Optogenetics application to cerebellar investigations in vivo: Comparison
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The cerebellum is most renowned for its role in sensorimotor control and coordination, but a growing number of anatomical and physiological studies are demonstrating its deep involvement in cognitive and emotional functions. Recently, the development and refinement of optogenetic techniques boosted research in the cerebellar field and, impressively, revolutionized the methodological approach and endowed the investigations with entirely new capabilities. This translated into a significant improvement in the data acquired for sensorimotor tests, allowing one to correlate single-cell activity with motor behavior to the extent of determining the role of single neuronal types and single connection pathways in controlling precise aspects of movement kinematics. These levels of specificity in correlating neuronal activity to behavior could not be achieved in the past, when electrical and pharmacological stimulations were the only available experimental tools. The application of optogenetics to the investigation of the cerebellar role in higher-order and cognitive functions, which involves a high degree of connectivity with multiple brain areas, has been even more significant. It is possible that, in this field, optogenetics has changed the game, and the number of investigations using optogenetics to study the cerebellar role in non-sensorimotor functions in awake animals is growing. The main issues addressed by these studies are the cerebellar role in epilepsy (through connections to the hippocampus and the temporal lobe), schizophrenia and cognition, working memory for decision making, and social behavior. It is also worth noting that optogenetics opened a new perspective for cerebellar neurostimulation in patients (e.g., for epilepsy treatment and stroke rehabilitation), promising unprecedented specificity in the targeted pathways that could be either activated or inhibited.

  • cerebellum
  • optogenetics
  • sensorimotor system
  • non-sensorimotor functions
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References

  1. Malacarne, V. Nuova Esposizione della Vera Struttura del Cervelletto Umano; Briolo, Eds.; Appresso Giammichele Briolo nella contrada de’guardinfanti: Torino, Italy, 1776; pp. 129.
  2. Flourens, P. Recherchers experimentales sur le proprietes et les functions du systeme nerveux dans les animaux vertebres; Crevot: Paris, 1824; pp. -.
  3. Schmahmann, J.D.; Sherman, J.C; The cerebellar cognitive affective syndrome. British Journal of Hospital Medicine 1998, 121 ( Pt 4), 561-579, 10.1093/brain/121.4.561.
  4. Schmahmann, J.D; Dysmetria of thought: clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn Sci 1998, 2, 362-371, 10.1016/s1364-6613(98)01218-2.
  5. Timmann, D; On the mechanism of cerebellar contributions to cognition. Fortschr. Neurol. Psychiatr. 2012, 80, 44-52, 10.1055/s-0031-1282022.
  6. Baillieux, H.; De Smet, H.J.; Paquier, P.F.; De Deyn, P.P; Cerebellar neurocognition: Insights into the bottom of the brain. Clinical Neurology and Neurosurgery 2008, 110, 763-773, 10.1016/j.clineuro.2008.05.013.
  7. Gottwald, B.; Wilde, B.; Mihajlovic, Z.; Mehdorn, H.M; Evidence for distinct cognitive deficits after focal cerebellar lesions. J. Neurol. Neurosurg. Psychiatry 2004, 75, 1524-1531, 10.1136/jnnp.2003.018093.
  8. Schmahmann, J.D; Disorders of the Cerebellum: Ataxia, Dysmetria of Thought, and the Cerebellar Cognitive Affective Syndrome. J. Neuropsychiatry Clin. Neurosci. 2004, 16, 367-378, 10.1176/appi.neuropsych.16.3.367.
  9. Manto, M; Cerebellar motor syndrome from children to the elderly.. Handb. Clin. Neurol. 2018, 154, 151-166, 10.1016/B978-0-444-63956-1.00009-6.
  10. Prestori, F.; Mapelli, L.; D’Angelo, E; Diverse Neuron Properties and Complex Network Dynamics in the Cerebellar Cortical Inhibitory Circuit.. Front. Mol. Neurosci. 2019, 12, 267, 10.3389/fnmol.2019.00267.
  11. D’Angelo, E.; Solinas, S.; Mapelli, J.; Gandolfi, D.; Mapelli, L.; Prestori, F; The cerebellar Golgi cell and spatiotemporal organization of granular layer activity. Front. Neural Circuits 2013, 7, 93, 10.3389/fncir.2013.00093.
