Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry ofAplysia

Teyke, Thomas; Rosen, Steven C.; Weiss, Klaudiusz R.; Kupfermann, Irving

doi:10.1016/0006-8993(93)90661-6

Cited by 104 publications

(129 citation statements)

References 42 publications

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“…FCAP-containing neurons and processes could be observed in the buccal and cerebral ganglia and the gut. Furthermore, both MALDI and IMM detected FCAPs in the CBC, a nerve that contains axons of CBIs and BCIs, two classes of neurons that are implicated in initiation and modulation of feeding motor programs (Rosen et al, 1991;Teyke et al, 1993;Hurwitz et al, 1997Hurwitz et al, , 1999Xin et al, 1999;Sanchez and Kirk, 2000;Jing and Weiss, 2001). We showed that FCAPs are present in several CBIs and BCIs, although the identity of these CBIs and BCIs remains to be defined.…”

Section: Discussionmentioning

confidence: 60%

“…These neurons include the cerebral-buccal interneurons (CBIs) and buccal-cerebral interneurons (BCIs), which are known to be involved in generating and shaping the cerebral and buccal ganglion-mediated components of feeding motor programs (Rosen et al, 1991;Teyke et al, 1993;Hurwitz et al, 1997;Perrins and Weiss, 1998;Xin et al, 1999). Modulators that can alter feeding motor program output have been localized to some of the known CBIs and BCIs, and evidence suggests that additional, as yet unidentified neuropeptides are present in the feeding circuitry (Lloyd, 1989;Li et al, 1998).…”

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confidence: 99%

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Identification and Characterization of the Feeding Circuit-Activating Peptides, a Novel Neuropeptide Family ofAplysia

Sweedler

Rubakhin

et al. 2002

J. Neurosci.

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We use a multidisciplinary approach to identify, map, and characterize the bioactivity of modulatory neuropeptides in the circuitry that generates feeding behavior in Aplysia. Matrixassisted laser desorption/ionization time-of-flight mass spectrometry of the cerebral-buccal connective (CBC), a nerve containing axons of many interneurons that control feeding behavior of Aplysia, was used to identify neuropeptides that may participate in generation and shaping of feeding motor programs. Using this functionally oriented search, we identified a novel family of peptides that we call the feeding circuitactivating peptides (FCAPs). Two peptides with masses identical to those observed in the CBCs (molecular weight 1387 and 1433) were purified from buccal ganglia and partially sequenced using mass spectrometry. The amino acid sequence was then used to clone the FCAP precursor, which encodes multiple copies of eight different FCAPs. The two FCAPs present in highest copy number correspond to those observed in the CBC. The distribution of FCAP expression was mapped using Northern analysis, whole-mount in situ hybridization, and immunocytochemistry. Consistent with our initial findings, FCAP-immunopositive axons were observed in the CBC. Furthermore, we found that FCAP was present in some cerebralbuccal and buccal-cerebral interneurons. As their name suggests, FCAPs are capable of initiating rhythmic feeding motor programs and are the first neuropeptides with such activity in this circuit. The actions of FCAPs suggest that these peptides may contribute to the induction and maintenance of foodinduced arousal. FCAPs were also localized to several other neuronal systems, suggesting that FCAPs may play a role in the regulation of multiple behaviors.

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Section: Discussionmentioning

confidence: 60%

mentioning

confidence: 99%

Identification and Characterization of the Feeding Circuit-Activating Peptides, a Novel Neuropeptide Family ofAplysia

Sweedler

Rubakhin

et al. 2002

J. Neurosci.

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“…One such interneuron, B20, is critical for the expression of egestive motor programs because it provides strong excitatory input to B8 during the protraction phase (17,23). We found that the evolution of the network toward the egestive steady state elicited by EN stimulation was accompanied by enhancement of the amplitude of B20 to B8 postsynaptic potentials (PSPs) (Fig.…”

Section: Resultsmentioning

confidence: 94%

Dynamical basis of intentions and expectations in a simple neuronal network

Proekt

Březina

Weiss

2004

Proc. Natl. Acad. Sci. U.S.A.

