Tigran P. Norekian

The ctenophore genome and the evolutionary origins of neural systems

The origins of neural systems remain unresolved. In contrast to other basal metazoans, ctenophores (comb jellies) have both complex nervous and mesoderm-derived muscular systems. These holoplanktonic predators also have sophisticated ciliated locomotion, behaviour and distinct development. Here we present the draft genome of Pleurobrachia bachei, Pacific sea gooseberry, together with ten other ctenophore transcriptomes, and show that they are remarkably distinct from other animal genomes in their content of neurogenic, immune and developmental genes. Our integrative analyses place Ctenophora as the earliest lineage within Metazoa. This hypothesis is supported by comparative analysis of multiple gene families, including the apparent absence of HOX genes, canonical microRNA machinery, and reduced immune complement in ctenophores. Although two distinct nervous systems are well recognized in ctenophores, many bilaterian neuron-specific genes and genes of ‘classical’ neurotransmitter pathways either are absent or, if present, are not expressed in neurons. Our metabolomic and physiological data are consistent with the hypothesis that ctenophore neural systems, and possibly muscle specification, evolved independently from those in other animals.

Modulation of swimming speed in the pteropod mollusc, Clione limacina: role of a compartmental serotonergic system.

In locomotory systems, the central pattern generator and motoneuron output must be modulated in order to achieve variability in locomotory speed, particularly when speed changes are important components of different behavior acts. The swimming system of the pteropod molluscClione limacina is an excellent model system for investigating such modulation. In particular, a system of central serotonergic neurons has been shown to be intimately involved in regulating output of the locomotory pattern generator and motor system ofClione. There are approximately 27 pairs of serotonin-immunoreactive neurons in the central nervous system ofClione, with about 75% of these identified. The majority of these identified immunoreactive neurons are involved in various aspects of locomotory speed modulation. A symmetrical cluster of pedal serotonergic neurons serves to increase wing contractility without affecting wing-beat frequency or motoneuron activity. Two clusters of cerebral cells produce widespread responses that lead to an increase in pattern generator cycle frequency, recruitment of swim motoneurons, activation of the pedal serotonergic neurons and excitation of the heart excitor neuron. A pair of ventral cerebral neurons provides weak excitatory inputs to the swimming system, and strongly inhibits neurons of the competing whole-body withdrawal network. Overall, the serotonergic system inClione is compartmentalized so that each subsystem (usually neuron cluster) can act independently or in concert to produce variability in locomotory speed.

FMRFamide and GABA Produce Functionally Opposite Effects on Prey-Capture Reactions in the Pteropod Mollusk Clione limacina

The effects of FMRFamide and gamma-aminobutyric acid (GABA) on prey-capture reactions in Clione and on cerebral A and B neurons, which control opposite movements of prey capture appendages, have been studied. FMRFamide hyperpolarized A neurons and depolarized and increased spike activity in B neurons. FMRFamide thus had a reciprocal effect on A and B neurons, triggering buccal cone withdrawal. In addition, FMRFamide inhibited swimming, acceleration of which is a component of feeding arousal. Many neurons throughout the central nervous system showed FMRFamide immunoreactivity. Dense networks of immunoreactive fibers were localized in the head wall, buccal mass and in buccal cones, adjacent to striated longitudinal muscle cells. In wings, immunoreactive processes were found mainly in association with smooth retractor muscles. GABA depolarized and activated A neurons but hyperpolarized and inhibited B neurons. The overall effect of GABA thus resulted in extrusion of buccal cones. Both direct GABA responses and inhibitory postsynaptic potentials (IPSPs) induced in B neurons by A neuron activity were chloride-mediated. However, picrotoxin and bicuculline did not block IPSPs or direct GABA responses in B cells.

An identified cerebral interneuron initiates different elements of prey capture behavior in the pteropod mollusc,Clione limacina

The prey capture phase of feeding behavior in the pteropod molluscClione limacina consists of an explosive extrusion of buccal cones, specialized oral appendages which are used to catch the prey, and significant acceleration of swimming. Several groups of neurons which control different components of prey capture behavior inClione have been previously identified in the CNS. However, the question of their coordination in order to develop a normal behavioral reaction still remains open. We describe here a cerebral interneuron which has wide-spread excitatory and inhibitory effects on a number of neurons in the cerebral and pedal ganglia, directed toward the initiation of prey capture behavior inClione. This bilaterally symmetrical neuron, designated Cr-PC (Cerebral interneuron initiating Prey Capture), produced monosynaptic activation of Cr-A motoneurons, which control buccal cone extrusion, and inhibition of Cr-B and Cr-L motoneurons, whose spike activities maintain buccal cones in a withdrawn position inside the head in non-feeding animals. In addition, Cr-PC produced monosynaptic activation of a number of swim motoneurons and interneurons of the swim central pattern generator (CPG) in the pedal ganglia, pedal serotonergic Pd-SW neurons involved in a peripheral modulation of swimming and the serotonergic Heart Excitor neuron.

Co-Activation of Antagonistic Motoneurons as a Mechanism of High-Speed Hydraulic Inflation of Prey Capture Appendages in the Pteropod Mollusk Clione limacina

The predatory pteropod mollusk Clione limacina catches its prey by using specialized oral appendages called buccal cones. Eversion and elongation of buccal cones is a hydraulic phenomenon. In the cerebral ganglia, two groups of motoneurons have been identified that underlie functionally opposite movements of buccal cones: extrusion and retraction. We suggest that the remarkably rapid inflation of buccal cones (50 ms) is achieved through initial co-activation of antagonistic neurons, which presumably produces high pressure in the head hemocoel prior to buccal cone extrusion. The subsequent sudden inhibition of retractor motoneuron activity results in a very rapid and powerful inflation of the buccal cones. Cerebral interneurons that evoke co-activation are described.