Cerebellar Projections to the Prefrontal Cortex of the Primate

Journal of Neuroscience - Tập 21 Số 2 - Trang 700-712 - 2001
Frank A. Middleton1, Peter L. Strick2,1,3
1Departments of Neurobiology, and
2Department of Veterans Affairs Medical Center, Pittsburgh, Pennsylvania 15240
3Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania 15261, and

Tóm tắt

The cerebellum is known to project via the thalamus to multiple motor areas of the cerebral cortex. In this study, we examined the extent and anatomical organization of cerebellar input to multiple regions of prefrontal cortex. We first used conventional retrograde tracers to map the origin of thalamic projections to five prefrontal regions: medial area 9 (9m), lateral area 9 (9l), dorsal area 46 (46d), ventral area 46, and lateral area 12. Only areas 46d, 9m, and 9l received substantial input from thalamic regions included within the zone of termination of cerebellar efferents. This suggested that these cortical areas were the target of cerebellar output. We tested this possibility using retrograde transneuronal transport of the McIntyre-B strain of herpes simplex virus type 1 from areas of prefrontal cortex. Neurons labeled by retrograde transneuronal transport of virus were found in the dentate nucleus only after injections into areas 46d, 9m, and 9l. The precise location of labeled neurons in the dentate varied with the prefrontal area injected. In addition, the dentate neurons labeled after virus injections into prefrontal areas were located in regions spatially separate from those labeled after virus injections into motor areas of the cerebral cortex. Our observations indicate that the cerebellum influences several areas of prefrontal cortex via the thalamus. Furthermore, separate output channels exist in the dentate to influence motor and cognitive operations. These results provide an anatomical substrate for the cerebellum to be involved in cognitive functions such as planning, working memory, and rule-based learning.

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Tài liệu tham khảo

10.1037/0735-7044.106.5.731

Allen, 1974, Cerebrocerebellar communication systems., Physiol Rev, 54, 957, 10.1152/physrev.1974.54.4.957

Allen, 1978, Convergence of cerebral inputs onto dentate neurons in monkey., Exp Brain Res, 32, 151, 10.1007/BF00239724

10.1073/pnas.93.18.9985

10.1016/0165-0173(83)90015-2

10.1002/cne.902860306

10.1002/cne.903130106

10.1212/WNL.35.6.866

10.1016/0304-3940(80)90208-6

10.1007/BF02333774

10.1093/brain/101.2.251

Brooks VB Thach WT (1981) Cerebellar control of posture and movement. in Handbook of physiology, Sec 1, The nervous system, Vol 2, Motor control, Pt II, ed Brooks VB (American Physiological Society, Bethesda, MD), pp 877–946.

10.1016/0165-0270(87)90100-2

10.1016/S0959-4388(97)80016-5

10.1056/NEJM198805263182102

10.1002/cne.902990103

10.1002/cne.903440403

Dum, 1999, Pallidal and cerebellar inputs to the digit representations of the lateral premotor areas., Soc Neurosci Abstr, 25, 1925

10.1146/annurev.ph.31.030169.002315

10.1093/brain/115.1.155

10.1523/JNEUROSCI.16-02-00808.1996

10.1212/WNL.48.3.589

10.1016/S0166-4328(96)00151-9

Fuster J (1997) The prefrontal cortex. (Raven, New York).

10.1126/science.272.5261.545

10.1002/cne.902350306

Goldman-Rakic PS (1987) Circuitry of primate prefrontal cortex and regulation of behavior by representational memory. in Handbook of physiology, Sec 1, The nervous system, Vol V, ed Plum F (American Physiological Society, Bethesda, MD), pp 373–413.

