Morphology of globus pallidus neurons: Its correlation with electrophysiology in guinea pig brain slices

Intracellular recordings obtained from globus pallidus neurons in guinea pig revealed, on the basis of their membrane properties, the existence of at least two major (types I and II) and one minor (type III) groups of neurons. Type I neurons were silent at the resting membrane level and generated a burst of spikes with strong accommodation to depolarizing current injection. Type II neurons fired at the resting membrane level or with small membrane depolarization, and their repetitive firing (≤200 Hz) was very sensitive to the amplitude of injected current and showed weak accomodation. Type III neurons did not fire spontaneously at the resting membrane level. These neurons were morphologically characterized by intracellular injection of biocytin following the electrophysiological recordings. Among the major groups, the soma size of type I neurons (40 × 23 μm) was larger than that of type II neurons (29 × 17 μm). Both types of neurons had three to six primary dendrites. Dendritic spines were very sparse. Occasionally, dendrites exhibited varicosities, especially in their terminal branches. Dendritic fields were disc‐like in shape and were perpendicular to striopallidal fibers. Most of the axons had intranuclear collaterals. Main axonal branches projected rostrally or caudally, and in some neurons one axonal branch could be followed caudally, and another rostrally, into the striatum. These two types were major neurons in the globus pallidus and were considered to be projection neurons. Type III neurons were small (18 × 12 μm), and their dendrites were covered with numerous spines. They were considered to be interneurons. J. Comp. Neurol. 377:85‐94, 1997. © 1997 Wiley‐Liss, Inc.

[1]  J. Rafols,et al.  The primate globus pallidus: a Golgi and electron microscopic study. , 1974, Journal fur Hirnforschung.

[2]  H. Kita,et al.  Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation , 1991, Brain Research.

[3]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

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

[5]  G. Percheron,et al.  A Golgi analysis of the primate globus pallidus. I. Inconstant processes of large neurons, other neuronal types, and afferent axons , 1984, The Journal of comparative neurology.

[6]  A. Alonso,et al.  Differential Oscillatory Properties of Cholinergic and Non‐cholinergic Nucleus Basalis Neurons in Guinea Pig Brain Slice , 1996, The European journal of neuroscience.

[7]  A. Parent,et al.  Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus) , 1986, Neuroscience.

[8]  A. Parent,et al.  Projection from the external pallidum to the reticular thalamic nucleus in the squirrel monkey , 1991, Brain Research.

[9]  G. Percheron,et al.  A Golgi analysis of the primate globus pallidus. III. Spatial organization of the striato‐pallidal complex , 1984, The Journal of comparative neurology.

[10]  P Pasik,et al.  A Golgi and ultrastructural study of the monkey globus pallidus , 1982, The Journal of comparative neurology.

[11]  George R. Marshall,et al.  Afferents to the rat substantia nigra studied with horseradish peroxidase, with special reference to fibres from the subthalamic nucleus , 1976, Brain Research.

[12]  H. Kita,et al.  Parvalbumin-immunopositive neurons in rat globus pallidus: a light and electron microscopic study , 1994, Brain Research.

[13]  A. Parent,et al.  Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidium in basal ganglia circuitry , 1995, Brain Research Reviews.

[14]  K. Berkley Spatial relationships between the terminations of somatic sensory motor pathways in the rostral brainstem of cats and monkeys. II. Cerebellar projections compared with those of the ascending somatic sensory pathways in lateral diencephalon , 1983, The Journal of comparative neurology.

[15]  K. Horikawa,et al.  A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates , 1988, Journal of Neuroscience Methods.

[16]  Robert M. Beckstead,et al.  A pallidostriatal projection in the cat and monkey , 1983, Brain Research Bulletin.

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

[18]  L. Tremblay,et al.  Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism , 1991, Brain Research.

[19]  N. A. Buchwald,et al.  Branched projections of pallidal and peripallidal neurons to neocortex and neostriatum: a double-labeling study in the cat , 1985, Brain Research.

[20]  A. Nambu,et al.  The distribution of the globus pallidus neurons with input from various cortical areas in the monkeys , 1993, Brain Research.

