4.6 Article

Neurons of the inferior olive respond to broad classes of sensory input while subject to homeostatic control

Journal

JOURNAL OF PHYSIOLOGY-LONDON
Volume 597, Issue 9, Pages 2483-2514

Publisher

WILEY
DOI: 10.1113/JP277413

Keywords

cerebellum; inferior olive; homeostatic mechanisms; sensory integration; Purkinje cell; climbing fibre

Funding

  1. Netherlands Organization for Scientific Research (NWO-ALW)
  2. Dutch Organization for Medical Sciences (ZonMW)
  3. Life Sciences
  4. ERC-adv
  5. ERC-POC
  6. China Scholarship Council [2010623033]

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Cerebellar Purkinje cells integrate sensory information with motor efference copies to adapt movements to behavioural and environmental requirements. They produce complex spikes that are triggered by the activity of climbing fibres originating in neurons of the inferior olive. These complex spikes can shape the onset, amplitude and direction of movements and the adaptation of such movements to sensory feedback. Clusters of nearby inferior olive neurons project to parasagittally aligned stripes of Purkinje cells, referred to as 'microzones'. It is currently unclear to what extent individual Purkinje cells within a single microzone integrate climbing fibre inputs from multiple sources of different sensory origins, and to what extent sensory-evoked climbing fibre responses depend on the strength and recent history of activation. Here we imaged complex spike responses in cerebellar lobule crus 1 to various types of sensory stimulation in awake mice. We find that different sensory modalities and receptive fields have a mild, but consistent, tendency to converge on individual Purkinje cells, with climbing fibres showing some degree of input-specificity. Purkinje cells encoding the same stimulus show increased events with coherent complex spike firing and tend to lie close together. Moreover, whereas complex spike firing is only mildly affected by variations in stimulus strength, it depends strongly on the recent history of climbing fibre activity. Our data point towards a mechanism in the olivo-cerebellar system that regulates complex spike firing during mono- or multi-sensory stimulation around a relatively low set-point, highlighting an integrative coding scheme of complex spike firing under homeostatic control.

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