Cellular-resolution Mapping Uncovers Spatial Adaptive Filtering at the Rat Cerebellum Input Stage

Overview

Journal Commun Biol

Specialty Biology

Date 2020 Oct 31

PMID 33128000

Citations 14

Authors

Stefano Casali

Marialuisa Tognolina

Daniela Gandolfi

Jonathan Mapelli

Egidio DAngelo

Affiliations

Soon will be listed here.

Abstract

Long-term synaptic plasticity is thought to provide the substrate for adaptive computation in brain circuits but very little is known about its spatiotemporal organization. Here, we combined multi-spot two-photon laser microscopy in rat cerebellar slices with realistic modeling to map the distribution of plasticity in multi-neuronal units of the cerebellar granular layer. The units, composed by ~300 neurons activated by ~50 mossy fiber glomeruli, showed long-term potentiation concentrated in the core and long-term depression in the periphery. This plasticity was effectively accounted for by an NMDA receptor and calcium-dependent induction rule and was regulated by the inhibitory Golgi cell loops. Long-term synaptic plasticity created effective spatial filters tuning the time-delay and gain of spike retransmission at the cerebellum input stage and provided a plausible basis for the spatiotemporal recoding of input spike patterns anticipated by the motor learning theory.

Citing Articles

Understanding Cerebellar Input Stage through Computational and Plasticity Rules.

Pali E, DAngelo E, Prestori F Biology (Basel). 2024; 13(6).

PMID: 38927283 PMC: 11200477. DOI: 10.3390/biology13060403.

Mesoscale simulations predict the role of synergistic cerebellar plasticity during classical eyeblink conditioning.

Geminiani A, Casellato C, Boele H, Pedrocchi A, De Zeeuw C, DAngelo E PLoS Comput Biol. 2024; 20(4):e1011277.

PMID: 38574161 PMC: 11060558. DOI: 10.1371/journal.pcbi.1011277.

A multi-layer mean-field model of the cerebellum embedding microstructure and population-specific dynamics.

Lorenzi R, Geminiani A, Zerlaut Y, De Grazia M, Destexhe A, Wheeler-Kingshott C PLoS Comput Biol. 2023; 19(9):e1011434.

PMID: 37656758 PMC: 10501640. DOI: 10.1371/journal.pcbi.1011434.

Long-Term Synaptic Plasticity Tunes the Gain of Information Channels through the Cerebellum Granular Layer.

Mapelli J, Boiani G, DAngelo E, Bigiani A, Gandolfi D Biomedicines. 2022; 10(12).

PMID: 36551941 PMC: 9775043. DOI: 10.3390/biomedicines10123185.

Computational models of neurotransmission at cerebellar synapses unveil the impact on network computation.

Masoli S, Rizza M, Tognolina M, Prestori F, DAngelo E Front Comput Neurosci. 2022; 16:1006989.

PMID: 36387305 PMC: 9649760. DOI: 10.3389/fncom.2022.1006989.

References

Gall D, Prestori F, Sola E, DErrico A, Roussel C, Forti L . Intracellular calcium regulation by burst discharge determines bidirectional long-term synaptic plasticity at the cerebellum input stage. J Neurosci. 2005; 25(19):4813-22. PMC: 6724778. DOI: 10.1523/JNEUROSCI.0410-05.2005. View

Valera A, Binda F, Pawlowski S, Dupont J, Casella J, Rothstein J . Stereotyped spatial patterns of functional synaptic connectivity in the cerebellar cortex. Elife. 2016; 5. PMC: 4805550. DOI: 10.7554/eLife.09862. View

DAngelo E, Antonietti A, Casali S, Casellato C, Garrido J, Luque N . Modeling the Cerebellar Microcircuit: New Strategies for a Long-Standing Issue. Front Cell Neurosci. 2016; 10:176. PMC: 4937064. DOI: 10.3389/fncel.2016.00176. View

DAngelo E, De Filippi G, Rossi P, Taglietti V . Synaptic excitation of individual rat cerebellar granule cells in situ: evidence for the role of NMDA receptors. J Physiol. 1995; 484 ( Pt 2):397-413. PMC: 1157902. DOI: 10.1113/jphysiol.1995.sp020673. View

