Abstract
Our growing understanding of how cerebral cortical areas communicate with the cerebellum in primates has enriched our understanding of the data that cerebellar circuits can access, and the neocortical areas that cerebellar activity can influence. The cerebellum is part of some large-scale networks involving several parts of the neocortex including association areas in the frontal lobe and the posterior parietal cortex that are known for their contributions to higher cognitive function. Understanding their connections with the cerebellum informs the debates around the role of the cerebellum in higher cognitive functions because they provide mechanisms through which association areas and the cerebellum can influence each others' operations. In recent years, evidence from connectional anatomy and human neuroimaging have comprehensively overturned the view that the cerebellum contributes only to motor control. The aim of this review is to examine our changing perspectives on the nature of cortico-cerebellar anatomy and the ways in which it continues to shape our views on its contributions to function. The review considers the anatomical connectivity of the cerebellar cortex with frontal lobe areas and the posterior parietal cortex. It will first focus on the anatomical organisation of these circuits in non-human primates before discussing new findings about this system in the human brain. It has been suggested that in non-human primates “although there is a modest input from medial prefrontal cortex, there is very little or none from the more lateral prefrontal areas” [33]. This review discusses anatomical investigations that challenge this claim. It also attempts to dispel the misconception that prefrontal projections to the cerebellum are from areas concerned only with the kinematic control of eye movements. Finally, I argue that our revised understanding of anatomy compels us to reconsider conventional views of how these systems operate in the human brain.
Similar content being viewed by others
Notes
The tissue in and around sulcus principalis in the prefrontal cortex is important to this debate because its projections to the cerebellum have recently been studied using trans-synaptic tracers (see below). Glickstein et al. [36] do indeed report the presence of label in this area (see Fig. 2), and as mentioned above, it has an important role in the processing of abstract information. In the nomenclature of Brodmann (1905), used by Glickstein et al. [36], area 9 encompasses the sulcus principalis extending onto the medial convexity to the upper bank of the cingulate sulcus. Others have used the nomenclature of Walker [95] and make a distinction between areas 9 and 46. Area 46 includes both banks of the sulcus principalis, and area extends from the upper bank of sulcus principalis. It is important to note that when Glickstein refers to area 9, this includes the tissue in sulcus principalis that other authors have called area 46. Glickstein et al. [36] show that this area sends projections to the pontine nuclei (see Fig. 2).
References
Akkal D, Dum RP, Strick PL. Supplementary motor area and presupplementary motor area: targets of basal ganglia and cerebellar output. J Neurosci. 2007;27:10659–73.
Amiez C, Petrides M. Anatomical organization of the eye fields in the human and non-human primate frontal cortex. Prog Neurobiol. 2009;89:220–30.
Andersen RA, Buneo CA. Intentional maps in posterior parietal cortex. Annu Rev Neurosci. 2002;25:189–220.
Andersen RA, Cui H. Intention, action planning, and decision making in parietal–frontal circuits. Neuron. 2009;63:568–83.
Angevine JB, Mancall EL, Yakolev PI. Terminology: cerebellar nomenclature. In: The human cerebellum: an atlas of gross topography in serial sections. London: J. & A. Churchill Ltd; 1961.
Apps R, Garwicz M. Anatomical and physiological foundations of cerebellar information processing. Nat Rev Neurosci. 2005;6:297–311.
Apps R, Hawkes R. Cerebellar cortical organization: a one-map hypothesis. Nat Rev Neurosci. 2009;10:670–81.
Asanuma C, Thach WT, Jones EG. Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res. 1983;286:237–65.
Badre D, D’Esposito M. Is the rostro-caudal axis of the frontal lobe hierarchical? Nat Rev Neurosci. 2009;10:659–69.
Balsters JH, Cussans E, Diedrichsen J, Phillips KA, Preuss TM, et al. Evolution of the cerebellar cortex: the selective expansion of prefrontal-projecting cerebellar lobules. Neuroimage. 2010;49:2045–52.
Balsters JH, Ramnani N. Symbolic representations of action in the human cerebellum. Neuroimage. 2008;43:388–98.
Balsters JH, Ramnani N. Cerebellar plasticity and the automation of first-order rules. J Neurosci. 2011;31:2305–12.
