Feeding Stimulants Activate an Identified Dopaminergic Interneuron That Induces the Feeding Motor Program in<i>Helisoma</i>

Quinlan, Elizabeth; Arnett, Bridgette C.; Murphy, A. D.

doi:10.1152/jn.1997.78.2.812

Cited by 46 publications

(54 citation statements)

References 51 publications

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“…The studies for the dopamine neurotoxin (Kemenes et al 1990) and for the development of the dopamine-containing neurons (Voronezhskaya et al 1999) also support the contribution of dopamine to the generation of the feeding motor program. In fact, several dopaminergic neurons have been found in the buccal ganglia and reported to induce the feeding motor program (Kabotyanski et al 1998;Kemenes et al 1990;Quinlan et al 1997;Teyke et al 1993). In contrast, our present results strongly suggest that a pair of cerebral dopaminergic neurons contribute to the generation of the patterned movements for rejection.…”

Section: Discussioncontrasting

confidence: 56%

Cerebral CBm1 Neuron Contributes to Synaptic Modulation Appearing During Rejection of Seaweed inAplysia kurodai

Narusuye

Nagahama

2002

Journal of Neurophysiology

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Narusuye, Kenji, and Tatsumi Nagahama. Cerebral CBM1 neuron contributes to synaptic modulation appearing during rejection of seaweed in Aplysia kurodai. J Neurophysiol 88: 2778J Neurophysiol 88: -2795J Neurophysiol 88: , 2002 10.1152/jn.00757.2001. The Japanese species Aplysia kurodai feeds well on Ulva but rejects Gelidium with distinctive rhythmic patterned movements of the jaws and radula. We have previously shown that the patterned jaw movements during the rejection of Gelidium might be caused by long-lasting suppression of the monosynaptic transmission from the multiaction MA neurons to the jaw-closing (JC) motor neurons in the buccal ganglia and that the modulation might be directly produced by some cerebral neurons. In the present paper, we have identified a pair of catecholaminergic neurons (CBM1) in bilateral cerebral M clusters. The CBM1, probably equivalent to CBI-1 in A. californica, simultaneously produced monosynaptic excitatory postsynaptic potentials (EPSPs) in the MA and JC neurons. Firing of the CBM1 reduced the size of the inhibitory postsynaptic currents (IPSCs) in the JC neuron, evoked by the MA spikes, for Ͼ100 s. Moreover, the application of dopamine mimicked the CBM1 modulatory effects and pretreatment with a D1 antagonist, SCH23390, blocked the modulatory effects induced by dopamine. It could also largely block the modulatory effects induced by the CBM1 firing. These results suggest that the CBM1 may directly modulate the synaptic transmission by releasing dopamine. Moreover, we explored the CBM1 spike activity induced by taste stimulation of the animal lips with seaweed extracts by the use of calcium imaging. The calciumsensitive dye, Calcium Green-1, was iontophoretically loaded into a cell body of the CBM1 using a microelectrode. Application of either Ulva or Gelidium extract to the lips increased the fluorescence intensity, but the Gelidium extract always induced a larger change in fluorescence compared with the Ulva extract, although the solution used induced the maximum spike responses of the CBM1 for each of the seaweed extracts. When the firing frequency of the CBM1 activity after taste stimulation was estimated, the Gelidium extract induced a spike activity of ϳ30 spikes/s while the Ulva extract induced an activity of ϳ20 spikes/s, consistent with the effective firing frequency (Ͼ25 spikes/s) for the synaptic modulation. These results suggest that the CBM1 may be one of the cerebral neurons contributing to the modulation of the basic feeding circuits for rejection induced by the taste of seaweeds such as Gelidium.

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Section: Discussioncontrasting

confidence: 56%

Cerebral CBm1 Neuron Contributes to Synaptic Modulation Appearing During Rejection of Seaweed inAplysia kurodai

Narusuye

Nagahama

2002

Journal of Neurophysiology

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“…Compared with the literature base documenting the physiological actions of DA on feeding-related circuits Flamm and Harris-Warrick, 1986;Kabotyanski et al, 2000;Quinlan et al, 1997), and the behavioral ramifications of genetically altered DA synthesis (Neckameyer, 1996;Pendleton et al, 2002), surprisingly little is known about the physiological actions of DA on invertebrate locomotor networks (Barthe et al, 1989). In this present study on the leech, we have established that DA does indeed play a role in the control of locomotion, and that a dopaminergic neural network is coupled to the command-like cephalic projection neuron, Tr2.…”

Section: Discussionmentioning

confidence: 99%

A cephalic projection neuron involved in locomotion is dye coupled to the dopaminergic neural network in the medicinal leech

Crisp

Mesce

2004

Journal of Experimental Biology

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SUMMARY It is widely appreciated that the selection and modulation of locomotor circuits are dependent on the actions of higher-order projection neurons. In the leech, Hirudo medicinalis, locomotion is modulated by a number of cephalic projection neurons that descend from the subesophageal ganglion in the head. Specifically, descending brain interneuron Tr2 functions as a command-like neuron that can terminate or sometimes trigger fictive swimming. In this study, we demonstrate that Tr2 is dye coupled to the dopaminergic neural network distributed in the head brain. These findings represent the first anatomical evidence in support of dopamine (DA) playing a role in the modulation of locomotion in the leech. In addition, we have determined that bath application of DA to the brain and entire nerve cord reliably and rapidly terminates swimming in all preparations exhibiting fictive swimming. By contrast, DA application to nerve cords expressing ongoing fictive crawling does not inhibit this motor rhythm. Furthermore, we show that Tr2 receives rhythmic feedback from the crawl central pattern generator. For example, Tr2 receives inhibitory post-synaptic potentials during the elongation phase of each crawl cycle. When crawling is not expressed, spontaneous inhibitory post-synaptic potentials in Tr2 correlate in time with spontaneous excitatory post-synaptic potentials in the CV motor neuron, a circular muscle excitor that bursts during the elongation phase of crawling. Our data are consistent with the idea that DA biases the nervous system to produce locomotion in the form of crawling.

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“…However, these cells are not thought to be homologous to SO. 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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Feeding Stimulants Activate an Identified Dopaminergic Interneuron That Induces the Feeding Motor Program inHelisoma

Cited by 46 publications

References 51 publications

Cerebral CBm1 Neuron Contributes to Synaptic Modulation Appearing During Rejection of Seaweed inAplysia kurodai

Cerebral CBm1 Neuron Contributes to Synaptic Modulation Appearing During Rejection of Seaweed inAplysia kurodai

A cephalic projection neuron involved in locomotion is dye coupled to the dopaminergic neural network in the medicinal leech

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

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