Habituation: a model phenomenon for the study of neuronal substrates of behavior

Thompson, Richard F.; Spencer, William A.

doi:10.1037/h0022681

Cited by 2,608Memory and Neural MechanismsNeural and Behavioral Psychology StudiesNeuroscience and Neuropharmacology Research

Habituation: a model phenomenon for the study of neuronal substrates of behavior

Thompson, Richard F., Spencer, William A.·1966·Psychological Review

DOI 10.1037/h0022681

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In habituation, behavioral and physiological responses during initial exposure to a stimulus diminish with repeated presentations of that stimulus.
“In habituation, behavioral and physiological responses during initial exposure to a stimulus diminish with repeated presentations of that stimulus (Grissom and Bhatnagar, 2009;Leussis and Bolivar, 2006;Thompson and Spencer, 1966).”
From Physiological feelings (2019) · cites this paper as Thompson and Spencer, 1966

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THE EFFECT OF PREVIOUS STIMULATION ON THE RESPONSIVENESS OF THE CAT'S NICTITATING MEMBRANE SENSITIZED BY DENERVATION
Simeone, F. A. (1938) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1938.122.3.650 · Cited by 2 · see citing works

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Emotional processing of fear: Exposure to corrective information.
Foa, E. B., & Kozak, M. J. (1986) · Psychological Bulletin · doi:10.1037/0033-2909.99.1.20 · Cited by 5,396 · see citing works
“consistent with the Thompson and Spencer (1966) usage of the term:”
The N1 wave of the human electric and magnetic response to sound: A review and an analysis of the component structure
Näätänen, R., & Picton, T. (1987) · Psychophysiology · doi:10.1111/j.1469-8986.1987.tb00311.x · Cited by 3,321 · see citing works
Emotion elicitation using films
Gross, J. J., & Levenson, R. W. (1995) · Cognition & Emotion · doi:10.1080/02699939508408966 · Cited by 2,179 · see citing works
Habituation: a dual-process theory.
Groves, P. M., & Thompson, R. F. (1970) · Psychology Review · doi:10.1037/h0029810 · Cited by 2,110 · see citing works
Self-citation
Habituation revisited: An updated and revised description of the behavioral characteristics of habituation
Rankin, C. H., Abrams, T., Barry, R. J., Bhatnagar, S., Clayton, D. F., Colombo, J., Coppola, G., Geyer, M. A., Glanzman, D. L., Marsland, S., et al. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.09.012 · Cited by 1,665 · see citing works
“There are nine characteristics of habituation that are based on the characteristics described in Thompson and Spencer (1966) ; one additional characteristic was added as a result of our deliberations.”
BackgroundMethodSelf-citation
Molecular Biology of Learning: Modulation of Transmitter Release
Kandel, E. R., & Schwartz, J. H. (1982) · Science · doi:10.1126/science.6289442 · Cited by 1,551 · see citing works
The Short-Run and Long-Run Effects of Behavioral Interventions: Experimental Evidence from Energy Conservation
Allcott, H., & Rogers, T. (2014) · American Economic Review · doi:10.1257/aer.104.10.3003 · Cited by 1,340 · see citing works
Cognitive Neuroscience and the Study of Memory
Milner, B. A., Squire, L. R., & Kandel, E. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80987-3 · Cited by 1,300 · see citing works
Plasticity and Primary Motor Cortex
Sanes, J. N., & Donoghue, J. P. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.393 · Cited by 1,202 · see citing works
“The mechanisms by which such changes may occur have been discussed above, but it also remains unclear whether the MI flexibility adheres to rules of behavioral or neural habituation (Thompson & Spencer 1966).”
Background
The Neurobiology of Learning and Memory
Thompson, R. F. (1986) · Science · doi:10.1126/science.3738519 · Cited by 1,159 · see citing works
Self-citation
Mechanisms of fear extinction
Myers, K. M., & Davis, M. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001939 · Cited by 1,277 · see citing works
Functions of the frontal cortex of the rat: A comparative review
Kolb, B. E. (1984) · Brain Research Reviews · doi:10.1016/0165-0173(84)90018-3 · Cited by 882 · see citing works
Behavioral studies of Pavlovian conditioning
Rescorla, R. A. (1988) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.11.030188.001553 · Cited by 715 · see citing works
“That course can be studied as a function of such primitive variables as stimulus intensity, modality, and spacing (e.g. Thompson & Spencer 1966).”
