Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study

A major mesolimbic projection towards the hippocampal formation (HF) has been extensively described, but no clear evidence of its dopaminergic content has been demonstrated. In order to evaluate the percentage of dopaminergic (DA) cells of ventral tegmental area (VTA-A10) and adjacent substantia nigra (SN-A9) projecting to the HF, the retrograde neuronal tracer technique was combined with the tyrosine hydroxylase (TH) immunocytochemistry. Fluoro-gold (FG) was injected in several areas (subiculum, CA1, CA3, dentate gyrus) of either septal and temporal HF. Sections containing retrogradely FG labeled neurons were either mounted directly as controls or incubated with TH antiserum and revealed with rhodamine. The quantitative evaluation of retrogradely labeled and TH-IR stained cells showed that both VTA and SN projections towards the HF are partially (15-18%) dopaminergic. Ten percent of the DA neurons of the VTA projected to contralateral HF, whereas none did in the SN. In conclusion, the temporal HF (mainly subiculum and adjacent CA1) appears to receive the main DA afferents from both VTA cells and medial half of SN, pars compacta, whereas the septal HF (particularly CA1) receives its DA input from neurons located in the ventral half and in the upper and lower borders of the VTA.

[1]  D. Jacobowitz,et al.  Topographic atlas of catecholamine and acetylcholinesterase‐containing neurons in the rat brain. I. Forebrain (telencephalon, diencephalon) , 1974, The Journal of comparative neurology.

[2]  Herve Simon,et al.  Origin of dopaminergic innervation of the rat hippocampal formation , 1980, Neuroscience Letters.

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

[4]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[5]  H. Simon,et al.  [Dopaminergic A10 neurons and frontal system (author's transl)]. , 1981, Journal de physiologie.

[6]  P. Mcgeer,et al.  Relative sparing in Parkinson's disease of substantia nigra dopamine neurons containing calbindin-D28K , 1990, Brain Research.

[7]  H. Wheal,et al.  Synaptic inhibition in the rat hippocampus in vivo following stimulation of the substantia nigra and ventral tegmentum. , 1990, The Journal of physiology.

[8]  S. Sesack,et al.  In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other , 1990, Brain Research.

[9]  R. Oades,et al.  Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity , 1987, Brain Research Reviews.

[10]  T. Crow,et al.  Distribution of neuropeptides in the limbic system of the rat: The hippocampus , 1984, Neuroscience.

[11]  T. Hökfelt,et al.  Occurrence of neurotensinlike immunoreactivity in subpopulations of hypothalamic, mesencephalic, and medullary catecholamine neurons , 1984, The Journal of comparative neurology.

[12]  M. Witter,et al.  Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin , 1987, Neuroscience.

[13]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[14]  B. Berger,et al.  Morphological evidence for a dopaminergic terminal field in the hippocampal formation of young and adult rat , 1985, Neuroscience.

[15]  L. Schmued,et al.  Fluoro-gold: a new fluorescent retrograde axonal tracer with numerous unique properties , 1986, Brain Research.

[16]  G. Ju,et al.  Fluorogold as a retrograde tracer used in combination with immunohistochemistry , 1989, Journal of Neuroscience Methods.

[17]  D. Amaral.  A golgi study of cell types in the hilar region of the hippocampus in the rat , 1978, The Journal of comparative neurology.

[18]  J. H. Fallon,et al.  Substantia nigra and ventral tegmental area projections to cortex: Topography and collateralization , 1984, Neuroscience.

[19]  A. Gasbarri,et al.  Organization of the projections from the ventral tegmental area of Tsai to the hippocampal formation in the rat. , 1991, Journal fur Hirnforschung.

[20]  W. Nauta,et al.  The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods , 1982, Neuroscience.

[21]  J. Korf,et al.  Biochemical evidence for a transmitter role of dopamine in the rat hippocamus , 1979, Brain Research.

[22]  R. Godbout,et al.  Inhibitory effects of ventral tegmental area stimulation on the activity of prefrontal cortical neurons: Evidence for the involvement of both dopaminergic and GABAergic components , 1992, Neuroscience.

[23]  L. Swanson,et al.  The projections of the ventral tegmental area and adjacent regions: A combined fluorescent retrograde tracer and immunofluorescence study in the rat , 1982, Brain Research Bulletin.

