Neocortical Networks Entrain Neuronal Circuits in Cerebellar Cortex

Journal of Neuroscience (2009)

Hana Roš Robert N. S. Sachdev Yuguo Yu Nenad Šestan David A. McCormick

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Abstract:

Activity in neocortex is often characterized by synchronized oscillations of neurons and networks, resulting in the generation of a local field potential (LFP) and electroencephalogram. Do the neuronal networks of the cerebellum also generate synchronized oscillations and are they under the influence of those in the neocortex? Here we show that, in the absence of any overt external stimulus, the cerebellar cortex generates a slow oscillation that is correlated with that of the neocortex. Disruption of the neocortical slow oscillation abolishes the cerebellar slow oscillation, whereas blocking cerebellar activity has no overt effect on the neocortex. We provide evidence that the cerebellar slow oscillation results in part from the activation of granule, Golgi, and Purkinje neurons. In particular, we show that granule and Golgi cells discharge trains of single spikes, and Purkinje cells generate complex spikes, during the "up" state of the slow oscillation. Purkinje cell simple spiking is weakly related to the cerebellar and neocortical slow oscillation in a minority of cells. Our results indicate that the cerebellum generates rhythmic network activity that can be recorded as an LFP in the anesthetized animal, which is driven by synchronized oscillations of the neocortex. Furthermore, we show that correlations between neocortical and cerebellar LFPs persist in the awake animal, indicating that neocortical circuits modulate cerebellar neurons in a similar manner in natural behavioral states. Thus, the projection neurons of the neocortex collectively exert a driving and modulatory influence on cerebellar network activity.

Keywords:

Neocortex

Deep cerebellar nuclei

Stimulus (psychology)

Premovement neuronal activity

Oscillation (cell signaling)

Topics:

Vestibular and auditory disorders

Neural dynamics and brain function

Neuroscience and Neuropharmacology Research

10.1523/jneurosci.2327-09.2009

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Cerebellar output regulation by the climbing and mossy fibers with and without the inferior olive

The Journal of Comparative Neurology (1983)

Jérémie Bardin C. Batini J.‐M. Billard C. Buisseret‐Delmas M. Conrath-Verrier

Abstract The activity of the olivocerebellar complex and the structures related in series with it have been studied using the complementary action of harmaline and 3‐acetylpyridine to isolate the two principal inputs to the cerebellar Purkinje cells. The activities of the various nuclei as well as the entire brain have been simultaneously monitored using the [ 14 C]2‐deoxyglucose method under the various combined effects of the pharmacological agents. (1) Tremogenic doses of harmaline increased the frequency of discharge in selected parts of the olivocerebellar system, increasing climbing fiber input and reducing Purkinje cell simple spike discharges in corresponding parts of the cerebellar cortex. The metabolic activity increased in the inferior olive and in the red nucleus. The results are interpreted as a net reduction of Purkinje cell inhibition on their target neurons, leading to a facilitatory cerebellar output. (2) Systemic injection of neurotoxic doses of 3‐acetylpyridine selectively produced total degeneration of the neurons in the inferior olive, resulting in the suppression of complex spikes and a net increase in simple spike output from the Purkinje cells. The metabolic consequences were a reduction or absence in the inferior olive, decrease in the red nucleus, and increases in the Purkinje cell target neuron regions, including the intracerebellar and vestibular nuclei. The study of long survival times following the neu‐ rotoxic treatment revealed a transient metabolic marking of the inferior olive during the active glial processes accompanying the degeneration. In other parts the radioautographic changes caused by the destruction of the inferior olive persisted for about 1 month after the administration of the drug. (3) Tremogenic doses of harmaline were given to rats at different times following treatment with 3‐acetylpyridine. It was demonstrated that: (a)intoxication of the inferior olive started within the second hour after 3‐acetylpyridine administration, corresponding to the time at which the metabolic response to harmaline was also abolished; and (b) the increased metabolic activity produced by harmaline in the olivocerebellar complex was a consequence of an increased activity of the neurons of the inferior olive rather than a direct pharmacological effect of the drug. (4) Partial lesions of the inferior olive led to increased metabolic activity of those parts of the intracerebellar nuclei topographically related to the destroyed parts of the inferior olive. (5) In 3‐acetylpyridine‐treated animals, local ablation as well as local inactivation of the cerebellar cortex produced localized suppression of the intense labeling in the intracerebellar nuclei obtained in these animals. Since these regions receive synapses which are normally inhibitory, suppression of labeling clearly supports the hypothesis that regional marking may very well be produced by the activity of the presynaptic terminals themselves. The increased marking following suppression of the olivocerebellar system was thus interpreted as due to an increased activity in the simple spikes, producing an increased inhibitory influence of the Purkinje cell and therefore a disfacilitatory cerebellar output.

Climbing fiber

Inferior olivary nucleus

Harmaline

Deep cerebellar nuclei

10.1002/cne.902130409

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Citations (44)

Immunohistochemical localisation of mGluR7 protein in the rodent and human cerebellar cortex using subtype specific antibodies

Molecular Brain Research (1998)

Timothy Phillips Andrew Makoff Elaine Murrison Michael L. Mimmack Henry J. Waldvogel

Immunostaining

Deep cerebellar nuclei