Background
Contingent negative variation (CNV) and psychological processes in man
Tecce, J. J. (1972) · Psychological Bulletin · doi:10.1037/h0032177 · Cited by 671 · see citing works
Chemotaxis by the Nematode <i>Caenorhabditis elegans:</i> Identification of Attractants and Analysis of the Response by Use of Mutants
Ward, S. (1973) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.70.3.817 · Cited by 572 · see citing works
Habituation to repeated stress: Get used to it
Grissom, N., & Bhatnagar, S. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.07.001 · Cited by 552 · see citing works
“This theme encompasses both Criterion 1, the basic phenomenon of habituation, and Criterion 9, habituation of responses to dishabituating stimuli, as the latter can be viewed as a special case of the former (Thompson & Spencer 1966).”
BackgroundMethodInfluential
The Comparator Hypothesis: A Response Rule for The Expression of Associations
Miller, R. R., & Matzel, L. D. (1988) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)60038-9 · Cited by 518 · see citing works
Locomotion in larval zebrafish: Influence of time of day, lighting and ethanol
MacPhail, R. C., Brooks, J., Hunter, D. L., Padnos, B. K., Irons, T. D., & Padilla, S. (2008) · NeuroToxicology · doi:10.1016/j.neuro.2008.09.011 · Cited by 475 · see citing works
Ecological And Evolutionary Aspects Of Learning In Phytophagous Insects
Papaj, D. R., & Prokopy, R. J. (1989) · Annual Review of Entomology · doi:10.1146/annurev.en.34.010189.001531 · Cited by 476 · see citing works
Neuroethology of releasing mechanisms: Prey-catching in toads
Ewert, J.-P. (1987) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00023128 · Cited by 463 · see citing works
Analyzing habituation responses to novelty in zebrafish (Danio rerio)
Wong, K., Elegante, M. F., Bartels, B. K., Elkhayat, S. I., Tien, D. H., Roy, S. S., Goodspeed, J. R., Suciu, C., Tan, J., Grimes, C., et al. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.023 · Cited by 464 · see citing works
“In general, our study parallels literature on rodent habituation responses to novelty, and reconfirms zebrafish as a promising model for cognitive neurobehavioral research. nxiety patial working memory .”
Background
Unpredictable and Uncontrollable Aversive Events
Seligman, M. E. P., Maier, S. F., & Solomon, R. L. (1971) · Elsevier eBooks · doi:10.1016/b978-0-12-137950-6.50011-0 · Cited by 459 · see citing works
Startle response models of sensorimotor gating and habituation deficits in schizophrenia
Geyer, M. A., Swerdlow, N. R., Mansbach, R. S., & Braff, D. L. (1990) · Brain Research Bulletin · doi:10.1016/0361-9230(90)90241-q · Cited by 456 · see citing works
The search for the engram.
Thompson, R. F. (1976) · American Psychologist · doi:10.1037//0003-066x.31.3.209 · Cited by 450 · see citing works
Self-citation
Long-term and short-term plasticity in the CA1, CA3, and dentate regions of the rat hippocampal slice
Alger, B. E., & Teyler, T. J. (1976) · Brain Research · doi:10.1016/0006-8993(76)90858-1 · Cited by 449 · see citing works
Habituation: A history
Thompson, R. F. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.07.011 · Cited by 448 · see citing works
“These and other views are treated at length in a number of publication, e.g., Groves and Thompson, 1970; Peeke and Herz, 1973 a&b; Thompson and Spencer, 1966.”
BackgroundSelf-citation
State dependent activity in monkey visual cortex
Haenny, P. E., & Schiller, P. H. (1988) · Experimental Brain Research · doi:10.1007/bf00247569 · Cited by 443 · see citing works
“Although our paradigm, in which individual stimuli were presented for 280 ms durations with 280 ms interstimulus times and 4-6 s intervals between stimulus sequences, does not strictly fulfill all criteria of classic short-term habituation (Thompson and Spencer 1966), we did observe, in many cells, an attenuation of t…”
Method
Dynamic systems theory and the complexity of change
Thelen, E. (2005) · Psychoanalytic Dialogues · doi:10.1080/10481881509348831 · Cited by 441 · see citing works
“habituation (Thompson and Spencer, 1966) ensure that infants fill their visual world with changing scenes.”
