A cholinergic projection to the rat superior colliculus demonstrated by retrograde transport of horseradish peroxidase and choline acetyltransferase immunohistochemistry

Acetylcholinesterase (AChE) has been localized by histochemistry in the superior colliculus and in the tegmentum of the caudal midbrain and rostral pons of the rat. The pattern of AChE localization in the superior colliculus was characterized by homogeneous staining in the superficial layers and patchlike staining in the intermediate gray layer. In the tegmentum, AChE was localized in the pedunculopontine nucleus (PPN), beginning rostrally at the caudal pole of the substantia nigra and extending caudally to the level of the parabrachial nuclei, and in the lateral dorsal tegmental nucleus (LDTN) of the central gray. The localization of AChE in these nuclei overlapped the distribution of neurons stained by immunohistochemistry using an antibody to choline acetyltransferase (CHAT), the synthesizing enzyme of the neurotransmitter acetylcholine. Other neighboring areas that were stained with AChE, but that did not contain ChAT‐immunoreactive neurons, included the microcellular tegmental nucleus and the ventral tegmental nucleus.

[1]  G. P. Smith,et al.  Efferent connections and nigral afferents of the nucleus accumbens septi in the rat , 1978, Neuroscience.

[2]  A. Graybiel,et al.  A stereometric pattern of distribution of acetylthiocholinesterase in the deep layers of the superior colliculus , 1978, Nature.

[3]  Clifford B. Saper,et al.  Projections of the pedunculopontine tegmental nucleus in the rat: evidence for additional extrapyramidal circuitry , 1982, Brain Research.

[4]  M. E. Anderson,et al.  Axonal branching patterns and location of nigrothalamic and nigrocollicular neurons in the cat. , 1980, Journal of neurophysiology.

[5]  David M. Jacobowitz,et al.  Neurochemical and histochemical studies of the effect of a lesion of the nucleus cuneiformis on the cholinergic innervation of discrete areas of the rat brain , 1979, Brain Research.

[6]  R. M. Beckstead,et al.  The distribution and some morphological features of substantia nigra neurons that project to the thalamus, superior colliculus and pedunculopontine nucleus in the monkey , 1982, Neuroscience.

[7]  H. Groenewegen,et al.  Efferent connections of the dorsal tegmental region in the rat, studied by means of anterograde transport of the lectin Phaseolus vulgaris-leucoagglutinin (PHA-L) , 1984, Brain Research.

[8]  E. Scarnati,et al.  Pedunculopontine-evoked excitation of substantia nigra neurons in the rat , 1984, Brain Research.

[9]  L. Butcher,et al.  Cholinergic systems in the rat brain: II. Projections to the interpeduncular nucleus , 1985, Brain Research Bulletin.

[10]  C. Hammond,et al.  Anatomical and electrophysiological studies on the reciprocal projections between the subthalamic nucleus and nucleus tegmenti pedunculopontinus in the rat , 1983, Neuroscience.

[11]  G. Jones,et al.  Akinesia, hypokinesia, and bradykinesia in the oculomotor system of patients with Parkinson's disease. , 1971, Experimental neurology.

[12]  H. Oka,et al.  Distribution and morphology of tegmental neurons receiving nigral inhibitory inputs in the cat: An intracellular HRP study , 1986, The Journal of comparative neurology.

[13]  H. Nauta,et al.  Efferent projections of the subthalamic nucleus: An autoradiographic study in monkey and cat , 1978, The Journal of comparative neurology.

[14]  P. M. Wilson A photographic perspective on the origins, form, course and relations of the acetylcholinesterase-containing fibres of the dorsal tegmental pathway in the rat brain , 1985, Brain Research Reviews.

[15]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[16]  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.

[17]  S B Edwards,et al.  Microinjector for use in the autoradiographic neuroanatomical tracing method. , 1974, Pharmacology, biochemistry, and behavior.

[18]  A M Graybiel,et al.  Fiber connections of the basal ganglia. , 1979, Progress in brain research.

[19]  S B Edwards,et al.  A comparison of the intranigral distribution of nigrotectal neurons labeled with horseradish peroxidase in the monkey, cat, and rat , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  W. Nauta,et al.  Projections of the lentiform nucleus in the monkey. , 1966, Brain research.