Beck E. The origin, course and termination of the prefronto-pontine tract in the human brain. Brain. 1950;73:368–91.
Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 2003;6:750–7.
Brodal A. The cerebellum. In: Neurological anatomy in relation to clinical medicine. New York, Oxford: Oxford University Press; 1981. pp. 312–9
Brodal P. The corticopontine projection in the rhesus monkey. Origin and principles of organization. Brain. 1978;101:251–83.
Brodal P. Principles of organization of the monkey corticopontine projection. Brain Res. 1978;148:214–8.
Bunge SA. How we use rules to select actions: a review of evidence from cognitive neuroscience. Cogn Affect Behav Neurosci. 2004;4:564–79.
Churchland MM, Yu BM, Ryu SI, Santhanam G, Shenoy KV. Neural variability in premotor cortex provides a signature of motor preparation. J Neurosci. 2006;26:3697–712.
Clower DM, West RA, Lynch JC, Strick PL. The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum. J Neurosci. 2001;21:6283–91.
Coe B, Tomihara K, Matsuzawa M, Hikosaka O. Visual and anticipatory bias in three cortical eye fields of the monkey during an adaptive decision-making task. J Neurosci. 2002;22:5081–90.
Cui H, Andersen RA. Posterior parietal cortex encodes autonomously selected motor plans. Neuron. 2007;56:552–9.
Culham JC, Kanwisher NG. Neuroimaging of cognitive functions in human parietal cortex. Curr Opin Neurobiol. 2001;11:157–63.
Deco, G, Jirsa, VK, McIntosh, AR. Emerging concepts for the dynamical organization of resting-state activity in the brain. Nat Rev Neurosci. 2011;12:43–56.
Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain. 1995;118(Pt 1):279–306.
Doron KW, Funk CM, Glickstein M. Fronto-cerebellar circuits and eye movement control: a diffusion imaging tractography study of human cortico-pontine projections. Brain Res. 2009;1307:63–71.
Dow RS. Cerebellar action potentials in response to stimulation of the cerebral cortex in monkeys and cats. J Neurophysiol. 1942;5:121–36.
Dum RP, Li C, Strick PL. Motor and nonmotor domains in the monkey dentate. Ann NY Acad Sci. 2002;978:289–301.
Dum RP, Strick PL. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003;89:634–9.
Evarts EV, Thach WT. Motor mechanisms of the CNS: cerebrocerebellar interrelations. Annu Rev Physiol. 1969;31:451–98.
Ferrera VP, Yanike M, Cassanello C. Frontal eye field neurons signal changes in decision criteria. Nat Neurosci. 2009;12:1458–62.
Ferrier D, Turner WA. An experimental research upon cerebro-cortical afferent and efferent tracts. J Anat Physiol. 1897;31:627–9.
Glickstein M. Thinking about the cerebellum. Brain 2006;129: 288–92.
Glickstein M, Doron K. Cerebellum: connections and functions. Cerebellum. 2008;7:589–94.
Glickstein M, Gerrits N, Kralj-Hans I, Mercier B, Stein J, Voogd J. Visual pontocerebellar projections in the macaque. J Comp Neurol. 1994;349:51–72.
Glickstein M, May 3rd JG, Mercier BE. Corticopontine projection in the macaque: the distribution of labelled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. J Comp Neurol. 1985;235:343–59.
Glickstein M, Sultan F, Voogd J. Functional localization in the cerebellum. Cortex. 2011;47(1):59–80.
Gottlieb J. From thought to action: the parietal cortex as a bridge between perception, action, and cognition. Neuron. 2007;53:9–16.
Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci. 2009;29:8586–94.
Hamani C, Mayberg H, Snyder B, Giacobbe P, Kennedy S, Lozano AM. Deep brain stimulation of the subcallosal cingulate gyrus for depression: anatomical location of active contacts in clinical responders and a suggested guideline for targeting. J Neurosurg. 2009;111:1209–15.
He SQ, Dum RP, Strick PL. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci. 1995;15:3284–306.
Holloway R. Evolution of the human brain. In: Lock A, Peter CR, editors. Handbook of human symbolic evolution. Malden: Blackwell Publishers Inc; 1999. p. 74–125.
Jones DK. Studying connections in the living human brain with diffusion MRI. Cortex. 2008;44:936–52.
Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23:8432–44.
Klein JT, Deaner RO, Platt ML. Neural correlates of social target value in macaque parietal cortex. Curr Biol. 2008;18:419–24.
Koechlin E, Ody C, Kouneiher F. The architecture of cognitive control in the human prefrontal cortex. Science. 2003;302:1181–5.
Krienen FM, Buckner RL. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex. 2009;19:2485–97.
Kuypers HGJM, Ugolini G. Viruses as transneuronal tracers. Trends Neurosci. 1990;13:71–5.
Larsell O. Comparative anatomy and histology of the cerebellum from monotremes through apes. Minneapolis: University of Minnesota Press; 1970.
Larsell O, Jansen O. The comparative anatomy and histology of the cerebellum: the human cerebellum, cerebellar connections and cerebellar cortex. Minneapolis: The University of Minnesota Press; 1972.
Le Bihan D. Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci. 2003;4:469–80.
Leiner HC, Leiner AL, Dow RS. Does the cerebellum contribute to mental skills? Behav Neurosci. 1986;100:443–54.
Levin PM. The efferent fibres of the frontal lobe of the monkey, Macaca mulatta. J Comp Neurol. 1936;63:369–419.
Lewis JW, Van Essen DC. J Com Neurol. 2000;428:79–111.
Lu X, Miyachi S, Ito Y, Nambu A, Takada M. Topographic distribution of output neurons in cerebellar nuclei and cortex to somatotopic map of primary motor cortex. Eur J Neurosci. 2007;25:2374–82.
Lynch JC, Hoover JE, Strick PL. Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp Brain Res. 1994;100:181–6.
Matano S. Brief communication: proportions of the ventral half of the cerebellar dentate nucleus in humans and great apes. Am J Phys Anthropol. 2001;114:163–5.
Mayberg HS, Lozano AM, Voon V, McNeely HE, Seminowicz D, et al. Deep brain stimulation for treatment-resistant depression. Neuron. 2005;45:651–60.
Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci. 2001;21:700–12.
Middleton FA, Strick PL. Cerebellar output channels. Int Rev Neurobiol. 1997;41:61–82.
Miller EK. The prefrontal cortex and cognitive control. Nat Rev Neurosci. 2000;1:59–65.
Miller EK, Cohen JD. An integrative theory of prefrontal cortex function. Annu Rev Neurosci. 2001;24:167–202.
Miller EK, Freedman DJ, Wallis JD. The prefrontal cortex: categories, concepts and cognition. Philos Trans R Soc Lond B Biol Sci. 2002;357:1123–36.
O’Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H. Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex. 2009;20:953–65.
Ohara S, Inoue K, Witter M, Iijima T. Untangling neural networks with dual retrograde transsynaptic viral infection. Front Neurosci. 2009;3:344–9.
Orban GA, Van Essen D, Vanduffel W. Comparative mapping of higher visual areas in monkeys and humans. Trends Cogn Sci. 2004;8:315–24.
Orioli PJ, Strick PL. Cerebellar connections with the motor cortex and the arcuate premotor area: an analysis employing retrograde transneuronal transport of WGA-HRP. J Comp Neurol. 1989;288:612–26.
Passingham RE, Stephan KE, Kotter R. The anatomical basis of functional localization in the cortex. Nat Rev Neurosci. 2002;3:606–16.
Platt ML, Glimcher PW. Neural correlates of decision variables in parietal cortex. Nature. 1999;400:233–8.
Petrides M, Pandya DN. Comparative architectonic analysis of the human and the macaque frontal cortex. In: Boller, F., Grafman, J. (Eds.), Handbook of Neuropsychology. Elsevier, Amsterdam; 1994. pp. 17–58.
Prevosto V, Graf W, Ugolini G. Cerebellar inputs to intraparietal cortex areas LIP and MIP: functional frameworks for adaptive control of eye movements, reaching, and arm/eye/head movement coordination. Cereb Cortex. 2010;20:214–28.
Ramnani N. The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci. 2006;7:511–22.
Ramnani N, Behrens TEJ, Johansen-Berg H, Richter MC, Pinsk MA, et al. The evolution of prefrontal inputs to the cortico-pontine system: diffusion imaging evidence from macaque monkeys and humans. Cereb Cortex. 2006;16:811–8.