Background
Impact of Maternal Stress, Depression and Anxiety on Fetal Neurobehavioral Development
KINSELLA, M. T., & MONK, C. (2009) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181b52df1 · Cited by 422 · see citing works
Habituation and Dishabituation of the Gill-Withdrawal Reflex in Aplysia
Pinsker, H. M., Kupfermann, I., Castellucci, V. F., & Kandel, E. R. (1970) · Science · doi:10.1126/science.167.3926.1740 · Cited by 431 · see citing works
Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli
Wright, C. I., Fischer, H., Whalen, P. J., McInerney, S. C., Shin, L. M., & Rauch, S. L. (2001) · Neuroreport · doi:10.1097/00001756-200102120-00039 · Cited by 533 · see citing works
Behavioral functions of the reticular formation
Siegel, J. M. (1979) · Brain Research Reviews · doi:10.1016/0165-0173(79)90017-1 · Cited by 421 · see citing works
Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis
Chan, A. A. Y.-H., Giraldo-Perez, P., Smith, S. M., & Blumstein, D. T. (2010) · Biology Letters · doi:10.1098/rsbl.2009.1081 · Cited by 419 · see citing works
“As anthropogenic sounds become more frequent, the strength of an animal’s response to them may decrease owing to habituation (Thompson & Spencer 1966).”
Background
Startle Habituation and Sensorimotor Gating in Schizophrenia and Related Animal Models
Geyer, M. A., & BRAFF, D. L. (1987) · Schizophrenia Bulletin · doi:10.1093/schbul/13.4.643 · Cited by 411 · see citing works
“Although it has frequently been assumed that short-term or "withinsession" habituation is mediated by changes intrinsic to the startle reflex pathway itself (Thompson and Spencer 1966; Groves and Thompson 1970), this assumption does not preclude the importance of Figure 3.”
Background
Competing for Consumer Identity: Limits to Self-Expression and the Perils of Lifestyle Branding
Chernev, A., Hamilton, R., & Gal, D. (2011) · Journal of Marketing · doi:10.1509/jmkg.75.3.66 · Cited by 385 · see citing works
“People’s ability to “recover” from satiation with the passage of time has been documented in other domains as well (McSweeney and Swindell 1999; Thompson and Spencer 1966).”
Background
Differential Influence of Associative and Nonassociative Learning Mechanisms on the Responsiveness of Prefrontal and Accumbal Dopamine Transmission to Food Stimuli in Rats FedAd Libitum
Bassareo, V., & Chiara, G. D. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-02-00851.1997 · Cited by 375 · see citing works
“Therefore, after stimulus preexposure, a form of habituation, defined as a decrease in response to a repetitive stimulus (Thompson and Spencer, 1966), differentially affects mesolimbic as compared with mesocortical DA transmission.”
Background
Is there a cell-biological alphabet for simple forms of learning?
Hawkins, R. D., & Kandel, E. R. (1984) · Psychological Review · doi:10.1037/0033-295x.91.3.375 · Cited by 436 · see citing works
Zebrafish Larvae as a Behavioral Model in Neuropharmacology
Basnet, R., Zizioli, D., Taweedet, S., Finazzi, D., & Memo, M. (2019) · Biomedicines · doi:10.3390/biomedicines7010023 · Cited by 328 · see citing works
“Habituation is a non-associative form of learning in which a repeated stimulus leads to an attenuated response [58,68].”
Background
TIME AND MEMORY: TOWARDS A PACEMAKER‐FREE THEORY OF INTERVAL TIMING
Staddon, J. E. R., & Higa, J. J. (1999) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.1999.71-215 · Cited by 375 · see citing works
Inhibitory component of externally controlled covert orienting in visual space.
Maylor, E. A., & Hockey, R. J. (1985) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037/0096-1523.11.6.777 · Cited by 374 · see citing works
Decrement of the N1 auditory event-related potential with stimulus repetition: habituation vs. refractoriness
Budd, T. W., Barry, R. J., Gordon, E., RENNIE, C. J., & Michie, P. T. (1998) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(98)00040-3 · Cited by 353 · see citing works
A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use
Chiara, G. D. (1998) · Journal of Psychopharmacology · doi:10.1177/026988119801200108 · Cited by 346 · see citing works
Activation theory and task design
Scott, W. E. (1966) · Organizational Behavior and Human Performance · doi:10.1016/0030-5073(66)90003-1 · Cited by 334 · see citing works
Recognition memory: neuronal substrates of the judgement of prior occurrence
Brown, M. W., & Xiang, J. ‐. (1998) · Progress in Neurobiology · doi:10.1016/s0301-0082(98)00002-1 · Cited by 329 · see citing works
“However, the response changes to be discussed in this review are stronger and far more rapid than are those that accumulate over many repetitions in habituation (Thompson and Spencer, 1966; Horn, 1967; Kandel and Spencer, 1968; Brown, 1996) (see further Section 5.”