[21]  M. Mesulam,et al.  Cortical projections arising from the basal forebrain: A study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase , 1984, Neuroscience.

[22]  M. Delong,et al.  Activity of pallidal neurons during movement. , 1971, Journal of neurophysiology.

[23]  M. Delong,et al.  Activity of identified wrist-related pallidal neurons during step and ramp wrist movements in the monkey. , 1990, Journal of neurophysiology.

[24]  N. Rajakumar,et al.  The pallidostriatal projection in the rat: a recurrent inhibitory loop? , 1994, Brain Research.

[25]  J. Penney,et al.  Evidence for a projection from the globus pallidus to the entopeduncular nucleus in the rat , 1991, Neuroscience Letters.

[26]  A. Parent,et al.  Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop , 1995, Brain Research Reviews.

[27]  C. Wilson,et al.  Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  B. Bunney,et al.  The precise localization of nigral afferents in the rat as determined by a retrograde tracing technique , 1976, Brain Research.

[29]  G. Percheron,et al.  A Golgi analysis of the primate globus pallidus. II. Quantitative morphology and spatial orientation of dendritic arborizations , 1984, The Journal of comparative neurology.

[30]  M. Delong,et al.  Altered Tonic Activity of Neurons in the Globus Pallidus and Subthalamic Nucleus in the Primate MPTP Model of Parkinsonism , 1987 .

[31]  S. Haber,et al.  Evidence for interconnections between the two segments of the globus pallidus in primates: a PHA-L anterograde tracing study , 1990, Brain Research.

[32]  H. Fibiger,et al.  Demonstration of a pallido‐nigral projection innervating dopaminergic neurons , 1975, The Journal of comparative neurology.

[33]  L. Tremblay,et al.  Responses of pallidal neurons to striatal stimulation in intact waking monkeys , 1989, Brain Research.

[34]  M. Mühlethaler,et al.  Cholinergic nucleus basalis neurons display the capacity for rhythmic bursting activity mediated by low-threshold calcium spikes , 1992, Neuroscience.

[35]  R. Llinás,et al.  Electrophysiology of globus pallidus neurons in vitro. , 1994, Journal of neurophysiology.

[36]  A. Parent,et al.  The striatopallidal projection displays a high degree of anatomical specificity in the primate , 1992, Brain Research.

[37]  Bryan Kolb,et al.  Non-cholinergic globus pallidus cells that project to the cortex but not to the subthalamic nucleus in rat , 1985, Neuroscience Letters.

[38]  M. Carpenter,et al.  The organization of pallidosubthalamic fibers in the monkey. , 1968, Brain research.

[39]  N. Mizuno,et al.  A Golgi study on the globus pallidus of the mouse , 1981, The Journal of comparative neurology.

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

[41]  O. E. Millhouse Pallidal neurons in the rat , 1986, The Journal of comparative neurology.

[42]  H. Kita Responses of globus pallidus neurons to cortical stimulation: intracellular study in the rat , 1992, Brain Research.

[43]  A. D. Smith,et al.  A correlated light and electron microscopic study of identified cholinergic basal forebrain neurons that project to the cortex in the rat , 1985, The Journal of comparative neurology.

[44]  M R Park,et al.  An intracellular HRP study of the rat globus pallidus. I. Responses and light microscopic analysis , 1982, The Journal of comparative neurology.

[45]  S. T. Kitai,et al.  Single neostriatal efferent axons in the globus pallidus: a light and electron microscopic study. , 1981, Science.

[46]  H. Bergman,et al.  Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. , 1990, Science.

[47]  H. Kita,et al.  The morphology of globus pallidus projection neurons in the rat: an intracellular staining study , 1994, Brain Research.

[48]  M R Park,et al.  An intracellular HRP study of the rat globus pallidus. II. Fine structural characteristics and synaptic connections of medially located large GP neurons , 1983, The Journal of comparative neurology.

[49]  H. Fibiger,et al.  Demonstration of a pallidostriatal pathway by retrograde transport of HRP-labeled lectin , 1981, Brain Research.