10.1002/cne.902420406

10.1016/0361-9230(90)90189-7

10.1212/WNL.42.8.1493

10.1176/ajp.140.10.1322

10.1093/brain/122.4.593

Hartmann-von Monakow, 1981, Projection of precentral, premotor and prefrontal cortex to the basilar pontine grey and to nucleus reticularis tegmenti pontis in the monkey (Macaca fascicularis)., Schweiz Arch Neurol Neurochir Psychiatr, 129, 189

10.1097/00005053-197910000-00001

Hikosaka, 1996, Activation of human presupplementary motor area in learning of sequential procedures: a functional MRI study., J Neurophysiol, 76, 617, 10.1152/jn.1996.76.1.617

10.1006/nlme.1998.3844

10.1126/science.7679223

10.1523/JNEUROSCI.19-04-01446.1999

10.1016/0006-8993(83)90816-8

10.1162/jocn.1989.1.2.136

Jacobsen, 1936, Studies of cerebral function in primates. I. The functions of the frontal association areas in monkeys., Comp Psychol Monogr, 13, 3

10.1523/JNEUROSCI.14-06-03775.1994

Joseph, 1985, Brainstem and vermis atrophy in catatonia., Am J Psychiatry, 142, 352, 10.1176/ajp.142.3.352

Jueptner, 1997, Anatomy of motor learning. I. Frontal cortex and attention to action., J Neurophysiol, 77, 1313, 10.1152/jn.1997.77.3.1313

Jueptner, 1997, Anatomy of motor learning. II. Subcortical structures and learning by trial and error., J Neurophysiol, 77, 1325, 10.1152/jn.1997.77.3.1325

10.1016/0920-9964(94)90076-0

10.1002/cne.901950105

Kelly, 1998, Cerebro-cerebellar “loops” are closed., Soc Neurosci Abstr, 24, 1407

10.1098/rstb.1971.0106

Kievit J Kuypers HGJM (1972) Fastigial cerebellar projections to the ventrolateral nucleus of the thalamus and the organization of the descending pathways. in Corticothalamic projections and sensorimotor activities, eds Frigyes T Rinvik E Yahr MO (Raven, New York), pp 91–114.

Kievit, 1977, Organization of thalamo-cortical connexions to the frontal lobe in the rhesus monkey., Exp Brain Res, 29, 299

10.1126/science.8052851

Kusama, 1971, Cerebellar projections to the thalamic nucleus in the monkey., Proc Jap Acad, 47, 505, 10.2183/pjab1945.47.505

10.1016/B978-0-12-008305-3.50014-3

10.1002/(SICI)1097-4547(19970815)49:4<485::AID-JNR9>3.0.CO;2-4

10.1002/cne.902280307

10.1037/0735-7044.100.4.443

Leiner, 1987, Cerebro-cerebellar learning loops in apes and humans., Ital J Neurol Sci, 8, 425, 10.1007/BF02334599

10.1037/0735-7044.103.5.998

10.1016/S0166-4328(05)80016-6

10.1016/0166-2236(93)90072-T

Lynch, 1994, Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport., Exp Brain Res, 100, 181, 10.1007/BF00227293

10.1093/schbul/21.2.241

10.1002/(SICI)1096-9861(19960812)372:1<59::AID-CNE6>3.0.CO;2-L

10.1002/cne.902800311

10.1016/0361-9230(89)90032-4

Mesulam MM (1982) Tracing neural connections (Mesulam MM, ed), pp 1–151. (Wiley, New York).

10.1126/science.7939688

10.1073/pnas.93.16.8683

Middleton, 1997, Dentate output channels: motor and cognitive components., Prog Brain Res, 114, 555

10.1016/S1364-6613(98)01220-0

10.1016/S0165-0173(99)00040-5

10.1016/0006-8993(83)90698-4

10.1093/brain/120.10.1753

Mushiake, 1993, Preferential activity of dentate neurons during limb movements., J Neurophysiol, 70, 2660, 10.1152/jn.1993.70.6.2660

Mushiake, 1995, Cerebellar and pallidal activity during instructed delay periods., Soc Neurosci Abstr, 21, 411

10.1002/cne.901940209

10.1016/S0028-3932(99)00138-4

Olszewski J (1952) The thalamus of Macaca mulatta. An atlas for use with the stereotaxic instrument. (Karger, Basel).