Ramnani N, Owen AM. Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci. 2004;5:184–94.
Rorie AE, Gao J, McClelland JL, Newsome WT. Integration of sensory and reward information during perceptual decision-making in lateral intraparietal cortex (LIP) of the macaque monkey. PLoS One.2011;5: e9308 (in press)
Rutishauser F. Experimenteller Beitrage zur Stabkranzfaserung im Frontalhirn des Affen. Monatschrift fur Psychiatrie und Neurologie. 1899;5:161–79.
Schall JD. The neural selection and control of saccades by the frontal eye field. Philos Trans R Soc Lond B Biol Sci. 2002;357:1073–82.
Schmahmann JD, Pandya DN. Anatomical investigation of projections to the basis pontis from posterior parietal association cortices in rhesus monkey. J Comp Neurol. 1989;289:53–73.
Schmahmann JD, Pandya DN. Projections to the basis pontis from the superior temporal sulcus and superior temporal region in the rhesus monkey. J Comp Neurol. 1991;308:224–48.
Schmahmann JD, Pandya DN. Course of the fiber pathways to pons from parasensory association areas in the rhesus monkey. J Comp Neurol. 1992;326:159–79.
Schmahmann JD, Pandya DN. Prelunate, occipitotemporal, and parahippocampal projections to the basis pontis in rhesus monkey. J Comp Neurol. 1993;337:94–112.
Schmahmann JD, Pandya DN. Prefrontal cortex projections to the basilar pons in rhesus monkey: implications for the cerebellar contribution to higher function. Neurosci Lett. 1995;199:175–8.
Schmahmann JD, Pandya DN. Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J Neurosci. 1997;17:438–58.
Schmahmann JD, Rosene DL, Pandya DN. Motor projections to the basis pontis in rhesus monkey. J Comp Neurol. 2004;478:248–68.
Seo H, Barraclough DJ, Lee D. Lateral intraparietal cortex and reinforcement learning during a mixed-strategy game. J Neurosci. 2009;29:7278–89.
Snyder LH, Batista AP, Andersen RA. Intention-related activity in the posterior parietal cortex: a review. Vis Res. 2000;40:1433–41.
Streidter GF. Evolutionary changes in brain region size. In: Principles of brain evolution. Sunderland, MA: Sinauer Associates; 2005.
Strick PL, Dum RP, Fiez JA. Cerebellum and nonmotor function. Annu Rev Neurosci. 2009;32:413–34.
Sultan F, Hamodeh S, Baizer JS. The human dentate nucleus: a complex shape untangled. Neuroscience. 2010;167:965–8.
Sunderland S. The projection of the cerebral cortex on the pons and cerebellum in the macaque monkey. J Anat. 1940;74(201–26):1.
Tehovnik EJ, Sommer MA, Chou IH, Slocum WM, Schiller PH. Eye fields in the frontal lobes of primates. Brain Res Brain Res Rev. 2000;32:413–48.
Tsujimoto S, Genovesio A, Wise SP. Evaluating self-generated decisions in frontal pole cortex of monkeys. Nat Neurosci. 2010;13(1):120–26.
Ugolini G, Kuypers HGJM. Collaterals of corticospinal and pyramidal fibers to the pontine gray demonstrated by a new application of the fluorescent fiber labeling technique. Brain Res. 1986;365:211–27.
Vogt BA, Pandya DN. Cingulate cortex of the rhesus monkey: II. Cortical afferents. J Comp Neurol. 1987. 262(2):271-89.
Walker AE. A cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol. 1940;73:59–86.
Wise SP. The primate premotor cortex: past, present, and preparatory. Annu Rev Neurosci. 1985;8:1–19
Wolpert DM, Miall RC. Forward models for physiological motor control. Neural Netw. 1996;9:1265–79.
Yacoub E, Harel N, Ugurbil K. High-field fMRI unveils orientation columns in humans. Proc Natl Acad Sci USA. 2008;105:10607–12.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ramnani, N. Frontal Lobe and Posterior Parietal Contributions to the Cortico-cerebellar System. Cerebellum 11, 366–383 (2012). https://doi.org/10.1007/s12311-011-0272-3
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12311-011-0272-3