Species‐specific modulation of pattern‐generating circuits

Abstract

Phylogenetic comparison can reveal general principles governing the organization and neuromodulation of neural networks. Suitable models for such an approach are the pyloric and gastric motor networks of the crustacean stomatogastric ganglion (STG). These networks, which have been well studied in several species, are extensively modulated by projection neurons originating in higher-order ganglia. Several of these have been identified in different decapod species, including the paired modulatory proctolin neuron (MPN) in the crab Cancer borealis [Nusbaum & Marder (1989) J. Neurosci., 9,1501-1599; Nusbaum & Marder (1989), J. Neurosci., 9, 1600-1607] and the apparently equivalent neuron pair, called GABA (gamma-aminobutyric acid) neurons 1 and 2 (GN1/2), in the lobster Homarus gammarus [Cournil et al. (1990) J. Neurocytol., 19, 478-493]. The morphologies of MPN and GN1/2 are similar, and both exhibit GABA-immunolabelling. However, unlike MPN, GN1/2 does not contain the peptide transmitter proctolin. Instead, GN1/2, but not MPN, is immunoreactive for the neuropeptides related to cholecystokinin (CCK) and FLRFamide. Nonetheless, GN1/2 excitation of the lobster pyloric rhythm is similar to the proctolin-mediated excitation of the crab pyloric rhythm by MPN. In contrast, GN1/2 and MPN both use GABA but produce opposite effects on the gastric mill rhythm. While MPN stimulation produces a GABA-mediated suppression of the gastric rhythm [Blitz & Nusbaum (1999) J. Neurosci., 19, 6774-6783], GN1/2 activates or enhances gastric rhythmicity. These results highlight the care needed when generalizing neuronal organization and function across related species. Here we show that the 'same' neuron in different species does not contain the same neurotransmitter complement, nor does it exert all of the same effects on its postsynaptic targets. Conversely, a different transmitter phenotype is not necessarily associated with a qualitative change in the way that a modulatory neuron influences target network activity.

Evolution of central pattern generators and rhythmic behaviours

“…Therefore, changes in neuromodulation, either through differences in receptor expression or neurotransmitter content, could cause species differences in the output of neural circuits [39]. Homologous neurons that provide neuromodulatory input to CPG circuits in the stomatogastric nervous system of decapod crustaceans differ in the presence of neuropeptides resulting in species-specific changes to the motor pattern [40]. The same is true for serotonin: in the crab, Cancer borealis and the lobster, Homarus americanus, serotonin is released from a set of mechanosensory neurons called GPR cells [41][42][43].…”

Ontogeny of Modulatory Inputs to Motor Networks: Early Established Projection and Progressive Neurotransmitter Acquisition

“…In this model, two neuronal networks, located in the stomatogastric ganglion (STG), generate two motor outputs controlled by identified central and peripheral modulatory neurons Meyrand et al, 1991Meyrand et al, , 1994Meyrand et al, , 2000Nagy et al, 1994;Combes et al, 1999). Moreover, central projection neurons play a key role in the ontogeny of STNS networks because their presence masks preexisting adultlike phenotypes (Le Feuvre et al, 1999).…”

“…In H. gammarus many of these projection neurons have been identified, and the central input neurons have been studied extensively (Meyrand et al, , 1994(Meyrand et al, , 2000Nagy et al, 1994;Combes et al, 1999). Many of the projection neurons are well characterized in terms of electrical activity, neurotransmitter phenotype, soma location (CoG, OG, ivn, and lvn), morphology, and projection pattern (Table 1).…”

“…We have shown previously that among the earliest detectable modulatory substances in the embryo [FLRFamide, proctolin, and Red Pigment concentrating hormone (RPCH)], only FLRFamide is commonly expressed in the adult by identified neurons such as GPR cells , GN1/2 neurons (Meyrand et al, 2000), and PS neurons (Fenelon et al, 1998a). In contrast, although RPCH and proctolin immunoreactivity have been detected in the STG, so far the detection of these substances has not been coupled to electrophysiological identification of known projection neurons.…”

“…Therefore we focused our attention on the three groups of projection neurons (GPR, GN1/2, PS) that have been shown to express FLRFamide immunoreactivity. Moreover, these neurons also express cotransmitters in the adult, such as serotonin for the GPR cells and GABA for GN1/2 neurons (Cournil et al, 1990;Meyrand et al, 2000), and in other species PS neuron homologs display histamine immunoreactivity (Mulloney and Hall, 1991). Previous indirect studies suggest that, for example, the GPR neurons gradually acquire their neurotransmitter (FLRFamide, allatostatin, and serotonin) phenotype during development .…”