Effects of stimulus frequency and intensity on habituation and sensitization in acute spinal cat

doi:10.1016/0031-9384(69)90194-2

Physiology & Behavior

Volume 4, Issue 3, May 1969, Pages 383-388

https://doi.org/10.1016/0031-9384(69)90194-2 Get rights and content

Abstract

Habituation and sensitization of the flexor withdrawal reflex (tibialis anterior muscle) were studied in acute spinal cat as a function of stimulus intensity and frequency for frequencies ranging above $12$ sec. The following relationships were consistently observed: (1) habituation is an exponential decline in response amplitude which occurs as a function of iterated stimulation of cutaneous afferents. In some instances habituation may be described as linear over much of its course; (2) habituation occurs more rapidly and to a greater degree of response decrement for higher frequencies of stimulation; (3) habituation is more pronounced for low intensities of stimulation than for high intensities, and; (4) sensitization occurs as a response increment with repetitive stimulation of cutaneous afferents under certain circumstances and may show two distinct time courses, short-term and long-term sensitization. These two phenomena may be differentiated on the basis of stimulus intensity, frequency and their interaction.

References (21)

J.P. Griffin et al.
The effect of bladder distension on habituation of the flexor withdrawal reflex in the decerebrate spinal cat
Brain Res.
(1968)
F.B. Beswick et al.
Reflex effects of repetitive stimulation of Group I muscle afferent fibres
J. Physiol.
(1955)
J.S. Buchwald et al.
Progressive changes in efferent unit response to repeated cutaneous stimulation in spinal cats
J. Neurophysiol.
(1965)
J.P. Griffin et al.
Habituation of the flexor reflex in the rat
J. Physiol.
(1967)
J.D. Harris
Habituatory response decrement in the intact organism
Psychol. Bull.
(1943)
R. Hinde
G. Horn
Neuronal mechanisms of habituation
Nature
(1967)
J.I. Hubbard et al.
An electrophysiological investigation of mammalian motor nerve terminals
J. Physiol.
(1963)
D.P. Lloyd
Electrotonus in dorsal nerve roots
D.P. Lloyd
Post-tetanic potentiation of responses in monosynaptic reflex pathways of the spinal cord
J. gen. Physiol.
(1949)

There are more references available in the full text version of this article.