BackgroundInfluential
The effects of visual stimulation and memory on neurons of the hippocampal formation and the neighboring parahippocampal gyrus and inferior temporal cortex of the primate
Riches, I. P., Wilson, F., & Mw, B. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-06-01763.1991 · Cited by 336 · see citing works
“They may therefore be distinguished from those of classical short-term habituation (Thompson and Spencer, 1966).”
Background
Is The Cerebral Cortex Hyperexcitable or Hyperresponsive in Migraine?
Coppola, G., Pierelli, F., & Schoenen, J. (2007) · Cephalalgia · doi:10.1111/j.1468-2982.2007.01500.x · Cited by 332 · see citing works
Altered processing of sensory stimuli in patients with migraine
de Tommaso, M., Ambrosini, A., Brighina, F., Coppola, G., Perrotta, A., Pierelli, F., Sandrini, G., Valeriani, M., Marinazzo, D., Stramaglia, S., et al. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.14 · Cited by 329 · see citing works
A Quantal Analysis of the Synaptic Depression Underlying Habituation of the Gill-Withdrawal Reflex in Aplysia
Castellucci, V. F., & Kandel, E. R. (1974) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.71.12.5004 · Cited by 317 · see citing works
In Search of Memory Traces
Thompson, R. F. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070239 · Cited by 314 · see citing works
Self-citation
Determination of motor activity and anxiety-related behaviour in rodents: methodological aspects and role of nitric oxide
Sestakova, N., Púzserová, A., Kluknavský, M., & Bernátová, I. (2013) · Interdisciplinary Toxicology · doi:10.2478/intox-2013-0020 · Cited by 314 · see citing works
“As described by Thompson and Spencer (1966), habituation is a form of simple nonassociative learning, in which the volume of the response to a specific stimulus decreases with repeated exposure to that stimulus.”
Background
Pathways of the Past: the Imprint of Memory
Horn, G. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1324 · Cited by 308 · see citing works
Habituation in rodents: a review of behavior, neurobiology, and genetics
LEUSSIS, M., & BOLIVAR, V (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2006.03.006 · Cited by 330 · see citing works
Failure in treating obsessive–compulsives
Foa, E. B. (1979) · Behaviour Research and Therapy · doi:10.1016/0005-7967(79)90031-7 · Cited by 305 · see citing works
Habituation in fetuses of diabetic mothers
Doherty, N., & Hepper, P. G. (2000) · Early Human Development · doi:10.1016/s0378-3782(00)00089-x · Cited by 296 · see citing works
The smell of danger: A behavioral and neural analysis of predator odor-induced fear
Takahashi, L. K., Nakashima, B. R., Hong, H., & Watanabe, K. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.008 · Cited by 298 · see citing works
“Repeated exposure to a stimulus often leads to habituation or a response decrement, which is a fundamental process of the nervous system (Thompson and Spencer, 1966).”
BackgroundInfluential
Repetition and Event-related Potentials: Distinguishing Early and Late Processes in Affective Picture Perception
Codispoti, M., Ferrari, V., & Bradley, M. M. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.4.577 · Cited by 288 · see citing works
“Habituation of responding to stimuli that are repeatedly processed is a central feature of stimulus orienting theories (Thompson & Spencer, 1966; Harris, 1943) and is held to reflect reduced attentional processing of a stimulus as its novelty wanes (Öhman, 1992; Siddle & Spinks, 1992; Kahneman,…”
Background
Effects of interstimulus interval length and variability on startle-response habituation in the rat.
Davis, M. (1970) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0029472 · Cited by 284 · see citing works
Full Weight-Bearing Hindlimb Standing Following Stand Training in the Adult Spinal Cat
de Leon, R. D., Hodgson, J. A., Roy, R. R., & Edgerton, V. R. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.1.83 · Cited by 279 · see citing works
WHAT'S ELEMENTARY ABOUT ASSOCIATIVE LEARNING?
Wasserman, E. A., & Miller, R. R. (1997) · Annual Review of Psychology · doi:10.1146/annurev.psych.48.1.573 · Cited by 277 · see citing works
“However, habituation wanes rapidly with increases in the retention interval (Thompson & Spencer 1966), whereas the CS-preexposure effect does not (Hall & Schachtman 1987).”