[21]  A. Levey,et al.  Distribution of cholinergic neurons in rat brain: Demonstrated by the immunocytochemical localization of choline acetyltransferase , 1983, The Journal of comparative neurology.

[22]  W. W. Kaelber TREMOR AT REST FROM TEGMENTAL LESIONS IN THE CAT , 1963, Journal of neuropathology and experimental neurology.

[23]  H. Fibiger,et al.  A comparison of the distribution of central cholinergic neurons as demonstrated by acetylcholinesterase pharmacohistochemistry and choline acetyltransferase immunohistochemistry , 1983, Brain Research Bulletin.

[24]  W. Nauta,et al.  Efferent connections of the substantia nigra and ventral tegmental area in the rat , 1979, Brain Research.

[25]  H. Kimura,et al.  The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat , 1981, The Journal of comparative neurology.

[26]  H. Oka,et al.  Nigral inputs to the pedunculopontine region: intracellular analysis , 1984, Brain Research.

[27]  H. Fibiger,et al.  Distribution of central cholinergic neurons in the baboon (papio papio). I. General morphology , 1985, The Journal of comparative neurology.

[28]  Mitsuo Yoshida,et al.  Electrophysiological evidence for branching nigral projections to pontine reticular formation, superior colliculus and thalamus , 1982, Brain Research.

[29]  A. Graybiel A satellite system of the superior colliculus: the parabigeminal nucleus and its projections to the superficial collicular layers , 1978, Brain Research.

[30]  R. Faull,et al.  The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat , 1978, Neuroscience.

[31]  M. Mesulam,et al.  Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6) , 1983, Neuroscience.

[32]  J. Folkerts,et al.  Tremor on stimulation of the midbrain tegmentum. , 1953, Confinia neurologica.

[33]  G. Holstege,et al.  The anatomy of brain stem pathways to the spinal cord in cat. A labeled amino acid tracing study. , 1982, Progress in brain research.

[34]  Jeffrey T. Keller,et al.  Connections of the subthalamic nucleus in the monkey , 1981, Brain Research.

[35]  H. Fibiger,et al.  Distribution of central cholinergic neurons in the baboon (papio papio). II. A topographic atlas correlated with catecholamine neurons , 1985, The Journal of comparative neurology.

[36]  A M Graybiel,et al.  The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus, pars compacta , 1983, The Journal of comparative neurology.

[37]  A. Harvey,et al.  The development of acetylcholinesterase activity in normal and transplanted superior colliculus in rats , 1985, The Journal of comparative neurology.

[38]  A. Graybiel Periodic-compartmental distribution of acetylcholinesterase in the superior colliculus of the human brain , 1979, Neuroscience.

[39]  A. Jackson,et al.  Basal ganglia and other afferent projections to the peribrachial region in the rat: A study using retrograde and anterograde transport of horseradish peroxidase , 1981, Neuroscience.

[40]  C. Shute,et al.  The distribution of cholinesterase in cholinergic neurons demonstrated with the electron microscope. , 1966, Journal of cell science.

[41]  R. M. Beckstead Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes , 1983, Neuroscience.

[42]  B. Jones,et al.  The efferent projections from the reticular formation and the locus coeruleus studied by anterograde and retrograde axonal transport in the rat , 1985, The Journal of comparative neurology.

[43]  R. Lund,et al.  Alterations of the crossed parabigeminotectal projection induced by neonatal eye removal in rats , 1982, The Journal of comparative neurology.

[44]  S. Folstein,et al.  Abnormal ocular motor control in Huntington's disease , 1983, Neurology.

[45]  W. A. McGovern,et al.  A Study in Experimental Tremor (Part 1 of 2) , 1962 .

[46]  E. Kawana,et al.  Efferent projections of the parabigeminal nucleus in rats: A horseradish peroxidase (HRP) study , 1979, Brain Research.

[47]  A. C. Cuello,et al.  Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry , 1985, Brain Research.

[48]  L. Butcher,et al.  Cholinergic systems in the rat brain: I. Projections to the limbic telencephalon , 1984, Brain Research Bulletin.