  12. Mapelli, L.; Solinas, S.; D’Angelo, E; Integration and regulation of glomerular inhibition in the cerebellar granular layer circuit. Front. Cell. Neurosci. 2014, 8, 55, 10.3389/fncel.2014.00055.
  13. Apps, R.; Hawkes, R.; Aoki, S.; Bengtsson, F.; Brown, A.M.; Chen, G.; Ebner, T.J.; Isope, P.; Jörntell, H.; Lackey, E.P; et al. Cerebellar Modules and Their Role as Operational Cerebellar Processing Units: A Consensus paper [corrected].. Cerebellum 2018, 17, 654-682, 10.1007/s12311-018-0952-3.
  14. Leto, K.; Arancillo, M.; Becker, E.B.; Buffo, A.; Chiang, C.; Ding, B.; Dobyns, W.B.; Dusart, I.; Haldipur, P.; Hatten, M.E; et al. Consensus Paper: Cerebellar Development.. Cerebellum 2016, 15, 789-828, 10.1007/s12311-015-0724-2.
  15. Marzban, H.; Del Bigio, M.R.; Alizadeh, J.; Ghavami, S.; Zachariah, R.M.; Rastegar, M; Cellular commitment in the developing cerebellum. Front. Cell. Neurosci. 2014, 8, 450, 10.3389/fncel.2014.00450.
  16. Kim, C.K.; Adhikari, A.; Deisseroth, K; Integration of optogenetics with complementary methodologies in systems neuroscience. Nature Reviews Neuroscience 2017, 18, 222-235, 10.1038/nrn.2017.15.
  17. Proville, R.D.; Spolidoro, M.; Guyon, N.; Dugue, G.P.; Selimi, F.; Isope, P.; Popa, D.; Lena, C; Cerebellum involvement in cortical sensorimotor circuits for the control of voluntary movements. Nature Neuroscience 2014, 17, 1233-1239, 10.1038/nn.3773.
  18. Kelly, R.M.; Strick, P.L; Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate. J. Neurosci. 2003, 23, 8432-8444, 10.1523/JNEUROSCI.23-23-08432.2003.
  19. Albergaria, C.; Silva, N.T.; Pritchett, D.L.; Carey, M.R; Locomotor activity modulates associative learning in mouse cerebellum. Nat. Neurosci. 2018, 21, 725–735.
  20. Gao, Z.; Proietti-Onori, M.; Lin, Z.; Ten Brinke, M.M.; Boele, H.J.; Potters, J.W.; Ruigrok, T.J.; Hoebeek, F.E.; De Zeeuw, C.I; Excitatory Cerebellar Nucleocortical Circuit Provides Internal Amplification during Associative Conditioning.. Neuron 2016, 89, 645-657, 10.1016/j.neuron.2016.01.008.
  21. El-Shamayleh, Y.; Kojima, Y.; Soetedjo, R.; Horwitz, G.D; Selective Optogenetic Control of Purkinje Cells in Monkey Cerebellum.. Neuron 2017, 95, 51-62.e54, 10.1016/j.neuron.2017.06.002.
  22. Sarnaik, R.; Raman, I.M; Control of voluntary and optogenetically perturbed locomotion by spike rate and timing of neurons of the mouse cerebellar nuclei. eLife 2018, 7, e29546, 10.7554/eLife.29546.
  23. Payne, H.L.; French, R.L.; Guo, C.C.; Nguyen-Vu, T.B.; Manninen, T.; Raymond, J.L; Cerebellar Purkinje cells control eye movements with a rapid rate code that is invariant to spike irregularity.. eLife 2019, 8, -, 10.7554/eLife.37102.
  24. Jelitai, M.; Puggioni, P.; Ishikawa, T.; Rinaldi, A.; Duguid, I; Dendritic excitation–inhibition balance shapes cerebellar output during motor behaviour. Nature Communications 2016, 7, 13722, 10.1038/ncomms13722.
  25. Chen, C.H.; Fremont, R.; Arteaga-Bracho, E.E.; Khodakhah, K; Short latency cerebellar modulation of the basal ganglia. Nature Neuroscience 2014, 17, 1767-1775, 10.1038/nn.3868.
  26. Van Overwalle, F.; D'Aes, T.; Marien, P; Social cognition and the cerebellum: A meta‐analytic connectivity analysis. Human Brain Mapping 2015, 36, 5137-5154, 10.1002/hbm.23002.
