The brain matters: effects of descending signals on motor control

Abstract

The ability of nerve cords and spinal cords to exhibit fictive rhythmic locomotion in the absence of the brain is well-documented in numerous species. Although the brain is important for modulating the fictive motor output, it is broadly assumed that the functional properties of neuronal circuits identified in simplified preparations are conserved with the brain attached. We tested this assumption by examining the properties of a novel interneuron recently identified in the leech (Hirudo verbana) nerve cord. This neuron, cell E21, initiates and drives stereotyped fictive swimming activity in preparations of the isolated leech nerve cord deprived of the head brain. We report that, contrary to expectation, the motor output generated when cell E21 is stimulated in preparations with the brain attached is highly variable. Swim frequency and episode duration are increased in some of these preparations and decreased in others. Cell E21 controls swimming, in part, via excitatory synaptic interactions with cells 204, previously identified gating neurons that reliably initiate and strongly enhance leech swimming activity when the brain is absent. We found that in preparations with the brain present, the magnitude of the synaptic interaction from cell E21 to cell 204 is reduced by 50% and that cell 204-evoked responses also were highly variable. Intriguingly, most of this variability disappeared in semi-intact preparations. We conclude that neuronal circuit properties identified in reduced preparations might be fundamentally altered from those that occur in more physiological conditions.

Purinergic modulation of neuronal gap junction circuits in the CNS of the leech

“…The slow oscillatory bursting behavior observed here when ATP was applied to the isolated ganglion might arise from the passive inputs of a central pacemaker cell. For example, an oscillatory bursting pattern of similar period and duration, has been attributed to the central pattern generator for crawling in the leech (Mullins & Friesen, ; Puhl & Mesce, ). This phasic activity is characterized by alternating activation of ventral and dorsal motoneurons with a 5–25 s period, which underlies the two‐step elongation—contraction cycle responsible for crawling behavior (Puhl & Mesce, ).…”

Activity in descending dopaminergic neurons represents but is not required for leg movements in the fruit flyDrosophila

“…Despite the significant correlation between DA-DN spike rates and leg movement speed, we found that bidirectional manipulations of DA-DN activity had no effect on ongoing leg movements. Given the abundant evidence that the brain provides brakes on the output of body motor circuits that are absent in reduced preparations (M'Cracken 1907;McDaniel and Horsfall 1957;Brodfuehrer and Friesen 1986;Thompson 1986;Mullins and Friesen 2012), one interpretation of these data is that with all descending pathways intact, activation of DA-DNs is not sufficient to alter ongoing leg movements in the behavioral contexts we examined. A related possibility is that the effects of DA-DN inputs to downstream motor circuits must combine with changes in other neuromodula- tory inputs to generate a detectable effect on leg movements, although it remains unknown whether and how other neuromodulatory neurons are recruited during leg movements in flies.…”

An annotated CNS transcriptome of the medicinal leech, Hirudo verbana: De novo sequencing to characterize genes associated with nervous system activity

“…Molecular sequence information for the Northwestern European medicinal leech Hirudo medicinalis has more recently been accumulating through studies targeting specific candidate gene sequences [ 9 – 14 ], tissue types [ 15 , 16 ], or life stages [ 17 ]. The Southeastern European medicinal leech Hirudo verbana has not received the same attention in the surge to bring transcriptomic approaches to traditionally “non-genetic” systems, even though it remains the most commonly used species in neurophysiological and behavioral studies [ 18 – 21 ]. While H .…”