[24]  M. Martres,et al.  Widespread distribution of brain dopamine receptors evidenced with [125I]iodosulpride, a highly selective ligand. , 1985, Science.

[25]  C J CLEMEDSON,et al.  DYNAMIC RESPONSE OF CHEST WALL AND LUNG INJURIES IN RABBITS EXPOSED TO AIR SHOCK WAVES OF SHORT DURATION. , 1964, Acta physiologica Scandinavica. Supplementum.

[26]  J. Olszewski,et al.  Cytoarchitecture of the Human Brain Stem , 1955 .

[27]  G. Halliday,et al.  Comparative anatomy of the ventromedial mesencephalic tegmentum in the rat, cat, monkey and human , 1986, The Journal of comparative neurology.

[28]  James L. McGaugh,et al.  Evidence for dopamine as a transmitter in dorsal hippocampus , 1982, Brain Research.

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

[30]  L. Descarries,et al.  Distribution and Morphological Characteristics of Dopamine‐Immunoreactive Neurons in the Midbrain of the Squirrel Monkey (Saimiri sciureus) , 1988, The Journal of comparative neurology.

[31]  M. Carpenter,et al.  Monoamine-containing cell bodies in the squirrel monkey brain. , 1974, The American journal of anatomy.

[32]  Y. Agid,et al.  Labeled wheat germ agglutinin (WGA) as a new, highly sensitive retrograde tracer in the rat brain hippocampal system , 1978, Brain Research.

[33]  A. Kelley,et al.  The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: An anterograde and retrograde-horseradish peroxidase study , 1982, Neuroscience.

[34]  S. Y. Assaf,et al.  Neuronal transmission in the dentate gyrus: role of inhibitory mechanisms , 1978, Brain Research.

[35]  T. Hattori,et al.  Organization of ventral tegmental area cells projecting to the occipital cortex and forebrain in the rat , 1987, Brain Research.

[36]  R. Wyatt,et al.  Biochemical evidence for uncrossed and crossed locus coeruleus projections to the spinal cord , 1980, Brain Research.

[37]  H. Fibiger,et al.  Ascending projections of presumed dopamine-containing neurons in the ventral tegmentum of the rat as demonstrated by horseradish peroxidase , 1977, Neuroscience.

[38]  T. Blackstad.  Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination , 1956, The Journal of comparative neurology.

[39]  K. Fuxe,et al.  EVIDENCE FOR THE EXISTENCE OF MONOAMINE-CONTAINING NEURONS IN THE CENTRAL NERVOUS SYSTEM. I. DEMONSTRATION OF MONOAMINES IN THE CELL BODIES OF BRAIN STEM NEURONS. , 1964, Acta physiologica Scandinavica. Supplementum.

[40]  Mark G. Packard,et al.  Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat , 1994, Brain Research Bulletin.

[41]  Hervé Simon,et al.  Efferents and afferents of the ventral tegmental-A10 region studied after local injection of [3H]leucine and horseradish peroxidase , 1979, Brain Research.

[42]  B. K. Hartman,et al.  The central adrenergic system. An immunofluorescence study of the location of cell bodies and their efferent connections in the rat utilizing dopamine‐B‐hydroxylase as a marker , 1975, The Journal of comparative neurology.

[43]  A. Siegel,et al.  Efferent connections of the hippocampal formation in the rat , 1977, Brain Research.

[44]  O. Phillipson.  The cytoarchitecture of the interfascicular nucleus and ventral tegmental area of tsai in the rat , 1979, The Journal of comparative neurology.

[45]  B. Berger,et al.  Further indication that distinct dopaminergic subsets project to the rat cerebral cortex: lack of colocalization with neurotensin in the superficial dopaminergic fields of the anterior cingulate, motor, retrosplenial and visual cortices , 1991, Brain Research.

[46]  R. Moore,et al.  Noradrenergic innervation of the adult rat hippocampal formation , 1980, The Journal of comparative neurology.

[47]  A. D. Smith,et al.  Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. , 1989, Journal of chemical neuroanatomy.

[48]  M. Palkovits,et al.  Norepinephrine and dopamine in the limbic system of the rat. , 1974, Brain research.