Mitchell S, Silver R . Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron. 2003; 38(3):433-45. DOI: 10.1016/s0896-6273(03)00200-9. View

Gal E, London M, Globerson A, Ramaswamy S, Reimann M, Muller E . Rich cell-type-specific network topology in neocortical microcircuitry. Nat Neurosci. 2017; 20(7):1004-1013. DOI: 10.1038/nn.4576. View

Arleo A, Nieus T, Bezzi M, DErrico A, DAngelo E, Coenen O . How synaptic release probability shapes neuronal transmission: information-theoretic analysis in a cerebellar granule cell. Neural Comput. 2010; 22(8):2031-58. DOI: 10.1162/NECO_a_00006-Arleo. View

Pozzi P, Gandolfi D, Tognolina M, Chirico G, Mapelli J, DAngelo E . High-throughput spatial light modulation two-photon microscopy for fast functional imaging. Neurophotonics. 2015; 2(1):015005. PMC: 4478992. DOI: 10.1117/1.NPh.2.1.015005. View

Jorntell H, Ekerot C . Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J Neurosci. 2006; 26(45):11786-97. PMC: 6674774. DOI: 10.1523/JNEUROSCI.2939-06.2006. View

10.

Straub I, Witter L, Eshra A, Hoidis M, Byczkowicz N, Maas S . Gradients in the mammalian cerebellar cortex enable Fourier-like transformation and improve storing capacity. Elife. 2020; 9. PMC: 7002074. DOI: 10.7554/eLife.51771. View

11.

Harvey R, Napper R . Quantitative studies on the mammalian cerebellum. Prog Neurobiol. 1991; 36(6):437-63. DOI: 10.1016/0301-0082(91)90012-p. View

12.

Mapelli J, DAngelo E . The spatial organization of long-term synaptic plasticity at the input stage of cerebellum. J Neurosci. 2007; 27(6):1285-96. PMC: 6673576. DOI: 10.1523/JNEUROSCI.4873-06.2007. View

13.

Billings G, Piasini E, Lorincz A, Nusser Z, Silver R . Network structure within the cerebellar input layer enables lossless sparse encoding. Neuron. 2014; 83(4):960-74. PMC: 4148198. DOI: 10.1016/j.neuron.2014.07.020. View

14.

Sgritta M, Locatelli F, Soda T, Prestori F, Ugo DAngelo E . Hebbian Spike-Timing Dependent Plasticity at the Cerebellar Input Stage. J Neurosci. 2017; 37(11):2809-2823. PMC: 6596728. DOI: 10.1523/JNEUROSCI.2079-16.2016. View

15.

Cerminara N, Lang E, Sillitoe R, Apps R . Redefining the cerebellar cortex as an assembly of non-uniform Purkinje cell microcircuits. Nat Rev Neurosci. 2015; 16(2):79-93. PMC: 4476393. DOI: 10.1038/nrn3886. View

16.

Xu L, Anwyl R, Rowan M . Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature. 1998; 394(6696):891-4. DOI: 10.1038/29783. View

17.

Cesana E, Pietrajtis K, Bidoret C, Isope P, DAngelo E, Dieudonne S . Granule cell ascending axon excitatory synapses onto Golgi cells implement a potent feedback circuit in the cerebellar granular layer. J Neurosci. 2013; 33(30):12430-46. PMC: 6618671. DOI: 10.1523/JNEUROSCI.4897-11.2013. View

18.

Wagner M, Kim T, Savall J, Schnitzer M, Luo L . Cerebellar granule cells encode the expectation of reward. Nature. 2017; 544(7648):96-100. PMC: 5532014. DOI: 10.1038/nature21726. View

19.

Sola E, Prestori F, Rossi P, Taglietti V, DAngelo E . Increased neurotransmitter release during long-term potentiation at mossy fibre-granule cell synapses in rat cerebellum. J Physiol. 2004; 557(Pt 3):843-61. PMC: 1665150. DOI: 10.1113/jphysiol.2003.060285. View

20.

Diwakar S, Lombardo P, Solinas S, Naldi G, DAngelo E . Local field potential modeling predicts dense activation in cerebellar granule cells clusters under LTP and LTD control. PLoS One. 2011; 6(7):e21928. PMC: 3139583. DOI: 10.1371/journal.pone.0021928. View