Responses to Tactile Stimulation in Deep Cerebellar Nucleus Neurons Result From Recurrent Activation in Multiple Pathways

Abstract

Rowland NC, Jaeger D. Responses to tactile stimulation in deep cerebellar nucleus neurons result from recurrent activation in multiple pathways. J Neurophysiol 99: 704 -717, 2008. First published December 12, 2007; doi:10.1152/jn.01100.2007. In a previous study, we found that neurons in the deep cerebellar nuclei (DCN) respond to 5-ms brief facial tactile stimulation in rats anesthetized with ketaminexylazine with multiphasic response patterns lasting over 200 ms. It remained unclear, however, to what extent these responses were shaped not only by ascending sensory input from the trigeminal nuclei but also by interactions with other major cerebellar afferent systems, in particular the inferior olive (IO) and cerebral cortex. In the present study, we recorded from the IO, cerebral cortex, cerebellar granule cell layer (GCL), and DCN during the presentation of 5-ms facial tactile stimuli to elucidate potential mechanisms of how extended DCN response patterns are generated. We found that tactile stimulation resulted in robust multiphasic local field potentials responses in the IO as well as in the activation of a wide region of the somatosensory cortex (SI) and the primary motor cortex (MI). DCN neurons responded to electrical stimulation of any of these structures (IO, SI, and MI) with complex temporal patterns strikingly similar to air-puff lip stimulation responses. Simultaneous recordings from multiple structures revealed that long-lasting activation patterns elicited in DCN neurons were based on recurrent network activation in particular between the IO and the DCN with a potential contribution of DCN rebound properties. These results are consistent with the hypothesis that sensory stimulation triggers a feedback network activation of cerebellum, IO, and cerebral cortex to generate temporal patterns of activity that may control the timing of behavior. I N T R O D U C T I O NIn the rat, sensory information from the face is conveyed from the trigeminal nuclear complex to the cerebellum through three principal pathways: direct trigeminocerebellar fibers, the inferior olive, and the somatosensory cortex via the basilar pontine nuclei (Waite and Tracey 1995). In a previous study, we demonstrated that stimulation of the orofacial region in anesthetized rats not only activates the cerebellar cortex (Bower and Woolston 1983;Shambes et al. 1978) but also produces reliable strong responses in the deep cerebellar nuclei (DCN) (Rowland and Jaeger 2005). Single units in the DCN responded to 5-ms air-puff stimulation of the lips with multiphasic and extended temporal activity patterns that were mostly invariant to stimulus parameters. These sensory-evoked responses could be described as a combination of three temporal components: a brief excitation comprising one or a few spikes with a mean latency of 10 Ϯ 0.9 (SD) ms, a strong inhibition at a mean latency of 18 Ϯ 1.25 ms, and a second prolonged excitation with a mean latency of 291 Ϯ 13.3 ms. Different combinations and different amplitudes of these response components were ...

Mechanisms Supporting Transfer of Inhibitory Signals into the Spike Output of Spontaneously Firing Cerebellar Nuclear Neurons In Vitro

“…Our results showing synaptic evoked rebounds in spontaneously firing DCNs are consistent with previous data obtained from more hyperpolarized levels [2][3][4][5], as well as from in vivo recordings [20], and support the idea that rebound excitation is used to transfer inhibitory signals to The stimulus intensity (in microamperes) is indicated for each trace. B Plots of average and maximal frequency, estimated over 1 s after the occurrence of the first spike after the IPSP, versus stimulus strength for the same neuron.…”

Differential olivo-cerebellar cortical control of rebound activity in the cerebellar nuclei

“…Whole-cell recordings in vivo showed that, whereas the increased firing frequency is accompanied by true rebound depolarizations, the timed-spiking activity occurs predominantly before these depolarizations. Despite the effectiveness of the train stimuli applied to the cerebellar cortex, we found the strongest increases in firing frequency when we directly stimulated the IO (41,49,53). Moreover, we found spontaneous rebound firing in CN neurons following hyperpolarizations that have temporal characteristics that are compatible with those of complex spike activities.…”

Reliability of triggering postinhibitory rebound bursts in deep cerebellar neurons

“…1,4,5,[8][9][10]12,13 Some evidence exists for the generation of rebound-like bursts in vivo following periods of reduced firing of DCN cells (including presumed Purkinje cellevoked inhibition) or rebound responses in motor control. [17][18][19][20][21] Yet the potential for intrinsic membrane properties of the type assessed in vitro to generate rebound bursts in response to Purkinje cell inhibitory input has not been extensively studied.…”