  27. Moulton, E.A.; Elman, I.; Becerra, L.R.; Goldstein, R.Z.; Borsook, D; The cerebellum and addiction: insights gained from neuroimaging research.. Addict. Biol. 2014, 19, 317-331, 10.1111/adb.12101.
  28. Schmahmann, J.D.; Caplan, D; Cognition, emotion and the cerebellum.. Brain 2006, 129, 290-292, 10.1093/brain/awh729.
  29. D'Angelo, E; The cerebellum gets social. Science 2019, 363, 229, 10.1126/science.aaw2571.
  30. Courchesne, E; Brainstem, cerebellar and limbic neuroanatomical abnormalities in autism. Current Opinion in Neurobiology 1997, 7, 568, 10.1016/s0959-4388(97)80038-4.
  31. Soda, T.; Mapelli, L.; Locatelli, F.; Botta, L.; Goldfarb, M.; Prestori, F.; D'Angelo, E; Hyperexcitability and Hyperplasticity Disrupt Cerebellar Signal Transfer in the IB2 KO Mouse Model of Autism.. J. Neurosci. 2019, 39, 2383-2397, 10.1523/JNEUROSCI.1985-18.2019.
  32. Badura, A.; Verpeut, J.L.; Metzger, J.W.; Pereira, T.D.; Pisano, T.J.; Deverett, B.; Bakshinskaya, D.E.; Wang, S.S; Normal cognitive and social development require posterior cerebellar activity. eLife 2018, 7, -, 10.7554/eLife.36401.
  33. Wang, S.S.; Kloth, A.D.; Badura, A; The cerebellum, sensitive periods, and autism.. Neuron 2014, 83, 518-532, 10.1016/j.neuron.2014.07.016.
  34. Andreasen, N.C.; Pierson, R; The Role of the Cerebellum in Schizophrenia. Biol. Psychiatry. 2008, 64, 81-88, 10.1016/j.biopsych.2008.01.003.
  35. Picard, H.; Amado, I.; Mouchet-Mages, S.; Olie, J.P.; Krebs, M.O; The Role of the Cerebellum in Schizophrenia: an Update of Clinical, Cognitive, and Functional Evidences. Schizophr. Bull. 2008, 34, 155-172, 10.1093/schbul/sbm049.
  36. Giza, J.; Urbanski, M.J.; Prestori, F.; Bandyopadhyay, B.; Yam, A.; Friedrich, V.; Kelley, K.; D'Angelo, E.; Goldfarb, M; Behavioral and cerebellar transmission deficits in mice lacking the autism-linked gene islet brain-2.. J. Neurosci. 2010, 30, 14805-14816, 10.1523/JNEUROSCI.1161-10.2010.
  37. Whyatt, C.; Craig, C; Sensory-motor problems in Autism. Front. Integr. Neurosci. 2013, 7, 51, 10.3389/fnint.2013.00051.
  38. Schmahmann, J.D.; Guell, X.; Stoodley, C.J.; Halko, M.A; The Theory and Neuroscience of Cerebellar Cognition. Annu. Rev. Neurosci. 2019, 42, 337-364, 10.1146/annurev-neuro-070918-050258.
  39. Strick, P.L.; Dum, R.P.; Fiez, J.A; Cerebellum and Nonmotor Function. Annual Review of Neuroscience 2009, 32, 413-434, 10.1146/annurev.neuro.31.060407.125606.
  40. Dum, R.P.; Strick, P.L; An Unfolded Map of the Cerebellar Dentate Nucleus and its Projections to the Cerebral Cortex. Journal of Neurophysiology 2003, 89, 634-639, 10.1152/jn.00626.2002.
  41. Steele, C.J.; Anwander, A.; Bazin, P.L.; Trampel, R.; Schaefer, A.; Turner, R.; Ramnani, N.; Villringer, A; Human Cerebellar Sub-millimeter Diffusion Imaging Reveals the Motor and Non-motor Topography of the Dentate Nucleus. Cerebral Cortex 2017, 27, 4537-4548, 10.1093/cercor/bhw258.
  42. Bernard, J.A.; Peltier, S.J.; Benson, B.L.; Wiggins, J.L.; Jaeggi, S.M.; Buschkuehl, M.; Jonides, J.; Monk, C.S.; Seidler, R.D; Dissociable Functional Networks of the Human Dentate Nucleus. Cerebral Cortex 2013, 24, 2151-2159, 10.1093/cercor/bht065.
