Regulation of Spike Initiation and Propagation in anAplysiaSensory Neuron: Gating-In via Central Depolarization

Abstract

Afferent transmission can be regulated (or gated) so that responses to peripheral stimuli are adjusted to make them appropriate for the ongoing phase of a motor program. Here, we characterize a gating mechanism that involves regulation of spike propagation in Aplysia mechanoafferent B21. B21 is striking in that afferent transmission to the motor neuron B8 does not occur when B21 is at resting membrane potential. Our data suggest that this results from the fact that spikes are not actively propagated to the lateral process of B21 (the primary contact with B8). When B21 is peripherally activated at its resting potential, electrotonic potentials in the lateral process are on average 11 mV. In contrast, mechanoafferent activity is transmitted to B8 when B21 is centrally depolarized via current injection. Our data suggest that central depolarization relieves propagation failure. Full-size spikes are recorded in the lateral process when B21 is depolarized and then peripherally activated. Moreover, changes in membrane potential in the lateral process affect spike amplitude, even when the somatic membrane potential is virtually unchanged. During motor programs, both the lateral process and the soma of B21 are phasically depolarized via synaptic input. These depolarizations are sufficient to convert subthreshold potentials to full-size spikes in the lateral process. Thus, our data strongly suggest that afferent transmission from B21 to B8 is, at least in part, regulated via synaptic control of spike initiation in the lateral process. Consequences of this control for compartmentalization in B21 are discussed, as are specific consequences for feeding behavior.

Mechanosensory Gating of Proprioceptor Input to Modulatory Projection Neurons

“…For example, there might have been a suppression of GPR spike propagation through the STG, so that the GPR spikes could not reach the CoGs. Focal regulation of sensory spike propagation within central ganglia is well documented in the molluscan nervous system (Evans et al, 2003;Frost et al, 2003) and also appears to occur in the cat spinal cord (Lomeli et al, 1998;Rudomin et al, 2004). However, our results indicate that the VCN gating of GPR actions in the CoGs Figure 7.…”

“…Previous studies of such gating focused on mechanisms involving the inhibition or enhancement of afferent input directly onto CPG elements or motor neurons, often involving a phasic regulation of the incoming sensory information (El Manira et al, 1997a;Nusbaum et al, 1997;Buschges and El Manira, 1998;DiCaprio, 1999;Evans et al, 2003;Frost et al, 2003;Rossignol et al, 2006). Because the GPR excitation of the projection neurons was gated out when the gastric mill rhythm had recently been activated by a distinct sensory pathway, this gating event ensured that the elicited motor pattern was not altered by changing the firing rate and/or pattern of the activated projection neurons.…”

Motor neuronal activity varies least among individuals when it matters most for behavior

“…First, by using a reduced preparation in which all but proprioceptive input from the feeding apparatus has been removed (McManus et al 2012), or by using a preparation in which the entire musculature has been disconnected (the isolated buccal ganglion), it may be possible to characterize the effects of removing much or all of the sensory input on motor neuronal variability. Second, because many of the key sensory neurons that provide chemoafferent or mechanoafferent inputs to the feeding apparatus have been characterized (Evans et al 2003;Evans and Cropper 1998;Rosen et al 2000aRosen et al , 2000b, working out the cellular mechanism by which sensory feedback can shape motor neuronal activity can focus on both identified sensory and motor neurons. Finally, the studies by Nargeot and his colleagues have elegantly demonstrated that it is possible to work out, at the level of individual identified neurons, the mechanisms by which variability can be reduced in the feeding neural circuitry (Sieling et al 2014), suggesting that similar studies can be done to understand how variability is regulated by sensory feedback.…”

Memory-Like Alterations inAplysiaAxons after Nerve Injury or Localized Depolarization

“…Previous reports focused on decreases rather than increases in excitability, produced by either high-frequency activation of an axon (Debanne, 2004) or axon injury (Titmus and Faber, 1990). Although enhancement of action potential conduction (or reflection) at branch points or in neuronal processes prone to conduction failure has been described, reported examples of enhancement barely outlast the duration of axonal firing or neuromodulatory input responsible for the enhancement (Mar and Drapeau, 1996;Baccus et al, 2000;Evans et al, 2003). A long-term, localized decrease in spike threshold triggered by depolarization during axon injury should counteract the increased probability of conduction failure that occurs in an injured region, e.g., by impedance mismatch when spikes invade normal segments after propagating through axon segments narrowed by injury (Titmus and Faber, 1990) or through thin regenerating neurites (Steffensen et al, 1995).…”