  The laminar source of efferent projections from the avian Wulst , 1983, Brain Research.

[37]  R. Oppenheim,et al.  Axonal projections and synaptogenesis by supraspinal descending neurons in the spinal cord of the chick embryo , 1991, The Journal of comparative neurology.

[38]  H. Karten,et al.  Intratelencephalic projections of the visual wulst in pigeons (Columba livia) , 1995, The Journal of comparative neurology.

[39]  W. Nauta,et al.  A General Profile of the Vertebrate Brain, with Sidelights on the Ancestry of Cerebral Cortex , 1970 .

[40]  M. Wiesendanger,et al.  Corticomotoneuronal connections in the rat: Evidence from double‐labeling of motoneurons and corticospinal axon arborizations , 1991, The Journal of comparative neurology.

[41]  H. Karten,et al.  The Origins of Neocortex: Connections and Lamination as Distinct Events in Evolution , 1989, Journal of Cognitive Neuroscience.

[42]  H Zeier,et al.  The archistriatum of the pigeon: organization of afferent and efferent connections. , 1971, Brain research.

[43]  C. Bagley CORTICAL MOTOR MECHANISM OF THE SHEEP BRAIN , 1922 .

[44]  J. Wild,et al.  Central projections and somatotopic organisation of trigeminal primary afferents in pigeon (Columba livia) , 1996, The Journal of comparative neurology.

[45]  E. Crosby,et al.  The nuclei and fiber paths of the avian diencephalon, with consideration of telencephalic and certain mesencephalic centers and connections , 1929 .

[46]  H. Künzle,et al.  Efferents from the lateral frontal cortex to spinomedullary target areas, trigeminal nuclei, and spinally projecting brainstem regions in the hedgehog tenrec , 1996, The Journal of comparative neurology.

[47]  H. Karten,et al.  Origin, course and terminations of the rubrospinal tract in the pigeon (Columba livia) , 1979, The Journal of comparative neurology.

[48]  J. Wild Avian somatosensory system: II. Ascending projections of the dorsal column and external cuneate nuclei in the pigeon , 1989, The Journal of comparative neurology.

[49]  J. Wild,et al.  Telencephalic connections of the trigeminal system in the pigeon (Columba livia): A trigeminal sensorimotor circuit , 1985, The Journal of comparative neurology.

[50]  J. Delius,et al.  Cutaneous sensory projections to the avian forebrain. , 1972, Brain research.

[51]  Tanemichi Chiba,et al.  Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study , 1991, Brain Research.

[52]  I. Divac,et al.  Dopaminergic innervation of the brain in pigeons. The presumed 'prefrontal cortex'. , 1994, Acta neurobiologiae experimentalis.

[53]  W Hodos,et al.  Neural connections of the “visual wulst” of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia) , 1973, The Journal of comparative neurology.

[54]  J. Wild Direct and indirect “cortico”‐rubral and rubro‐cerebellar cortical projections in the pigeon , 1992, The Journal of comparative neurology.

[55]  W. Verhaart The non‐crossing of the pyramidal tract in procavia capensis (storr) and other instances of absence of the pyramidal crossing , 1967 .

[56]  H. Zeigler,et al.  Organization of the cerebellum in the pigeon (Columba livia): II. Projections of the cerebellar nuclei , 1991, The Journal of comparative neurology.

[57]  A. Reiner,et al.  Avian bulbospinal pathways: anterograde and retrograde studies of cells of origin, funicular trajectories and laminar terminations. , 1982, Progress in brain research.

[58]  O. W. Henson,et al.  The descending auditory pathway and acousticomotor systems: connections with the inferior colliculus , 1990, Brain Research Reviews.

[59]  W. Verhaart,et al.  Cortical projections to brain stem and spinal cord in the goat by way of the pyramidal tract and the bundle of Bagley , 1967 .

[60]  J. Repérant,et al.  Extratelencephalic projections of the avian visual Wulst. A quantitative autoradiographic study in the pigeon Columbia livia. , 1987, Journal fur Hirnforschung.

[61]  J. Price,et al.  Prefrontal cortical projections to the hypothalamus in Macaque monkeys , 1998, The Journal of comparative neurology.

[62]  I. Divac,et al.  Cortical area in the rat that mediates visual pattern discrimination. , 1994, Acta neurobiologiae experimentalis.

[63]  J. Pettigrew,et al.  Origins of descending spinal pathways in prehensile birds: do parrots have a homologue to the corticospinal tract of mammals? , 1990, Brain, behavior and evolution.

[64]  G. Palmieri,et al.  The pyramidal tract of the hedgehog (Erinaceus europaeus) and its relationship with the olfactory bulb. , 1993, Archives italiennes de biologie.

[65]  H. Karten,et al.  The trigeminal system in the pigeon (Columba livia) I. Projections of the Gasserian ganglion , 1978, The Journal of comparative neurology.

[66]  J. Wild,et al.  Visual and somatosensory inputs to the avian song system via nucleus uvaeformis (Uva) and a comparison with the projections of a similar thalamic nucleus in a nonsongbird, columbia livia , 1994, The Journal of comparative neurology.

[67]  Fernando Nottebohm,et al.  Descending auditory pathways in the adult male zebra finch (Taeniopygia Guttata) , 1998, The Journal of comparative neurology.

[68]  J. Jansen,et al.  Experimental demonstration of a pontine homologue in birds , 1950 .

[69]  F. Nottebohm,et al.  The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates , 1974, The Journal of comparative neurology.

[70]  H. Karten,et al.  Connections of the auditory forebrain in the pigeon (columba livia) , 1993, The Journal of comparative neurology.

[71]  J. Armand,et al.  The origin, course and terminations of corticospinal fibers in various mammals. , 1982, Progress in brain research.

[72]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.