Rhythmic activity of feline dorsal and ventral spinocerebellar tract neurons during fictive motor actions

Abstract

Neurons of the dorsal spinocerebellar tracts (DSCT) have been described to be rhythmically active during walking on a treadmill in decerebrate cats, but this activity ceased following deafferentation of the hindlimb. This observation supported the hypothesis that DSCT neurons primarily relay the activity of hindlimb afferents during locomotion, but lack input from the spinal central pattern generator. The ventral spinocerebellar tract (VSCT) neurons, on the other hand, were found to be active during actual locomotion (on a treadmill) even after deafferentation, as well as during fictive locomotion (without phasic afferent feedback). In this study, we compared the activity of DSCT and VSCT neurons during fictive rhythmic motor behaviors. We used decerebrate cat preparations in which fictive motor tasks can be evoked while the animal is paralyzed and there is no rhythmic sensory input from hindlimb nerves. Spinocerebellar tract cells with cell bodies located in the lumbar segments were identified by electrophysiological techniques and examined by extra-and intracellular microelectrode recordings. During fictive locomotion, 57/81 DSCT and 30/30 VSCT neurons showed phasic, cycle-related activity. During fictive scratch, 19/29 DSCT neurons showed activity related to the scratch cycle. We provide evidence for the first time that locomotor and scratch drive potentials are present not only in VSCT, but also in the majority of DSCT neurons. These results demonstrate that both spinocerebellar tracts receive input from the central pattern generator circuitry, often sufficient to elicit firing in the absence of sensory input.

Simulating Spinal Border Cells and Cerebellar Granule Cells under Locomotion – A Case Study of Spinocerebellar Information Processing

“…It follows, similar to the magnitude of synaptic weights in other synaptic junctions of the cat spinal cord [40], that the responses of the individual synaptic connections are likely to amount to only a few µVs in amplitude in SBCs. On the other hand, since the SBCs receive so many RST synapses and inhibitory synapses from interneurons activated by Ib afferents, concerted activation of these inputs will be translated to relatively massive excitatory and inhibitory modulations of the intracellular potential (shown for VSCT neurons under fictive locomotion [9]), which are much slower than the responses obtained by synchronous fiber activation obtained on tract stimulation and nerve shock stimulation [7], [8]. The amplitude of these intracellular membrane potential changes should be related to the average firing rate of the neurons that converge onto the individual SBC.…”

“…The spike response of the SBC model to an input intracellular signal recorded during one step cycle (adapted from [9]). The gray area indicates the 95% confidence bounds of the model response and the solid line the average measured instantaneous firing frequency from 12 cycles [9].…”

“…The granule cells and spinal neurons were simulated using different models of spike generation for two reasons. Firstly, VSCT neurons, of which the SBCs are a subpopulation, work as straight-forward rate coders during fictive locomotion [9] whereas granule cells differ from these and other rate coding neurons by having a great gap between the resting potential and firing threshold [15] allowing them to have fast transient responses that cannot be captured by the escape rate model but can be described by the integrate-and-fire model. Secondly, whereas the data from VSCT/SBC neurons exist in the form of firing rate modulations to relatively slowly modulated intracellular depolarizations, suitable for escape rate models such as the one we use [28], the data available for granule cells responding to SBC tract stimulation, which generates artificially synchronized and very sharp population EPSPs, is more suitable to approximate with the integrate-and-fire model.…”

“…Briefly, the spike firing rate was described by a modulated log-normal hazard function that was fitted to respond with the same intensity as the VSCT neurons in [9], [10] when subjected to input that depolarizes the membrane potential in the range of 0 and 7 mV from the resting potential, similar to the maximal depolarization of 7.1 mV recorded in VSCT neurons under fictive locomotion [9].…”

“…SBCs receive a massive excitatory input from the reticulospinal tract (RST), representing a motor command, and powerful inhibition from Ib interneurons, representing a main sensory feedback to the SBCs [6]–[8]. Given the strong input from the RST, SBCs are likely to participate in the control of locomotion, similar to other cells of the VSCT [9], [10]. SBCs as a group also features input from group II and possibly group Ia afferents.…”