Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area

Journal of Comparative Neurology - Tập 320 Số 2 - Trang 145-160 - 1992
Susan R. Sesack1,2, Virginia M. Pickel1
1Division of Neurobiology, Department of Neurology and Neuroscience, Cornell University Medical College, New York, New York 10021
2University of Pittsburgh, Department of Behavioral Neuroscience, A312A Langley Hall, Pittsburgh, PA 15260

Tóm tắt

AbstractPhysiological and pharmacological studies indicate that descending projections from the prefrontal cortex modulate dopaminergic transmission in the nucleus accumbens septi and ventral tegmental area. We investigated the ultrastructural bases for these interactions in rat by examining the synaptic associations between prefrontal cortical terminals labeled with anterograde markers (lesion‐induced degeneration or transport of Phaseolus vulgaris leucoagglutinin; PHA‐L) and neuronal processes containing immunoreactivity for the catecholamine synthesizing enzyme, tryosine hydroxylase.Prefrontal cortical terminals in the nucleus accumbens and ventral tegmental area contained clear, round vesicles and formed primarily asymmetric synapses on spines or small dendrites. In the ventral tegmental area, these terminals also formed asymmetric synapses on large dendrites and a few symmetric axodendritic synapses. In the nucleus accumbens septi, degenerating prefrontal cortical terminals synapsed on spiny dendrites which received convergent input from terminals containing peroxidase immunoreactivity for tyrosine hydroxylase, or from unlabeled terminals. In single sections, some tyrosine hydroxylase‐labeled terminals formed thin and punctate symmetric synapses with dendritic shafts, or the heads and necks of spines. Close appositions, but not axo‐axonic synapses, were frequently observed between degenerating prefrontal cortical afferents and tyrosine hydroxylase‐labeled or unlabeled terminals. In the ventral tegmental area, prefrontal cortical terminals labeled with immunoperoxidase for PHA‐L were in synaptic contact with dendrites containing immunogold reaction product for tyrosine hydroxylase, or with unlabeled dendrites.These results suggest that: (1) catecholaminergic (mainly dopaminergic) and prefrontal cortical terminals in the nucleus accumbens septi dually synapse on common spiny neurons; and (2) dopaminergic neurons in the ventral tegmental area receive monosynaptic input from prefrontal cortical afferents. This study provides the first ultrastructural basis for multiple sites of cellular interaction between prefrontal cortical efferents and mesolimbic dopaminergic neurons.

Từ khóa


Tài liệu tham khảo

Bannon M. J., 1983, Pharmacology of mesocortical dopamine neurons, Pharmacol. Rev., 35, 53

Bayer V. E., 1990, Ultrastructural localization of tyrosine hydroxylase in the rat ventral tegmental area: Relationship between immunolabeling density and neuronal associations, J. Neurosci., 10, 2996, 10.1523/JNEUROSCI.10-09-02996.1990

10.1016/0306-4522(78)90115-X

10.1016/0304-3940(79)91480-0

Björklund A., 1984, Handbook of Chemical Neuroanatomy, Vol 2: Classical Neurotransmitters in the CNS, Part I, 55

10.1002/cne.902270110

10.1016/0167-0115(84)90165-4

10.1016/0006-8993(84)90239-7

10.1083/jcb.86.3.831

10.1016/0893-133X(88)90012-7

10.1016/0165-0270(90)90015-8

10.1016/0306-4522(86)90124-7

10.1016/0006-8993(85)90140-4

10.1111/j.1471-4159.1985.tb04013.x

Clow D. W., 1989, Characterization of L‐glutamate action on the release of endogenous dopamine from the rat caudateputamen, J. Pharm. Exp. Therap., 248, 722