[49]  A K Moschovakis,et al.  Nigral inhibitory termination on efferent neurons of the superior colliculus: An intracellular horseradish peroxidase study in the cat , 1985, The Journal of comparative neurology.

[50]  R. Tomlinson,et al.  Ocular motor deficits in Parkinson's disease. II. Control of the saccadic and smooth pursuit systems. , 1983, Brain : a journal of neurology.

[51]  D. Mash,et al.  Cholinergic projections from the parabigeminal nucleus (Ch8) to the superior colliculus in the mouse: a combined analysis of horseradish peroxidase transport and choline acetyltransferase immunohistochemistry , 1986, Brain Research.

[52]  A. Parent,et al.  The subcortical afferents to caudate nucleus and putamen in primate: A fluorescence retrograde double labeling study , 1983, Neuroscience.

[53]  David A. Hopkins,et al.  Substantia nigra projections to the reticular formation, superior colliculus and central gray in the rat, cat and monkey , 1976, Neuroscience Letters.

[54]  S. Sugita,et al.  The organization of neurons in the nucleus of the lateral lemniscus projecting to the superior and inferior colliculi in the rat , 1985, Brain Research.

[55]  A. Hodgson,et al.  Acetylcholinesterase hydrolyzes substance P , 1980, Neuroscience.

[56]  H. Karten,et al.  Cluster-and-sheet pattern of enkephalin-like immunoreactivity in the superior colliculus of the cat , 1984, Neuroscience.

[57]  C. Shute,et al.  The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. , 1967, Brain : a journal of neurology.

[58]  A. Parent,et al.  Distribution of Acetylcholinesterase-Containing Neurons in the Basal Forebrain and Upper Brainstem of the Squirrel Monkey (Saimiri sciureus) , 1984, Brain Research Bulletin.

[59]  B. Stein,et al.  Sources of subcortical projections to the superior colliculus in the cat , 1979, The Journal of comparative neurology.

[60]  M. Carpenter,et al.  Projections of the globus pallidus and adjacent structures: An autoradiographic study in the monkey , 1976, The Journal of comparative neurology.

[61]  D. A. Godfrey,et al.  Distributions of choline acetyltransferase and acetylcholinesterase activities in layers of rat superior colliculus. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[62]  A. Jackson,et al.  Subthalamic projection to nucleus tegmenti pedunculopontinus in the rat , 1981, Neuroscience Letters.

[63]  Paul R. Martin,et al.  Subcortical projections to lateral geniculate and thalamic reticular nuclei in the hooded rat , 1983, The Journal of comparative neurology.

[64]  A M Graybiel,et al.  Direct and indirect preoculomotor pathways of the brainstem: An autoradiographic study of the pontine reticular formation in the cat , 1977, The Journal of comparative neurology.

[65]  T. Hattori,et al.  Organization and efferent projections of nucleus tegmenti pedunculopontinus pars compacta with special reference to its cholinergic aspects , 1984, Neuroscience.

[66]  H. Thoenen,et al.  Production of specific antisera and monoclonal antibodies to choline acetyltransferase: characterization and use for identification of cholinergic neurons. , 1982, The EMBO journal.

[67]  A. Graybiel,et al.  Convergence of afferents from frontal cortex and substantia nigra onto acetylcholinesterase-rich patches of the cat's superior colliculus , 1985, Neuroscience.

[68]  J. K. Harting,et al.  The Mammalian Superior Colliculus: Studies of Its Morphology and Connections , 1984 .

[69]  A. Hodgson,et al.  The enkephalins are amongst the peptides hydrolyzed by purified acetylcholinesterase , 1983, Neuroscience.

[70]  M. Carpenter,et al.  Interconnections and organization of pallidal and subthalamic nucleus neurons in the monkey , 1981, The Journal of comparative neurology.

[71]  M. Mesulam,et al.  Atlas of cholinergic neurons in the forebrain and upper brainstem of the macaque based on monoclonal choline acetyltransferase immunohistochemistry and acetylcholinesterase histochemistry , 1984, Neuroscience.

[72]  L. Poirier Experimental and histological study of midbrain dyskinesias. , 1960, Journal of neurophysiology.

[73]  R. Wurtz,et al.  Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. , 1985, Journal of neurophysiology.