Role of interneurons in defensive withdrawal reflexes in Aplysia.

Cleary, Len; Byrne, John H.; Frost, William N.

doi:10.1101/lm.2.3-4.133

Cited by 71 publications

(75 citation statements)

References 81 publications

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“…Our finding that a reduction in synaptic transmission in tail sensory neurons does not accompany habituation shifts the focus onto interneurons in the reflex circuits (Hawkins et al, 1981;Cleary et al, 1995;Frost and Kandel, 1995). In the case of tail-elicited siphon withdrawal, interneurons fully mediate sensory-to-motor communication .…”

Section: Additional Sites and Mechanisms Of Habituationmentioning

confidence: 86%

Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes ofAplysia

Stopfer¹,

Carew

1996

J. Neurosci.

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In cellular studies of habituation, such as in the gill and siphon withdrawal reflex to tactile stimulation of the siphon of Aplysia, a mechanism that has emerged as an explanation for response decrement during habituation is homosynaptic depression at sensory neurons mediating the behavioral response. We have examined the contribution of homosynaptic depression to habituation in sensory neurons that contribute to two reflex behaviors in Aplysia, tail withdrawal and siphon withdrawal, both elicited by threshold-level tail stimulation. In a companion paper (this issue), we reported that repeated tail stimulation, identical to that producing habituation in siphon withdrawal in freely moving animals, also produces habituation in reduced preparations. In this paper, we extend these behavioral findings by showing that in reduced preparations, identical tail stimulation also produces habituation of the tail withdrawal reflex. In addition, our cellular experiments show that (1) identified sensory and motor neurons in both reflex systems respond to identical repeated tail stimulation; in sensory neurons it produces a progressive decrease in spike number and increase in spike latency, and in motor neurons it produces progressive decrement in complex EPSPs and spike output. (2) Homosynaptic depression of the tail sensory neuron to tail motor neuron synapse does occur when the sensory neurons are activated repetitively by intracellular current. (3) Homosynaptic depression at this synapse does not occur when the sensory neurons are activated repetitively by threshold-level tail stimuli that elicit the behavioral reflex and cause habituation; rather, the sensory neurons exhibit significant heterosynaptic facilitation. Thus, in these reflexes, habituation is not accompanied by homosynaptic depression at the sensory neurons, suggesting that the plasticity underlying habituation occurs primarily at interneuronal sites.

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Section: Additional Sites and Mechanisms Of Habituationmentioning

confidence: 86%

Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes ofAplysia

Stopfer¹,

Carew

1996

J. Neurosci.

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“…Four types of interneurons are excitatory (L25, R25, L29, and L34), five are inhibitory (L16, L26, L30, L33, and Pl 4), and Pl 17 seems to be excitatory to tail MNs and inhibitory to tail SNs ( Fig. 1; Cleary et al 1995). When excitatory and inhibitory interneurons are recruited during siphon reflex retraction, their synaptic potentials sum at the level of MNs and various interneurons.…”

Section: Modulation Of Defensive Reflex Circuits By 5-ht During Sensimentioning

confidence: 99%

“…5-HT also induces metaplasticity at L30-L29 synapses (green) and increases glutamate responses in LFS MNs (orange). Adapted from Cleary et al 1995.…”

Section: Modulation Of Defensive Reflex Circuits By 5-ht During Sensimentioning

confidence: 99%

“…These reflexes involve three central ganglia: the pleural, pedal, and abdominal ganglia. A tactile stimulus applied to the tail or siphon activates tail or siphon SNs, which excite MNs through monosynaptic (SN-MN synapses) and polysynaptic pathways (for a more detailed review, see Cleary et al 1995;Frost and Kandel 1995). More than 10 types of interneurons are known to participate in these polysynaptic pathways between SNs and MNs: (1) L25, R25, L26, and L33 are recruited during siphon withdrawal reflex and respiratory pumping (Kanz et al 1979;Byrne 1983;Eberly and Pinsker 1984;Frost and Kandel 1995), (2) L16, L29, L30, L33, and L34 mediate siphon withdrawal reflex only, and (3) Pl 4 and Pl 17 are involved in reflex tail withdrawal (Buonomano et al 1992;Cleary and Byrne 1993;Xu et al 1994).…”

Section: Modulation Of Defensive Reflex Circuits By 5-ht During Sensimentioning

confidence: 99%

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Multiple Serotonergic Mechanisms Contributing to Sensitization in Aplysia: Evidence of Diverse Serotonin Receptor Subtypes

Barbas¹,

DesGroseillers²,

Castellucci³

et al. 2003

Learn. Mem.