Background
Phytochemicals and Insect Control: An Antifeedant Approach
Koul, O. (2008) · Critical Reviews in Plant Sciences · doi:10.1080/07352680802053908 · Cited by 275 · see citing works
“Habituation differs from sensory adaptation in its ability to be terminated or reversed immediately by a novel or noxious stimulus (Thompson and Spencer, 1966).”
Background
Moral Suasion and Economic Incentives: Field Experimental Evidence from Energy Demand
Ito, K., Ida, T., & Tanaka, M. (2018) · American Economic Journal Economic Policy · doi:10.1257/pol.20160093 · Cited by 274 · see citing works
Neuroconstructivism - IHow the brain constructs cognition
Mareschal, D., Johnson, M. H., Sirois, S., Spratling, M., Thomas, M. S. C., & Westermann, G. (2007) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780198529910.001.0001 · Cited by 271 · see citing works
Effect of naloxone and morphine on various forms of memory in the rat: Possible role of endogenous opiate mechanisms in memory consolidation
Izquierdo, I. (1979) · Psychopharmacology · doi:10.1007/bf00427631 · Cited by 268 · see citing works
PERCEPTUAL‐COGNITIVE DEVELOPMENT IN INFANCY: A GENERALIZED EXPECTANCY MODEL AS A FUNCTION OF THE MOTHER‐INFANT INTERACTION1
Lewis, M., & Goldberg, S. (1968) · ETS Research Bulletin Series · doi:10.1002/j.2333-8504.1968.tb00568.x · Cited by 267 · see citing works
Associative and nonassociative theories of the UCS preexposure phenomenon: Implications for Pavlovian conditioning.
Randich, A., & LoLordo, V. M. (1979) · Psychological Bulletin · doi:10.1037/0033-2909.86.3.523 · Cited by 265 · see citing works
Psychic cost of adaptation to an environmental stressor.
Glass, D. C., Singer, J. E., & Friedman, L. N. (1969) · Journal of Personality and Social Psychology · doi:10.1037/h0027629 · Cited by 264 · see citing works
Reduced Neural Habituation in the Amygdala and Social Impairments in Autism Spectrum Disorders
Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., & Aylward, E. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2008.07101681 · Cited by 255 · see citing works
Neuronal Activity in Medial Frontal Cortex During Learning of Sequential Procedures
Nakamura, K., Sakai, K., & Hikosaka, O. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.5.2671 · Cited by 262 · see citing works
“The ‘‘habituation’’-like behavior of pre-SMA neurons would raise the possibility that they encode ‘‘arousal’’ or ‘‘vigilance’’ (Thompson and Spencer 1966; Vinogradova and Sokolov 1975).”
Short-term habituation of the auditory evoked response in man
Fruhstorfer, H., Soveri, P., & Järvilehto, T. (1970) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(70)90183-5 · Cited by 259 · see citing works
Using dynamic field theory to rethink infant habituation.
Schöner, G., & Thelen, E. (2006) · Psychological Review · doi:10.1037/0033-295x.113.2.273 · Cited by 259 · see citing works
“The processes must be working whether the stimuli have rich " cognitive " content or much simpler aversive consequences (Thompson & Spencer, 1966).”
Background
QUANTITATIVE EVOKED POTENTIAL CORRELATES OF THE PROBABILITY OF EVENTS
Tueting, P. A., Sutton, S., & Zubin, J. (1970) · Psychophysiology · doi:10.1111/j.1469-8986.1970.tb01763.x · Cited by 256 · see citing works
A physiological model of phobic anxiety and desensitization
LADER, M. H., & Mathews, A. (1968) · Behaviour Research and Therapy · doi:10.1016/0005-7967(68)90021-1 · Cited by 253 · see citing works
Infant visual habituation
Colombo, J., & Mitchell, D. W. (2009) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.06.002 · Cited by 237 · see citing works
“Theoretical Models Although the literature on habituation flourished during the 1960s and 1970s (Groves & Thompson, 1970; Thompson & Spencer, 1966), the theoretical context for addressing infant visual habituation was relatively sparse (Lewis & Baldini, 1979).”
Hate Speech Epidemic. The Dynamic Effects of Derogatory Language on Intergroup Relations and Political Radicalization
Bilewicz, M., & Soral, W. (2020) · Political Psychology · doi:10.1111/pops.12670 · Cited by 283 · see citing works
Physiological plasticity in auditory cortex: rapid induction by learning.