  43. Magnotta, V.A.; Adix, M.L.; Caprahan, A.; Lim, K.; Gollub, R.; Andreasen, N.C; Investigating connectivity between the cerebellum and thalamus in schizophrenia using diffusion tensor tractography: a pilot study. Psychiatry Research 2008, 163, 193-200, 10.1016/j.pscychresns.2007.10.005.
  44. Gornati, S.V.; Schafer, C.B.; Eelkman Rooda, O.H.J.; Nigg, A.L.; De Zeeuw, C.I.; Hoebeek, F.E; Differentiating Cerebellar Impact on Thalamic Nuclei. Cell Reports 2018, 23, 2690-2704, 10.1016/j.celrep.2018.04.098.
  45. Parnaudeau, S.; O'Neill, P.K.; Bolkan, S.S.; Ward, R.D.; Abbas, A.I.; Roth, B.L.; Balsam, P.D.; Gordon, J.A.; Kellendonk, C; Inhibition of mediodorsal thalamus disrupts thalamofrontal connectivity and cognition.. Neuron 2013, 77, 1151-62, 10.1016/j.neuron.2013.01.038.
  46. Ferguson, B.R.; Gao, W.J; Thalamic Control of Cognition and Social Behavior Via Regulation of Gamma-Aminobutyric Acidergic Signaling and Excitation/Inhibition Balance in the Medial Prefrontal Cortex. Biological Psychiatry 2018, 83, 657-669, 10.1016/j.biopsych.2017.11.033.
  47. Sieveritz, B.; Garcia-Munoz, M.; Arbuthnott, G.W; Thalamic afferents to prefrontal cortices from ventral motor nuclei in decision‐making. European Journal of Neuroscience 2018, 49, 646-657, 10.1111/ejn.14215.
  48. Collins, D.P.; Anastasiades, P.G.; Marlin, J.J.; Carter, A.G; Reciprocal Circuits Linking the Prefrontal Cortex with Dorsal and Ventral Thalamic Nuclei. Neuron 2018, 98, 366-379.e4, 10.1016/j.neuron.2018.03.024.
  49. Rogers, T.D.; Dickson, P.E.; McKimm, E.; Heck, D.H.; Goldowitz, D.; Blaha, C.D.; Mittleman, G; Reorganization of circuits underlying cerebellar modulation of prefrontal cortical dopamine in mouse models of autism spectrum disorder.. The Cerebellum 2013, 12, 547-56, 10.1007/s12311-013-0462-2.
  50. Thierry, A.M.; Tassin, J.P.; Blanc, G.; Glowinski, J; Selective activation of mesocortical DA system by stress.. Nature 1976, 263, 242-244, 10.1038/263242a0.
  51. Brozoski, T.J.; Brown, R.M.; Rosvold, H.E.; Goldman, P.S; Cognitive deficit caused by regional depletion of dopamine in prefrontal cortex of rhesus monkey. Science 1979, 205, 929-932, 10.1126/science.112679.
  52. Y Chudasama; Trevor W. Robbins; Dopaminergic Modulation of Visual Attention and Working Memory in the Rodent Prefrontal Cortex. Neuropsychopharmacology 2004, 29, 1628-1636, 10.1038/sj.npp.1300490.
  53. Stan B Floresco; Prefrontal dopamine and behavioral flexibility: shifting from an “inverted-U” toward a family of functions. Frontiers in Neuroscience 2013, 7, 62, 10.3389/fnins.2013.00062.
  54. Braver, T.S.; Krug, M.K.; Chiew, K.S.; Kool, W.; Westbrook, J.A.; Clement, N.J.; Adcock, R.A.; Barch, D.M.; Botvinick, M.M.; Carver, C.S; et al. Mechanisms of motivation-cognition interaction: challenges and opportunities. Cogn. Affect. Behav. Neurosci. 2014, 14, 443-472, 10.1002/chin.201338012.
  55. Andrew Westbrook; Todd S. Braver; Dopamine Does Double Duty in Motivating Cognitive Effort. Neuron 2016, 91, 708, 10.1016/j.neuron.2016.07.020.
  56. Oliver D. Howes; Shitij Kapur; The Dopamine Hypothesis of Schizophrenia: Version III—The Final Common Pathway. Schizophrenia Bulletin 2009, 35, 549-562, 10.1093/schbul/sbp006.