10.1007/978-1-4613-3189-6_4

10.1016/0006-8993(90)91557-W

10.1016/0006-8993(86)91260-6

10.1016/0306-4522(84)90294-X

10.1016/0006-8993(91)90933-M

10.1016/0006-8993(88)90606-3

10.1126/science.2799392

10.1016/0006-8993(84)90940-5

10.1016/0306-4522(80)90131-1

10.1073/pnas.86.22.9015

10.1016/0006-8993(85)91581-1

Gray E. G., 1959, Axosomatic and axo‐dendritic synapses of the cerebral cortex: An electron microscopic study, J. Anat., 93, 420

Halpairi S., 1990, Activation of NMDA receptors induces dephosphorylation of DARP‐32 in rat striatal slices, Nature, 343, 369, 10.1038/343369a0

10.1016/0306-4522(91)90202-Y

Herve D., 1989, Nondopaminergic prefrontocortical efferent fibers modulate D1 receptor denervation supersensitivity in specific regions of the rat striatum, J. Neurosci., 9, 3699, 10.1523/JNEUROSCI.09-11-03699.1989

10.1016/0006-8993(84)90675-9

10.1177/29.4.6166661

10.1016/0006-8993(90)91286-P

10.1016/0006-8993(90)90138-2

10.1016/0006-8993(90)90149-6

10.1073/pnas.70.10.2767

Kalivas P. W., 1989, Regulation of the mesocorticolimbic dopamine system by glutamic acid receptor subtypes, J. Pharmacol. Exp. Therap., 251, 378

10.1111/j.1471-4159.1987.tb05661.x

10.1016/0024-3205(86)90013-5

10.1016/0006-8993(84)91189-2

Krettek J. E., 1977, The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat, J. Comp. Neurol., 177, 157, 10.1002/cne.901710204

10.1016/0028-3908(87)90091-8

Leranth C., 1989, Tract‐Tracing Methods 2, Recent Progress, 129

Lonart G., 1991, High glutamate concentrations evoke Ca++ ‐independent dopamine release from striatal slices: A possible role of reverse dopamine transport, J. Pharmacol. Exp. Therap., 256, 1132

Maura G., 1988, Release‐regulating D‐2 dopamine receptors are located on striatal glutamatergic nerve terminals, J. Pharmacol. Exp. Therap., 247, 680

10.1007/978-1-4613-3189-6_11

10.1126/science.283.5400.401

10.1016/0306-4522(86)90076-X

Peters A., 1991, The Fine Structure of the Nervous System. Neurons and Their Supporting Cells

10.1002/cne.901870106

10.1002/jnr.490250302

Pickel V. M., 1989, Tract‐Tracing Methods 2, Recent Progress, 97

10.1002/jnr.490310203

10.1002/cne.902720102

10.1038/286074a0

10.1016/0006-8993(84)91117-X

10.1016/0006-8993(88)91427-8

10.1016/0006-8993(90)91146-8

Sesack S. R., 1990, Prefrontal cortical terminals synapse on dopaminergic neurons in the ventral tegmental area and on unlabeled neuronal targets of dopaminergic terminals in the nucleus accumbens septi, Proc. Soc. Neurosci., 16, 238

10.1002/cne.902900205

10.1016/0006-8993(90)90448-K

10.1016/0006-8993(79)90084-2

10.1016/0361-9230(82)90145-9

10.1002/cne.901630406

10.1016/0304-3940(79)96097-X

10.1007/BF00239191

Totterdell S., 1989, Convergence of hippocampal and dopaminergic input to identified neurons in the nucleus accumbens of the rat, J. Chemical. Neuroanat., 2, 285

10.1002/cne.902510106

10.1001/archpsyc.1987.01800190080012

10.1016/0165-0173(90)90015-G

10.1016/0006-8993(85)91402-7

10.1016/0006-8993(84)90623-1

Yang C. R., 1986, Dopamine enhances terminal excitability of hippocampal‐accumbens neurons via D2 receptor: Role of dopamine in presynaptic inhibition, J. Neurosci., 6, 2470, 10.1523/JNEUROSCI.06-08-02470.1986

Thông tin
Thông tin xuất bản

Journal of Comparative Neurology

Tập 320 Số 2

145-160

Thông tin tác giả