10.1002/cne.902880408

10.1002/ana.410340414

10.1111/j.1749-6632.1995.tb38131.x

Pascual-Leone, 1996, The role of the dorsolateral prefrontal cortex in implicit procedural learning., Exp Brain Res, 107, 479, 10.1007/BF00230427

Passingham R (1993) The frontal lobes and voluntary action. (Oxford UP, Oxford).

Percheron, 1977, The thalamic territory of cerebellar afferents and the lateral region of the thalamus of the macaque in stereotaxic ventricular coordinates., J Hirnforsch, 18, 375

10.1016/0165-0173(96)00003-3

10.1038/331585a0

10.1523/JNEUROSCI.15-01-00359.1995

10.1016/0028-3932(82)90100-2

10.1093/cercor/4.1.8

10.1016/0165-0270(90)90101-K

10.1177/26.1.413864

10.1177/34.10.3745909

10.1002/cne.903450204

10.1523/JNEUROSCI.17-12-04829.1997

10.1523/JNEUROSCI.18-05-01827.1998

10.1002/(SICI)1096-9861(19960429)368:2<215::AID-CNE4>3.0.CO;2-6

10.1007/BF01474266

10.1523/JNEUROSCI.04-02-00539.1984

10.1001/archneur.1991.00530230086029

Schmahmann, 1997, Rediscovery of an early concept., Int Rev Neurobiol, 41, 3, 10.1016/S0074-7742(08)60345-1

10.1016/0304-3940(95)12056-A

10.1523/JNEUROSCI.17-01-00438.1997

10.1016/S0074-7742(08)60346-3

10.1093/brain/121.4.561

Shelton RC Weinberger DR (1986) X-ray computerized tomography studies in schizophrenia: a review and synthesis. in Handbook of schizophrenia, eds Nasrallah HA Weinberger DR (Elsevier, New York), pp 207–250.

10.1016/0149-7634(82)90006-9

10.1002/cne.901900406

10.1016/0006-8993(85)90475-5

Strick PL Card JP (1992) Transneuronal mapping of neural circuits with alpha herpesviruses. in Experimental neuroanatomy: a practical approach, ed Bolam JP (Oxford UP, Oxford), pp 81–101.

Strick PL Hoover JE Mushiake H (1993) Evidence for “output channels” in the basal ganglia and cerebellum. in Role of the cerebellum and basal ganglia in voluntary movement, eds Mano N Hamada I DeLong MR (Elsevier, Amsterdam), pp 171–180.

Tolbert, 1978, Multiple branching of cerebellar efferent projections in cats., Exp Brain Res, 31, 305, 10.1007/BF00237291

10.1016/0006-8993(81)90348-6

Volkow, 1992, Low cerebellar metabolism in medicated patients with chronic schizophrenia., Am J Psychiatry, 149, 686, 10.1176/ajp.149.5.686

10.1002/cne.900730106

Weinberger, 1979, Cerebellar atrophy in chronic schizophrenia., Lancet, 1, 718, 10.1016/S0140-6736(79)91164-4

Wiesendanger, 1985, The thalamic connections with medial area 6 (supplementary motor cortex) in the monkey (Macaca fascicularis)., Exp Brain Res, 59, 91, 10.1007/BF00237670

Wiesendanger, 1985, Cerebello-cortical linkage in the monkey as revealed by transcellular labeling with the lectin wheat germ agglutinin conjugated to the marker horseradish peroxidase., Exp Brain Res, 59, 105, 10.1007/BF00237671

Wilson, 1994, Dissociation of object and spatial processing domains in primate prefrontal cortex., Science, 260, 1995

10.1016/0006-8993(92)90067-J

Yates, 1987, Cerebellar atrophy in schizophrenia and affective disorder., Am J Psychiatry, 144, 465, 10.1176/ajp.144.4.465

10.1073/pnas.88.18.8048