Projections from the Rat Prefrontal Cortex to the Ventral Tegmental Area: Target Specificity in the Synaptic Associations with Mesoaccumbens and Mesocortical Neurons

Journal of Neuroscience - Tập 20 Số 10 - Trang 3864-3873 - 2000
David B. Carr1, Susan R. Sesack1
1Departments of Neuroscience and Psychiatry, University of Pittsburgh, Pittsburgh, PennsylvaniA 15260

Tóm tắt

Excitatory projections from the prefrontal cortex (PFC) to the ventral tegmental area (VTA) play an important role in regulating the activity of VTA neurons and the extracellular levels of dopamine (DA) within forebrain regions. Previous investigations have demonstrated that PFC terminals synapse on the dendrites of DA and non-DA neurons in the VTA. However, the projection targets of these cells are not known. To address whether PFC afferents innervate different populations of VTA neurons that project to the nucleus accumbens (NAc) or to the PFC, a triple labeling method was used that combined peroxidase markers for anterograde and retrograde tract-tracing with pre-embedding immunogold–silver labeling for either tyrosine hydroxylase (TH) or GABA. Within the VTA, PFC terminals formed asymmetric synapses onto dendritic shafts that were immunoreactive for either TH or GABA. PFC terminals also synapsed on VTA dendrites that were retrogradely labeled from the NAc or the PFC. Dendrites retrogradely labeled from the NAc and postsynaptic to PFC afferents were sometimes immunoreactive for GABA but were never TH-labeled. Conversely, dendrites retrogradely labeled from the PFC and postsynaptic to PFC afferents were sometimes immunoreactive for TH but were never GABA-labeled. These results provide the first demonstration of PFC afferents synapsing on identified cell populations in the VTA and indicate a considerable degree of specificity in the targets of the PFC projection. The unexpected finding of selective PFC synaptic input to GABA-containing mesoaccumbens neurons and DA-containing mesocortical neurons suggests novel mechanisms through which the PFC can influence the activity of ascending DA and GABA projections.

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Tài liệu tham khảo

10.1523/JNEUROSCI.17-02-00851.1997

10.1523/JNEUROSCI.11-09-02694.1991

10.1016/S0006-3223(98)00380-1

Card, 1998, Different patterns of neuronal infection after intracerebral injection of two strains of pseudorabies virus., J Virol, 72, 4434, 10.1128/JVI.72.5.4434-4441.1998

10.1523/JNEUROSCI.19-24-11049.1999

Carr DB, Sesack SR (2000) GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse In Press.

Charlety, 1991, Burst firing of mesencephalic dopamine neurons is inhibited by somatodendritic application of kynurenate., Acta Physiol Scand, 142, 105, 10.1111/j.1748-1716.1991.tb09134.x

10.1111/j.1460-9568.1993.tb00479.x

10.1016/0006-8993(85)90140-4

10.1093/cercor/1.4.273

10.1016/0306-4522(94)00331-X

10.1016/0006-8993(88)90606-3

10.1016/0306-4522(88)90307-7

Grace AA (1987) The regulation of dopamine neuron activity as determined by in vivo and in vitro intracellular recordings. in Neurophysiology of dopamine systems: current status and clinical perspectives, eds Chiodo LA Freeman AS (Lakeshore, Grosse Pointe), pp 1–66.

10.1111/j.1749-6632.1988.tb42096.x

Gray, 1959, Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study., J Anatomy, 93, 420

Grenhoff, 1988, The excitatory amino acid antagonist kynurenate induces pacemaker-like firing of dopamine neurons in rat ventral tegmental area in vivo., Acta Physiol Scand, 134, 567, 10.1111/j.1365-201X.1988.tb10639.x

Horger, 1996, The role of mesoprefrontal dopamine neurons in stress., Crit Rev Neurobiol, 10, 395, 10.1615/CritRevNeurobiol.v10.i3-4.60

10.1002/cne.903080210

Jedema, 1996, Characterization of excitatory amino acid modulation of dopamine release in the prefrontal cortex of conscious rats., J Neurochem, 66, 1448, 10.1046/j.1471-4159.1996.66041448.x

10.1046/j.1471-4159.1996.66020589.x

Kosaka, 1987, Catecholaminergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat., Exp Brain Res, 66, 191, 10.1007/BF00236215

10.1073/pnas.93.17.9235

10.1016/S0006-8993(98)01317-1

Leranth C Pickel VM (1989) Electron microscopic preembedding double-immunostaining methods. in Neuroanatomical tract tracing methods 2: recent progress, eds Heimer L Záborszky L (Plenum, New York), pp 129–172.

10.1002/(SICI)1098-2396(199702)25:2<205::AID-SYN11>3.0.CO;2-X

10.1016/0306-4522(88)90285-0

10.1016/0006-8993(89)91263-8

10.1016/0304-3940(93)90641-W

10.1523/JNEUROSCI.15-09-05859.1995

10.1016/0006-8993(94)90263-1

10.1523/JNEUROSCI.17-06-02143.1997

10.1002/syn.890100208

Paxinos G Watson C (1986) The rat brain in stereotaxic coordinates. (Academic, New York).

Peters A Palay SL Webster H (1991) The fine structure of the nervous system: neurons and their supporting cells, Ed 3. (Oxford, New York).

10.1016/0006-8993(88)90614-2

10.1016/S0306-4522(96)00382-X

10.1016/S0959-4388(97)80007-4

10.1126/science.275.5306.1593

10.1002/cne.902790306

Sesack, 1989, Pharmacological characterization of the receptor mediating electrophysiological responses to dopamine in the rat medial prefrontal cortex: a microiontophoretic study., J Pharmacol Exp Ther, 248, 1323

10.1002/cne.903200202

10.1002/cne.902900205

10.1002/(SICI)1096-9861(19960108)364:2<254::AID-CNE5>3.0.CO;2-4

Streckler RL Jacobs BL (1987) Dopaminergic unit activity during behavior. in Neurophysiology of dopamine systems: current status and clinical perspectives, eds Chiodo LA Freeman AS (Lakeshore, Grosse Pointe), pp 165–185.

10.1111/j.1748-1716.1989.tb08640.x

10.1016/0361-9230(82)90145-9

10.1523/JNEUROSCI.15-05-03896.1995

10.1046/j.1471-4159.1995.65031407.x

Takahata, 1998, Glutamatergic regulation of basal and stimulus-activated dopamine release in the prefrontal cortex., J Neurochem, 71, 1443, 10.1046/j.1471-4159.1998.71041443.x

10.1038/263242a0

10.1016/0304-3940(79)96097-X

10.1111/j.1749-6632.1988.tb42099.x

10.1002/(SICI)1098-2396(199603)22:3<195::AID-SYN1>3.0.CO;2-7

10.1007/s002210050303

10.1016/0006-8993(95)00334-M

10.1016/0166-4328(95)80001-8

10.1523/JNEUROSCI.15-07-05169.1995

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Journal of Neuroscience

Tập 20 Số 10

3864-3873

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