Command or obey? Homologous neurons differ in hierarchical position for the generation of homologous behaviors
Akira Sakurai and Paul S. Katz
J Neurosci 17 June 2019, 3229-18
DOI: https://doi.org/10.1523/JNEUROSCI.3229-18.2019
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Nudibranchs have homologous neurons that can be identified across species. Cross-species comparisons of motor system organization provide fundamental insights into their function and origin. This paper shows that an identified cerebral ganglion neuron serves as a command neuron for the swimming behavior in a nudibranch species. The same neuron serves as a member of a central pattern generator (CPG) in another species. We described the synaptic and neuromodulatory mechanisms by which the command neuron initiates and accelerates rhythmic motor patterns.
Two sea slug species show homologous swimming behaviors
In motor systems, higher-level components issue commands that are carried out by lower-level circuits. In this paper, we describe the physiological actions of an identified neuron, which turned out to be a "command" neuron for the swimming behavior of a giant sea slug, Dendronotus iris. We determined which functional components of the swim CPG are modulated by the command inputs to initiate, maintain, and terminate the rhythmic activity of a central pattern generator circuit.
Among the swimming nudibranchs, two species Melibe leonina and Dendronotus iris show the homologous swimming behavior by flexing their bodies from left to right (Sakurai et al., 2011).
Homologous behaviors are produced by homologous neurons
Phylogenetic analysis indicates that the most recent common ancestor of these species likely swam in this manner, making the swimming behaviors homologous (Goodheart et al., 2015; Sakurai and Katz, 2017).
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| The brains of Melibe leonina (left) and Dendronotus iris (right) |
Homologous behaviors are produced by distinct neural circuit designs
The neural circuits underlying their behaviors have been studied extensively in both species. All neurons in the swim CPGs have been identified, and their synaptic connections have been determined with careful pairwise electrophysiological recordings (Sakurai et al., 2014; Sakurai and Katz 2016). The two swim CPGs employ different network architectures for producing similar rhythmic motor patterns.
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| The swim CPGs of Melibe (left) and Dendronotus (right) have distinct synaptic organizations |
Si1 as a command neuron in Dendronotus
In this study we found that Si1 neurons in Dendronotus iris serves as a neuromodulatory "command" neuron for the swim CPG.
Synaptic and neuromodulatory actions underlie the command input
It turned out that the organization of the Dendronotus swim CPG closely resembles the model that was originally proposed for a half-center oscillator with excitatory drive arising from a command neuron (Friesen, 1994).
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| A classical model of the half-center oscillator (left) and the Dendronotus swim CPG (right) |
The command neuron Si1 provides not only the overall excitatory drive but also the neuromodulation of synaptic potentiation within each half of the oscillator. Our results also suggest that the functional position of neurons in a motor hierarchy can shift from one level (CPG) to another (a command neuron) over evolutionary time.
- Friesen WO (1994) Reciprocal inhibition: a mechanism underlying oscillatory animal movements. Neuroscience and biobehavioral reviews 18:547-553.
- Goodheart JA, Bazinet AL, Collins AG, Cummings MP (2015) Relationships within Cladobranchia (Gastropoda: Nudibranchia) based on RNA-Seq data: an initial investigation. R Soc Open Sci 2:150196.
- Sakurai A, Katz PS (2016) The central pattern generator underlying swimming in Dendronotus iris: a simple half-center network oscillator with a twist. J Neurophysiol 116:1728-1742.
- Sakurai A, Katz PS (2017) Artificial Synaptic Rewiring Demonstrates that Distinct Neural Circuit Configurations Underlie Homologous Behaviors. Curr Biol 27:1721-1734 e1723.
- Sakurai A, Newcomb JM, Lillvis JL, Katz PS (2011) Different roles for homologous interneurons in species exhibiting similar rhythmic behaviors. Curr Biol 21:1036-1043.
- Sakurai A, Gunaratne CA, Katz PS (2014) Two interconnected kernels of reciprocally inhibitory interneurons underlie alternating left-right swim motor pattern generation in the mollusc Melibe leonina. J Neurophysiol 112:1317-1328.