  57. M Ernst; Alan J. Zametkin; J A Matochik; D Pascualvaca; R M Cohen; Low medial prefrontal dopaminergic activity in autistic children.. The Lancet 1997, 350, 638, 10.1016/s0140-6736(05)63326-0.
  58. Nakamura, K.; Sekine, Y.; Ouchi, Y.; Tsujii, M.; Yoshikawa, E.; Futatsubashi, M.; Tsuchiya, K.J.; Sugihara, G.; Iwata, Y.; Suzuki, K; et al. Brain Serotonin and Dopamine Transporter Bindings in Adults With High-Functioning Autism. Archives of General Psychiatry 2010, 67, 59-68, 10.1001/archgenpsychiatry.2009.137.
  59. Guy Mittleman; Daniel Goldowitz; Detlef H Heck; Charles Blaha; Cerebellar modulation of frontal cortex dopamine efflux in mice: relevance to autism and schizophrenia.. Synapse 2008, 62, 544-50, 10.1002/syn.20525.
  60. Tiffany D. Rogers; Price E. Dickson; Detlef H Heck; Daniel Goldowitz; Guy Mittleman; Charles Blaha; Connecting the dots of the cerebro-cerebellar role in cognitive function: neuronal pathways for cerebellar modulation of dopamine release in the prefrontal cortex.. Synapse 2011, 65, 1204-12, 10.1002/syn.20960.
  61. Ilaria Carta; Christopher H. Chen; Amanda L. Schott; Schnaude Dorizan; Kamran Khodakhah; Cerebellar modulation of the reward circuitry and social behavior. Science 2019, 363, -, 10.1126/science.aav0581.
  62. Ben Deverett; Mikhail Kislin; David W. Tank; Samuel S.-H. Wang; Cerebellar disruption impairs working memory during evidence accumulation.. Nature Communications 2019, 10, 3128, 10.1038/s41467-019-11050-x.
  63. Krystal Parker; Nandakumar S. Narayanan; Nancy C. Andreasen; The therapeutic potential of the cerebellum in schizophrenia. Frontiers in Systems Neuroscience 2014, 8, 63, 10.3389/fnsys.2014.00163.
  64. Krystal Parker; Timing Tasks Synchronize Cerebellar and Frontal Ramping Activity and Theta Oscillations: Implications for Cerebellar Stimulation in Diseases of Impaired Cognition. Frontiers in Psychology 2015, 6, 190, 10.3389/fpsyt.2015.00190.
  65. Krystal Parker; Youngcho Kim; R M Kelley; A J Nessler; K-H Chen; V A Muller-Ewald; Nancy C. Andreasen; Nandakumar S. Narayanan; Delta-frequency stimulation of cerebellar projections can compensate for schizophrenia-related medial frontal dysfunction.. Molecular Psychiatry 2017, 22, 647-655, 10.1038/mp.2017.50.
  66. Esther I. Krook-Magnuson; Peijun Li; Scott M. Paluszkiewicz; Molly M. Huntsman; Tonically active inhibition selectively controls feedforward circuits in mouse barrel cortex.. Journal of Neurophysiology 2008, 100, 932-44, 10.1152/jn.01360.2007.
  67. Streng, M.L.; Krook-Magnuson, E; Excitation, but not inhibition, of the fastigial nucleus provides powerful control over temporal lobe seizures.. J. Physiol. 2020, 598, 171-187, 10.1113/JP278747.
  68. Kros, L.; Eelkman Rooda, O.H.; Spanke, J.K.; Alva, P.; van Dongen, M.N.; Karapatis, A.; Tolner, E.A.; Strydis, C.; Davey, N.; Winkelman, B.H; et al. Cerebellar output controls generalized spike‐and‐wave discharge occurrence. Annals of Neurology 2015, 77, 1027-1049, 10.1002/ana.24399.
  69. Krook-Magnuson, E.; Szabo, G.G.; Armstrong, C.; Oijala, M.; Soltesz, I; Cerebellar Directed Optogenetic Intervention Inhibits Spontaneous Hippocampal Seizures in a Mouse Model of Temporal Lobe Epilepsy. eneuro 2014, 1, null, 10.1523/eneuro.0005-14.2014.
  70. T. Tsubota; Y. Ohashi; Keita Tamura; Yasushi Miyashita; Optogenetic inhibition of Purkinje cell activity reveals cerebellar control of blood pressure during postural alterations in anesthetized rats. Neuroscience 2012, 210, 137-144, 10.1016/j.neuroscience.2012.03.014.
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