Neuronal Correlates of Habituation and Dishabituation of the Gill-Withdrawal Reflex in
            <i>Aplysia</i>

Kupfermann, Irving; Castellucci, Vincent F.; Pinsker, H. M.; Kandel, E. R.

doi:10.1126/science.167.3926.1743

Cited by 469 publications

(84 citation statements)

References 3 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…The possible role and site of homosynaptic depression during habituation in Aplysia was investigated initially in the siphonelicited gill withdrawal reflex Kupfermann et al, 1970;Pinsker et al, 1970;Carew et al, 1971). This work supported the conclusion that homosynaptic depression at the LE siphon sensory neurons underlies the response decrement observed in the behaving animal.…”

Section: Habituation In the Gill Withdrawal Reflexsupporting

confidence: 64%

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

Stopfer¹,

Carew

1996

J. Neurosci.

View full text Add to dashboard Cite

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.

show abstract

Section: Habituation In the Gill Withdrawal Reflexsupporting

confidence: 64%

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

Stopfer¹,

Carew

1996

J. Neurosci.

View full text Add to dashboard Cite

show abstract

“…Studies of the cellular correlates of habituation have shown that tactile stimulation of the siphon skin initiates a complex excitatory postsynaptic potential (EPSP), produced largely by direct synaptic connections from the sensory cells (7,13), that discharges the motor cells and causes gill contraction. Habituation produces a progressive decrease in the complex EPSP (17). Analyses of the various components of the reflex during short-term habituation (including measurements of the threshold and input conductance of the motor cell) indicate that the critical change occurs at the synapses between the sensory cell and the motor neurons and interneurons (refs.…”

Section: Methodsmentioning

confidence: 99%

A Quantal Analysis of the Synaptic Depression Underlying Habituation of the Gill-Withdrawal Reflex in Aplysia

Castellucci

Kandel

1974

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

278

131

View full text Add to dashboard Cite

Habituation, one of the simplest behavioral paradigms for studying memory, has recently been examined on the cellular level in the gill-withdrawal reflex in the mollusc Aplysia and in the escape response in crayfish. In both cases short-term habituation involved a decrease in excitatory synaptic transmission at the synapses between the sensory neurons and their central target cells. To analyze the mechanisms of the synaptic depression in Aplysia, we applied a quantal analysis to synaptic transmission between the sensory and motor neurons of the gillwithdrawal reflex. Our results indicate that short-term habituation results from a presynaptic mechanism: a decrease in the number of transmitter quanta released per impulse. The sensitivity of the postsynaptic receptor remains unaltered.Habituation, the decrease in a behavioral response to repeated presentation of a novel stimulus, is the most ubiquitous behavioral modification found in animals and man and one of the simplest paradigms for probing memory mechanisms (1-5). Habituation in different response systems and in different animals probably cannot be explained by a single neuronal mechanism. But in animals having a well-differentiated central nervous system, certain types of habituation share similar parametric features and time course, making it likely that in these cases a restricted family of mechanisms is involved. Thus certain reflex responses of vertebrates and higher invertebrates undergo short-term habituation lasting minutes and hours following a single training session of TO to 15 stimuli, but repeated training sessions can produce long-term habituation that lasts weeks. The acquisition of long-term habituation is sensitive to the pattern of stimulation. Spaced training is more effective in producing the long-term effects than is massed training. Finally, immediate restoration of a habituated response (dishabituation) can be produced by stimulating another pathway (2, 6).Because habituation can be studied in higher invertebrates and simple vertebrate systems, it is the only behavioral modification that has been successfully studied on the cellular level. In the gill-withdrawal reflex in the mollusc Aplysia (7) and in the escape response in crayfish (8), short-term habituation has been found to involve a similar cellular locus and a common synaptic change. There is a decrease in excitatory synaptic transmission (homosynaptic depression) at the central synapses made by the sensory neurons on their central target cells. Synaptic depression, although at a different locus, may also underlie habituation of the flexion reflex in vertebrates (9).The mechanism producing the synaptic depression is not known. It could be either a presynaptic change in transmitter release or a postsynaptic change in receptor responsiveness. To distinguish between these alternatives a quantal analysis is required. With rare exception (10, 11) this has been difficult to achieve in central neurons because they receive many synaptic inputs, making the analysis of spontaneous ...

show abstract

“…The gill-withdrawal reflex studied in Aplysia is a classic example of the habituation (desensitization) of reflex in response to repeated non-noxious stimuli [6][7][8]. Intuitively, this adaptation corresponds to the interpretation that since the sea slug is constantly bombarded with stimuli from sea waves, those harmless stimuli can be ignored if they do not represent potential threats to the animal.…”

Section: Gill-withdrawal Reflex As An Examplementioning

confidence: 99%

EMOTION-I Model: A Biologically-Based Theoretical Framework for Deriving Emotional Context of Sensation in Autonomous Control Systems

Tam

2007

TOCSJ

View full text Add to dashboard Cite

A theoretical model for deriving the origin of emotional functions from first principles is introduced. The model, called "Emotional Model Of the Theoretical Interpretations Of Neuroprocessing", abbreviated as the "EMO-TION", derives how emotional context can be evolved from innate responses. It is based on a biological framework for autonomous systems with minimal assumptions on the system or what emotion is. The first phase of the model (EMO-TION-I) addresses the progressive abstraction of the sensory input signals within relevant context of the environment to produce the appropriate output actions for survival. It uses a probabilistic feedforward and feedback neural network with multiple adaptable gains, self-adaptive learning rate and modifiable connection weights to produce a self-organizing, selfadaptive system incorporating associative reinforcement learning rules for conditioning and fixation of circuitry into hardwire to form innate responses such that contextual feel of sensation is evolved as an emergent property known as emotional feel.

show abstract

Neuronal Correlates of Habituation and Dishabituation of the Gill-Withdrawal Reflex in Aplysia

Cited by 469 publications

References 3 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

A Quantal Analysis of the Synaptic Depression Underlying Habituation of the Gill-Withdrawal Reflex in Aplysia

EMOTION-I Model: A Biologically-Based Theoretical Framework for Deriving Emotional Context of Sensation in Autonomous Control Systems

Contact Info

Product

Resources

About