Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat

Employing anterograde tracing with Phaseolus vulgaris-leucoagglutinin (PHA-L), and a triple labeling protocol using retrogradely transported fluorescent tracers, we examined the projections from the ventral tegmental area (VTA-A10) to the hippocampal formation (HF) in the rat. Injections of PHA-L into VTA resulted in labeling in the ventral subiculum (stratum oriens and molecular layer) and in the adjacent CA1 field (stratum oriens, pyramidal, suprapyramidal and molecular layers) of HF. Additional labeling was observed in the stratum oriens of CA3 and in the hilus of fascia dentata. In the dorsal HF labeling was present in the subicular and CA1 field polymorphic layers. The distribution of VTA neurons projecting to the HF was also examined by injecting retrograde fluorescent tracers (Fluoro Gold, Fast Blue, and Nuclear Yellow) in several hippocampal areas. The most abundant VTA-HF projections originate from the upper and lower edges and the lower half of the VTA. These terminal fields in the HF match with the hippocampal areas projecting to the nucleus accumbens. The VTA, via projections to interconnected regions of the HF and nucleus accumbens, may modulate the hypothesized functional link between the limbic system and basal ganglia.

[1]  Bryan Kolb,et al.  Spatial mapping: definitive disruption by hippocampal or medial frontal cortical damage in the rat , 1982, Neuroscience Letters.

[2]  T. Hattori,et al.  Collateral projections from the substantia nigra to the cingulate cortex and striatum in the rat , 1986, Brain Research.

[3]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[4]  Y. Agid,et al.  Evidence for the Existence of a Dopaminergic Innervation of the Rat and Human Hippocampal Formation , 1982 .

[5]  J. Rawlins,et al.  The neuropsychology of schizophrenia , 1991, Behavioral and Brain Sciences.

[6]  G. Mogenson,et al.  The role of the hippocampal-nucleus accumbens pathway in radial-arm maze performance , 1989, Brain Research.

[7]  Stephen B. Dunnett,et al.  The effects of excitotoxic lesions of the nucleus accumbens on a matching to position task , 1991, Behavioural Brain Research.

[8]  H. Groenewegen,et al.  Neuroanatomical tracing by use of Phaseolus vulgaris-leucoagglutinin (PHA-L): electron microscopy of PHA-L-filled neuronal somata, dendrites, axons and axon terminals , 1985, Brain Research.

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

[10]  Behavioral Responses to Amphetamine Challenge following 6-Ohda Hippocampal Lesions in Rats , 1992 .

[11]  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.

[12]  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.

[13]  R. Hirsh The hippocampus and contextual retrieval of information from memory: a theory. , 1974, Behavioral biology.

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

[15]  J. Fallon Collateralization of monoamine neurons: mesotelencephalic dopamine projections to caudate, septum, and frontal cortex , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  G. Mogenson,et al.  A study of the contribution of hippocampal-accumbens-subpallidal projections to locomotor activity. , 1984, Behavioral and neural biology.

[17]  R. M. Beckstead,et al.  Convergent thalamic and mesencephalic projections to the anterior medial cortex in the rat , 1976, The Journal of comparative neurology.

[18]  N. White,et al.  Conditioned place preference from intra-accumbens but not intra-caudate amphetamine injections. , 1983, Life sciences.

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

[20]  N. White,et al.  Operationalizing and Measuring the Organizing Influence of Drugs on Behavior , 1987 .

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

[22]  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.

[23]  M. Packard,et al.  Dissociation of hippocampus and caudate nucleus memory systems by posttraining intracerebral injection of dopamine agonists , 1991 .

[24]  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.

[25]  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.

[26]  M. Herkenham,et al.  Cell clusters in the nucleus accumbens of the rat, and the mosaic relationship of opiate receptors, acetylcholinesterase and subcortical afferent terminations , 1984, Neuroscience.

[27]  J. V. van Rossum,et al.  Effects of chemical stimulation of the mesolimbic dopamine system upon locomotor activity. , 1976, European journal of pharmacology.

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

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

[30]  G. Mogenson,et al.  Electrophysiological studies of neurons in the ventral tegmental area of tsai , 1980, Brain Research.

[31]  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.

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

[33]  T. Robbins,et al.  The effects of ibotenic acid lesions of the nucleus accumbens on spatial learning and extinction in the rat , 1989, Behavioural Brain Research.

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

[35]  R. Sutherland,et al.  The role of the fornix/fimbria and some related subcortical structures in place learning and memory , 1989, Behavioural Brain Research.

[36]  M. Le Moal,et al.  Alternation behavior, spatial discrimination, and reversal disturbances following 6-hydroxydopamine lesions in the nucleus accumbens of the rat. , 1985, Behavioral and neural biology.

[37]  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.

[38]  I. Whishaw,et al.  Hippocampal modulation of nucleus accumbens: behavioral evidence from amphetamine-induced activity profiles. , 1991, Behavioral and neural biology.

[39]  S. Iversen,et al.  Amphetamine and apomorphine responses in the rat following 6-OHDA lesions of the nucleus accumbens septi and corpus striatum , 1975, Brain Research.

[40]  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.

[41]  L. Heimer,et al.  Iontophoretic injection of fluoro-gold and other fluorescent tracers. , 1990, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[42]  J. Fallon,et al.  Catecholamine innervation of the basal forebrain IV. Topography of the dopamine projection to the basal forebrain and neostriatum , 1978, The Journal of comparative neurology.

[43]  W. Nauta,et al.  Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber‐of‐passage problem , 1977, The Journal of comparative neurology.

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

[45]  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.

[46]  U. Ungerstedt Stereotaxic mapping of the monoamine pathways in the rat brain. , 1971, Acta physiologica Scandinavica. Supplementum.

[47]  R. Wise Neuroleptics and operant behavior: The anhedonia hypothesis , 1982, Behavioral and Brain Sciences.

[48]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

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

[50]  M. Le Moal,et al.  Mesocorticolimbic dopaminergic network: functional and regulatory roles. , 1991, Physiological reviews.

[51]  A. Albanese,et al.  Organization of the ascending projections from the ventral tegmental area: A multiple fluorescent retrograde tracer study in the rat , 1983, The Journal of comparative neurology.

[52]  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.

[53]  O. Lindvall,et al.  The organization of the ascending catecholamine neuron systems in the rat brain as revealed by the glyoxylic acid fluorescence method. , 1974, Acta physiologica Scandinavica. Supplementum.

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

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

[56]  H. Groenewegen,et al.  Subcortical afferents of the nucleus accumbens septi in the cat, studied with retrograde axonal transport of horseradish peroxidase and bisbenzimid , 1980, Neuroscience.