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Of the total 327 animals tested across all experiments, 45 animals were excluded based on this criteria. In many studies of habituation, the ability to reverse habituation (dishabituation) is used to confirm that the observed response decrement is not due to fatigue or sensory adaption (Groves, Lee, & Thompson, 1970; Rankin et al., 2009). Since noxious stimuli are often effective at producing dishabituation, we used the post-test delivery of the nociceptive thermal stimulus (i.e. the Hargreaves apparatus) as a convenient dishabituating stimulus (Fig. 2A).
Repetitive activation of non-nociceptive afferents is known to attenuate nociceptive signaling. However, the functional details of how this modulatory process operates are not understood and this has been a barrier in using such stimuli to effectively treat chronic pain. The present study tests the hypothesis that the ability of repeated non-nociceptive stimuli to reduce nociception is a form of generalized habituation from the non-nociceptive stimulus-response pathway to the nociceptive pathway. Habituation training, using non-nociceptive mechanosensory stimuli, did reduce responses to nociceptive thermal stimulation. This generalization of habituation to nociceptive stimuli required endocannabinoid-mediated neuromodulation, although disrupting of endocannabinoid signaling did not affect “direct” habituation of to the non-nociceptive stimulus. Surprisingly, the reduced response to nociceptive stimuli following habituation training was very long-lasting (3–8 days). This long-term habituation required endocannabinoid signaling during the training/acquisition phase, but endocannabinoids were not required for post-training retention phase. The implications of these results are that applying principles of habituation learning could potentially improve anti-nociceptive therapies utilizing repeated non-nociceptive stimulation such as transcutaneous nerve stimulation (TENS), spinal cord stimulation (SCS), or electro-acupuncture.
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However, there are some features associated with sensory adaptation that allow discarding this phenomenon and confirming habituation in learning experiments. In sensory adaptation, stronger stimuli produce a higher decrease in the response; the opposite is expected in habituation, where response decrements to higher stimulus intensities take longer (Asztalos et al., 2007; Groves et al., 1969; Kuenen and Baker, 1981). In addition, the recovery of the response is usually faster in sensory adaptation, while habituation shows more temporal stability (Devaud et al., 2001; Kuenen and Baker, 1981).
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A crucial difference that determines whether habituation or sensitization occurs is the intensity of the stimulus. Habituation is more rapid with low-intensity stimulation (e.g., Groves et al., 1968); with intense or noxious stimuli, sensitization is likely to occur first, followed by habituation (e.g., Davis et al., 1982). The presentation of a novel, arousing (i.e., sensitizing) stimulus can cause the recovery of a previously habituated response; this effect is known as dishabituation (Thompson and Spencer, 1966; Castellucci and Kandel, 1976).
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Food-induced arousal and nonassociative learning in honeybees: Dependence of sensitization on the application site and duration of food stimulation
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Stimulus-induced arousal (sensitization) of a component of appetitive behavior in honeybees, the proboscis extension reflex (PER), was used to investigate different aspects of nonassociative memory. The sensitizing stimulus (sucrose solution) was applied to one antenna, as a compound to antenna and proboscis, and to the proboscis. Stimulus duration was either 1 or 3 s. Sensitization was evaluated by monitoring PER toward an odor before (pretest) and after (test) application of the sensitizing stimulus. All responses were quantified by recording from muscle M17 which represents the motor program of PER. Data were analyzed by determining (1) the response probability to the odor and (2) the response strength by determing the number of M17-spikes and the percentage of licking bees per trial. The analysis of the response probability led to two main results: the proportion of animals responding to the test odor depended on stimulus site, and, dependent on stimulus site, a longer application of the sensitizing stimulus resulted in different sensitization rates. The strength of the sensitized response, however, did not correspond to the probability, with which it was elicited, but rather to the strength of the response to the sensitizing stimulus itself. Furthermore, the three groups were not equally affected by the short and long stimulation. The analysis of the proportion of animals licking during test confirmed the data obtained using the number of muscle spikes as a measure of response strength. These results suggest an internal evaluation of the sensitizing stimulus depending on its quality and intensity. The differential affects after antennal and proboscis stimulation may be realized via an arousal system which has two independent functions, a permissive one modulating response probability and one modulating response strength. The permissive function of arousal may be regulated via an intervening inhibitory system whose activation critically depends on the functional significance of the arousing stimulus. The content of this short-term form of memory may be interpreted as an expectation for food which is regulated according to experienced consequences.

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^☆: Supported in part by research grant NB 02161 from the National Institutes of Health and MH 1, 279-01 from the National Institute of Mental Health, Research Scientist award MH 6650 from the National Institute of Mental Health, and the National Science Foundation Undergraduate Research Participation Program GY 4507. The authors gratefully acknowledge the skilled technical assistance of Sarah Beydler.

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Effects of stimulus frequency and intensity on habituation and sensitization in acute spinal cat☆

Abstract

Brain Res.

Reflex effects of repetitive stimulation of Group I muscle afferent fibres

J. Physiol.

Progressive changes in efferent unit response to repeated cutaneous stimulation in spinal cats

J. Neurophysiol.

Habituation of the flexor reflex in the rat

J. Physiol.

Habituatory response decrement in the intact organism

Psychol. Bull.

Neuronal mechanisms of habituation

Nature

An electrophysiological investigation of mammalian motor nerve terminals

J. Physiol.

Electrotonus in dorsal nerve roots

Post-tetanic potentiation of responses in monosynaptic reflex pathways of the spinal cord

J. gen. Physiol.