105

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The neurotransmitter serotonin (5-HT) plays an important role in memory encoding in Aplysia. Early evidence showed that during sensitization, 5-HT activates a cyclic AMP-protein kinase A (cAMP-PKA)-dependent pathway within specific sensory neurons (SNs), which increases their excitability and facilitates synaptic transmission onto their follower motor neurons (MNs). However, recent data suggest that serotonergic modulation during sensitization is more complex and diverse. The neuronal circuits mediating defensive reflexes contain a number of interneurons that respond to 5-HT in ways opposite to those of the SNs, showing a decrease in excitability and/or synaptic depression. Moreover, in addition to acting through a cAMP-PKA pathway within SNs, 5-HT is also capable of activating a variety of other protein kinases such as protein kinase C, extracellular signal-regulated kinases, and tyrosine kinases. This diversity of 5-HT responses during sensitization suggests the presence of multiple 5-HT receptor subtypes within the Aplysia central nervous system. Four 5-HT receptors have been cloned and characterized to date. Although several others probably remain to be characterized in molecular terms, especially the Gs-coupled 5-HT receptor capable of activating cAMP-PKA pathways, the multiplicity of serotonergic mechanisms recruited into action during learning in Aplysia can now be addressed from a molecular point of view.The marine mollusk Aplysia has proven to be a powerful model system for the study of learning and memory. This animal displays several simple forms of nonassociative learning, such as habituation, dishabituation, and sensitization (Pinsker et al. 1970(Pinsker et al. , 1973Carew et al. 1971), but also more complex forms of associative learning such as classical, operant, and fear conditioning (Carew et al. , 1983Walters et al. 1981; Lechner et al. 2000a,b;Brembs et al. 2002). The strength of this model system arises from the relative simplicity of its central nervous system (CNS), which contains a small number of neurons, some of which are well characterized both morphologically and electrophysiologically. Thus, one can study a specific synaptic connection in different animals subjected to a wide variety of behavioral training protocols. For this reason, it has been possible to discover many of the mechanisms of learning and memory in this animal at the behavioral, cellular, and molecular levels, and provide direct evidence that certain forms of learning rely on the plasticity of individual synaptic connections (for review, see Kandel 2001).One of the best characterized forms of learning in Aplysia is sensitization, in which a noxious stimulus facilitates an animal's pre-existing response to the presentation of another innocuous stimulus. It has been most thoroughly studied in the defensive reflex responses of Aplysia. For example, a mild tactile stimulus applied to the tail evokes the retraction of respiratory organs (gill and siphon) inside the mantle cavity situated on the back of the animal. The stre...

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“…Although the T-TWR can be expressed through the central tail SN-MN monosynaptic circuit (Walters et al 1983a), there also exists a parallel polysynaptic circuit involving identified interneurons (INs: RPl4 and LP117) (Buonomano et al 1992;Cleary and Byrne 1993;Xu et al 1994). Whereas the monosynaptic circuit is believed to control the early response amplitude and slope of the T-TWR, the polysynaptic circuit may contribute to shaping the later portion of the response where it could be a major determinant of the T-TWR duration (see White et al 1993;Cleary et al 1995). A role for the recruitment of plasticity in INs for short-term modifications of behavior is well established (Frost et al 1988;Trudeau and Castellucci 1992;Fischer and Carew 1995;Frost and Kandel 1995;Wright and Carew 1995;Xu et al 1995).…”

Section: Interneurons May Help Shape the Reflex Responsementioning

confidence: 99%

The tail-elicited tail withdrawal reflex of Aplysia is mediated centrally at tail sensory-motor synapses and exhibits sensitization across multiple temporal domains

Philips¹,

Sherff²,

Menges³

et al. 2011

Learn. Mem.

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The defensive withdrawal reflexes of Aplysia californica have provided powerful behavioral systems for studying the cellular and molecular basis of memory formation. Among these reflexes the tail-elicited tail withdrawal reflex (T-TWR) has been especially useful. In vitro studies examining the monosynaptic circuit for the T-TWR, the tail sensory-motor (SN-MN) synapses, have identified the induction requirements and molecular basis of different temporal phases of synaptic facilitation that underlie sensitization in this system. They have also permitted more recent studies elucidating the role of synaptic and nuclear signaling during synaptic facilitation. Here we report the development of a novel, compartmentalized semi-intact T-TWR preparation that allows examination of the unique contributions of processing in the SN somatic compartment (the pleural ganglion) and the SN-MN synaptic compartment (the pedal ganglion) during the induction of sensitization. Using this preparation we find that the T-TWR is mediated entirely by central connections in the synaptic compartment. Moreover, the reflex is stably expressed for at least 24 h, and can be modified by tail shocks that induce sensitization across multiple temporal domains, as well as direct application of the modulatory neurotransmitter serotonin. This preparation now provides an experimentally powerful system in which to directly examine the unique and combined roles of synaptic and nuclear signaling in different temporal domains of memory formation.

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Role of interneurons in defensive withdrawal reflexes in Aplysia.

Cited by 71 publications

References 81 publications

Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes ofAplysia

Heterosynaptic Facilitation of Tail Sensory Neuron Synaptic Transmission during Habituation in Tail-Induced Tail and Siphon Withdrawal Reflexes ofAplysia

Multiple Serotonergic Mechanisms Contributing to Sensitization in Aplysia: Evidence of Diverse Serotonin Receptor Subtypes

The tail-elicited tail withdrawal reflex of Aplysia is mediated centrally at tail sensory-motor synapses and exhibits sensitization across multiple temporal domains

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