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166

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Selection of behavioral responses to external stimuli is strongly influenced by internal states, such as intentions and expectations. These internal states are often attributed to higher-order brain functions. Yet here we show that even in the simple feeding network of Aplysia, external stimuli do not directly specify which motor output is expressed; instead, the motor output is specified by the state of the network at the moment of stimulation. The history-dependence of this network state manifests itself in the same way as do intentions and expectations in the behavior of higher animals. Remarkably, we find that activity-dependent plasticity of a synapse within the network itself, rather than some higher-order network, mediates one important aspect of the change in the network state. Through this mechanism, changes in the network state become an automatic consequence of the generation of behavior. Altogether, our findings suggest that intentions and expectations may emerge within behavior-generating networks themselves from the plasticity of the very processes that generate the behavior.A nimal behavior is not merely a passive response to external stimuli; rather, it expresses also the internal state of the animal. This internal state is presumably somehow embodied in the state of the nervous system. Here we study the manifestations and the neurophysiological basis of the internal state in the experimentally advantageous feeding network of the mollusk Aplysia.State-dependence of network function is not a new concept. In the neurophysiological literature, state-dependence is typically discussed as the ability of contextual cues to modify the response to a stimulus. This type of state-dependence has been demonstrated, for example, for locomotion by using stimulation of the mesencephalic locomotor region to elicit walking in the decerebrate cat. The speed of locomotion is determined by the speed of the treadmill on which the cat is placed (1). In another compelling example, stimulation of a command-like neuron in a leech immersed in water elicits swimming, whereas stimulation of the same neuron when the leech is placed on solid substrate elicits crawling (2). Similarly, stimulation of a command-like neuron in a cricket suspended in air elicits avoidance responses but it fails to do so when the cricket is placed on the ground (3). State-dependence of this type is also seen with neuromodulation. For instance, the ability of sensory stimulation to elicit stridulation in the grasshopper is critically dependent on the presence of a muscarinic agonist (4). The setting of network state by application of neuromodulators is a common phenomenon that has been well characterized in simple neuronal networks, such as the stomatogastric system of crustaceans (5-9).This type of state-dependence fails, however, to account for a fundamental feature of the state-dependence that is observed in animal behavior and human psychology. In the type of statedependence just discussed, the behavior is still unambiguously specified by the ext...

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“…Like the SO in Lymnaea, a variety of buccal neurons are capable of driving rhythmic fictive feeding in Aplysia (Susswein and Byrne, 1988;Kirk, 1989;Teyke et al, 1993;Hurwitz and Susswein, 1996;Kabotyanski et al, 1998), Helisoma (Quinlan et Figure 7. Alternative schemes for the organization of neurons for higher-order control of the Lymnaea feeding CPG.…”

Section: Comparisons With Other Systemsmentioning

confidence: 99%

“…Two of these cell types, the B1 cells of Achatina (Yoshida and Kobayashi, 1992) and the N1a cells of Helisoma (Quinlan et al, 1997), were tested for chemosensory responses, and it was shown that activity in these neurons was not necessary for fictive feeding to occur. N1M-type buccal CPG interneurons also have been found in other molluscan feeding systems (Aplysia, Susswein and Byrne, 1988;Teyke et al, 1993;Clione, Arshavsky et al, 1989;Planorbis, Arshavsky et al, 1988a,b), but their role in the sensory activation of feeding has not yet been investigated.…”

Section: Comparisons With Other Systemsmentioning

confidence: 99%

Multiple Types of Control by Identified Interneurons in a Sensory-Activated Rhythmic Motor Pattern

2001

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Modulatory interneurons that can drive central pattern generators (CPGs) are considered as good candidates for decisionmaking roles in rhythmic behaviors. Although the mechanisms by which such neurons activate their target CPGs are known in detail in many systems, their role in the sensory activation of CPG-driven behaviors is poorly understood. In the feeding system of the mollusc Lymnaea, one of the best-studied rhythmical networks, intracellular stimulation of either of two types of neuron, the cerebral ventral 1a (CV1a) and the slow oscillator (SO) cells, leads to robust CPG-driven fictive feeding patterns, suggesting that they might make an important contribution to natural food-activated behavior. In this paper we investigated this contribution using a lip-CNS preparation in which feeding was elicited with a natural chemostimulant rather than intracellular stimulation. We found that despite their CPG-driving capabilities, neither CV1a nor SO were involved in the initial activation of sucrose-evoked fictive feeding, whereas a CPG interneuron, N1M, was active first in almost all preparations. Instead, the two interneurons play important and distinct roles in determining the characteristics of the rhythmic motor output; CV1a by modulating motoneuron burst duration and SO by setting the frequency of the ongoing rhythm. This is an example of a distributed system in which (1) interneurons that drive similar motor patterns when activated artificially contribute differently to the shaping of the motor output when it is evoked by the relevant sensory input, and (2) a CPG rather than a modulatory interneuron type plays the most critical role in initiation of sensory-evoked rhythmic activity.

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Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry ofAplysia

Cited by 104 publications

References 42 publications

Identification and Characterization of the Feeding Circuit-Activating Peptides, a Novel Neuropeptide Family ofAplysia

Identification and Characterization of the Feeding Circuit-Activating Peptides, a Novel Neuropeptide Family ofAplysia

Dynamical basis of intentions and expectations in a simple neuronal network

Multiple Types of Control by Identified Interneurons in a Sensory-Activated Rhythmic Motor Pattern

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