Sensory function and gating of histaminergic neuron C2 in Aplysia

Weiss, K. R.; Chiel, Hillel J.; Kupfermann, Irving

doi:10.1523/jneurosci.06-08-02416.1986

Cited by 43 publications

(32 citation statements)

References 35 publications

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“…C2 is a primary mechanoafferent that responds both to active feeding movements and to touch of the perioral zone (Weiss et al 1986a). It is likely to respond vigorously not only to food in the mouth when animals eat physically complex foods, or to a cannula within the mouth, but also to attempts to pull inedible food into the mouth during training (Chiel et al 1986).…”

Section: No At Concentrations Causing Memory Affects MCC Firingmentioning

confidence: 99%

“…In addition, followers of C2 innervate muscles that are active during the retraction phase of swallows and contribute to swallowing (Chiel et al 1986). C2 releases two transmitters, NO and histamine, which together excite a well-studied follower, the giant metacerebral cell (MCC) (Jacket 1995; Weiss et al 1986a), as well as additional cerebral ganglion neurons (Chiel et al 1986;McCaman and Weinreich 1985). If C2 signals efforts to swallow, and its activity is necessary for learning that food is inedible, blocking its other transmitter, histamine, should also block memory after learning that food is inedible and exogenous histamine should also cause memory when paired with lip stimulation.…”

Section: Possible Roles Of Neurons C2 and The MCCmentioning

confidence: 99%

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Nitric Oxide Signals ThatAplysiaHave Attempted to Eat, a Necessary Component of Memory Formation After Learning That Food Is Inedible

Katzoff

Ben‐Gedalya²,

Hurwitz³

et al. 2006

Journal of Neurophysiology

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To gain insight into the function of NO transmission during learning we tested whether blocking NO synthesis affects aspects of feeding that are expressed both in a nonlearning context and during learning. Inhibiting NO synthesis with L-NAME and blocking guanylyl cyclase with methylene blue decreased the efficacy of ad libitum feeding. D-NAME had no effect. L-NAME also decreased rejection responses frequency, but did not affect rejection amplitude. The effect of L-NAME was explained by a decreased signaling that efforts to swallow are not successful, leading to a decreased rejection rate, and a decreased ability to reposition and subsequently consume food in ad libitum feeding. Signaling that animals have made an effort to swallow is a critical component of learning that food is inedible. Stimulation of the lips with food alone did not produce memory, but stimulation combined with the NO donor SNAP did produce memory. Exogenous NO at a concentration causing memory also excited a key neuron responding to NO, the MCC. Block of the cGMP secondmessenger cascade during training by methylene blue also blocked memory formation after learning. Our data indicate that memory arises from the contingency of three events during learning that food is inedible. One of the events is efforts to swallow, which are signaled by NO by cGMP.

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Section: No At Concentrations Causing Memory Affects MCC Firingmentioning

confidence: 99%

Section: Possible Roles Of Neurons C2 and The MCCmentioning

confidence: 99%

Nitric Oxide Signals ThatAplysiaHave Attempted to Eat, a Necessary Component of Memory Formation After Learning That Food Is Inedible

Katzoff

Ben‐Gedalya²,

Hurwitz³

et al. 2006

Journal of Neurophysiology

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“…Notably, precedents for such gating out exist in the feeding system of Aplysia (Weiss et al, 1986;Evans et al, 2003;Hurwitz et al, 2005) as well as in the crab (Bartos and Nusbaum, 1997). Thus, we tested the possibility that the output of B64 is functional in CBI-2-elicited ingestive programs but is gated out in ENelicited egestive programs.…”

Section: B64 Early Activation In Ingestive Versus Egestive Programsmentioning

confidence: 99%

State Dependence of Spike Timing and Neuronal Function in a Motor Pattern Generating Network

Due²,

Sasaki³

et al. 2007

J. Neurosci.

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When sustained firing of a neuron is similar in different types of motor programs, its role in the generation of these programs is often similar. We investigated whether this is also the case for neurons involved in phase transition. In the Aplysia feeding central pattern generator (CPG), identified interneuron B64 starts firing at the transition between the protraction and the retraction phases of all types of motor programs, and its firing is sustained during the retraction phase. It was thought that B64 functions as a protraction terminator as it provides strong inhibitory input to protraction interneurons and motoneurons. Furthermore, premature activation of B64 can lead to premature termination of the protraction phase. Indeed, as we show here, B64 can terminate the protraction phase regardless of the type of motor program. However, B64 actually only functions as a protraction terminator in ingestive-like but not in egestive-like programs. This differential role of B64 results from a differential timing of the initiation of B64 spiking in the two types of programs. In turn, this differential timing of the initiation of B64 firing is determined by the internal state of the CPG. Thus, this study indicates the importance of the timing of initiation of firing in determining the functional role of a neuron and demonstrates that this role depends on the activity-dependent state of the network.

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“…C2 is an unconventional sensory neuron (Weiss et al 1986a) responding to active feeding movements, particularly in response to tough foods. It is likely to respond to increases in the toughness of a food (Chiel et al 1986(Chiel et al , 1990.…”

Section: C2 and MCCmentioning

confidence: 99%

Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

Katzoff¹,

Miller²,

Susswein³

2009

Learn. Mem.

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Memory that food is inedible in Aplysia arises from training requiring three contingent events. Nitric oxide (NO) and histamine are released by a neuron responding to one of these events, attempts to swallow food. Since NO release during training is necessary for subsequent memory and NO substitutes for attempts to swallow, it was suggested that NO functions during training as a signal of attempts to swallow. However, it has been shown that NO may also be released in other contexts affecting feeding, raising the possibility that its role in learning is unrelated to signaling attempts to swallow. We confirmed that NO during learning signals attempts to swallow, by showing that a variety of behavioral effects on feeding of blocking or adding NO do not affect learning and memory that a food is inedible. In addition, histamine had effects similar to NO on learning that food is inedible, as expected if the transmitters are released together when animals attempt to swallow. Blocking histamine during training blocked long-term memory, and exogenous histamine substituted for attempts to swallow. NO also substituted for histamine during training. Histamine at concentrations relevant to learning activates neuron metacerebral cell (MCC). However, MCC activity is not a good monitor of attempts to swallow during training, since the neuron responds equally well to other stimuli. These findings support and extend the hypothesis that NO and histamine signal efforts to swallow during learning, acting on targets other than the MCC that specifically respond to attempts to swallow.

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Sensory function and gating of histaminergic neuron C2 in Aplysia

Cited by 43 publications

References 35 publications

Nitric Oxide Signals ThatAplysiaHave Attempted to Eat, a Necessary Component of Memory Formation After Learning That Food Is Inedible

Nitric Oxide Signals ThatAplysiaHave Attempted to Eat, a Necessary Component of Memory Formation After Learning That Food Is Inedible

State Dependence of Spike Timing and Neuronal Function in a Motor Pattern Generating Network

Nitric oxide and histamine signal attempts to swallow: A component of learning that food is inedible inAplysia

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