Command or Obey? Homologous Neurons Differ in Hierarchical Position for the Generation of Homologous Behaviors

Abstract

In motor systems, higher-order neurons provide commands to lower-level central pattern generators (CPGs) that autonomously produce rhythmic motor patterns. Such hierarchical organization is often thought to be inherent in the anatomical position of the neurons. Here, however, we report that a neuron that is member of a CPG in one species acts as a higher-order neuron in another species. In the nudibranch mollusc, Melibe leonina, swim interneuron 1 (Si1) is in the CPG underlying swimming, firing rhythmic bursts of action potentials as part of the swim motor pattern. We found that its homolog in another nudibranch, Dendronotus iris, serves as a neuromodulatory command neuron for the CPG of a homologous swimming behavior. In Dendronotus, Si1 fired irregularly throughout the swim motor pattern. The burst and spike frequencies of Dendronotus swim CPG neurons correlated with Si1 firing frequency. Si1 activity was both necessary and sufficient for the initiation and maintenance of the swim motor pattern. Each Si1 was electrically coupled to all of the CPG neurons and made monosynaptic excitatory synapses with both Si3s. Si1 also bilaterally potentiated the excitatory synapse from Si3 to Si2. "Virtual neuromodulation" of both Si3-to-Si2 synapses using dynamic clamp combined with depolarization of both Si3s mimicked the effects of Si1 stimulation on the swim motor pattern. Thus, in Dendronotus, Si1 is a command neuron that turns on, maintains, and accelerates the motor pattern through synaptic and neuromodulatory actions, thereby differing from its homolog in Melibe in its functional position in the motor hierarchy.

Bursting emerges from the complementary roles of neurons in a four-cell network

“…It is currently unclear which ion permeability underlies the sag and the rebound discharge in Si3 neurons. In the previous study, we have shown that the central command neuron, Si1, makes synapses onto Si3 and potentiates the Si3 synaptic strength (Sakurai and Katz 2019). The modulatory effects of Si1 on the membrane excitability of Si3 are of interest and remain to be investigated in the future.…”

A tale of two leeches: Toward the understanding of the evolution and development of behavioral neural circuits

“…In any case, evidence suggests that the output of a neural circuit is remarkably evolutionarily stable. For example, in some of the simplest central pattern generator (CPG) circuits, such as the crustacean pyloric rhythm circuits and the gastropod swimming circuits, the output pattern is relatively consistent between individuals and between species, despite the observed variation in the circuit parameters, for example, synapse strength, wiring pattern, and cellular composition (Goaillard et al, 2009; Prinz et al, 2004; Sakurai & Katz, 2015, 2019; Sakurai et al, 2011). Nevertheless, comparisons between gastropod species showed that changes in the circuit parameters could at times produce changes in homologous CPG circuits (Newcomb et al, 2012; Sakurai & Katz, 2017), suggesting that the output of the circuit is not inherently immutable but is stabilized by compensatory changes in different components of the circuits.…”

Comprehensive analysis of behavioral dynamics in the protochordateCiona intestinalis

“…Researchers in the field have been able to employ the aforementioned modern technologies to define motor actions as a function of their natural stereotyped elements, known as behavioral 'modules', 'motifs', 'syllables', or 'primitives'(1, [6][7][8][9][10], where these basic building blocks of motor behavior operate under organizational and hierarchical rules that bear similarities to phonological and syntactical rules that govern language. Modern systems neuroscience approaches have greatly facilitated the investigation of vertebrate motor modules (11)(12)(13), which in invertebrates are even more likely to be interrogated with high sensitivity and precision, largely due to the latter's smaller nervous systems (14)(15)(16). In addition, the next generation of neuroscience discovery capitalizes on developing and studying new non-traditional model species to reveal not only common principles, but also differences in behavioral organization across the tree of life as well as within important clades (17,18).…”