Weinberger, N., & Diamond, D. (1987) · Progress in neurobiology · doi:10.1016/0301-0082(87)90014-1 · Cited by 254 · see citing works
Non-Associative Learning in Larval Zebrafish
Best, J. D., Berghmans, S., Hunt, J., Clarke, S. C., Fleming, A., Goldsmith, P., & Roach, A. G. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301489 · Cited by 241 · see citing works
“This is in keeping with the criterion that the more rapid the frequency of stimulation the more rapidly habituation is seen (Thompson and Spencer, 1966).”
BackgroundResultInfluential
Detecting Moments of Stress from Measurements of Wearable Physiological Sensors
Kyriakou, K., Resch, B., Sagl, G., Petutschnig, A., Werner, C., Niederseer, D., Liedlgruber, M., Wilhelm, F. H., Osborne, T., & Pykett, J. (2019) · Sensors · doi:10.3390/s19173805 · Cited by 242 · see citing works
“This concurs with the phenomenon of habituation, describing the reduction of the physiological responses elicited by repeated exposure to a monotypic stressor [80].”
Background
Plasma corticosterone levels during repeated presentation of two intensities of restraint stress: chronic stress and habituation
Pitman, D. L., Ottenweller, J. E., & Natelson, B. H. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90097-2 · Cited by 295 · see citing works
Vestibulospinal and Reticulospinal Systems
Wilson, V. J., & Peterson, B. W. (1981) · Comprehensive physiology · doi:10.1002/cphy.cp010214 · Cited by 237 · see citing works
Mechanisms underlying spontaneous recovery in autoshaping.
Robbins, S. J. (1990) · Journal of Experimental Psychology Animal Behavior Processes · doi:10.1037/0097-7403.16.3.235 · Cited by 234 · see citing works
Habituation and sensitization in primary headaches
Coppola, G., Lorenzo, C. D., Schoenen, J. E., & Pierelli, F. (2013) · The Journal of Headache and Pain · doi:10.1186/1129-2377-14-65 · Cited by 237 · see citing works
“It is an ubiquitous phenomenon observed in different experimental settings and in neuronal circuits of a wide range of complexity, from the withdrawal reflex of the gill and siphon in Aplysia to the autonomic and behavioral component of the whole-of-body reflex called the “orienting response” in humans [5-7].”
Background
Physiological feelings
Pace-Schott, E. F., Amole, M. C., Aue, T., Balconi, M., Bylsma, L. M., Critchley, H., Demaree, H. A., Friedman, B. H., Gooding, A. E. K., Gosseries, O., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.002 · Cited by 221 · see citing works
“posure to a stimulus diminish with repeated presentations of that stimulus (Grissom and Bhatnagar, 2009; Leussis and Bolivar, 2006; Thompson and Spencer, 1966).”
A Computational Approach to Hippocampal Function
Levy, W. B. (1989) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/s0079-7421(08)60113-9 · Cited by 228 · see citing works
Potentiation instead of habituation characterizes visual evoked potentials in migraine patients between attacks
Schoenen, J. E., Wang, W., Albert, A., & Delwaide, P. J. (1995) · European Journal of Neurology · doi:10.1111/j.1468-1331.1995.tb00103.x · Cited by 227 · see citing works
ISPAD Clinical Practice Consensus Guidelines 2018: Assessment and management of hypoglycemia in children and adolescents with diabetes
Abraham, M. B., Jones, T. W., Naranjo, D. M., Karges, B., Oduwole, A. O., Tauschmann, M., & Maahs, D. M. (2018) · Pediatric Diabetes · doi:10.1111/pedi.12698 · Cited by 228 · see citing works
“This adaptive process is referred to as habituation.(113) A habituated response can also be, at least temporarily, reversed by the introduction of a novel (heterotypic) stimulus (dishabituation).”
Morphine tolerance as habituation.
Baker, T. B., & Tiffany, S. T. (1985) · Psychological Review · doi:10.1037/0033-295x.92.1.78 · Cited by 223 · see citing works
Plasticity of local GABAergic interneurons drives olfactory habituation
Das, S., Sadanandappa, M. K., Dervan, A., Larkin, A., Lee, J. A., Sudhakaran, I. P., Priya, R., Heidari, R., Holohan, E. E., Pimentel, A., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106411108 · Cited by 219 · see citing works
“In the DM2 glomerulus, two-way ANOVA yielded a significant difference between EB/mock treatments [F(1,82) = 11.”
BackgroundMethodInfluential
Repetition counts: repeated exposure increases intake of a novel vegetable in UK pre-school children compared to flavour–flavour and flavour–nutrient learning
Caton, S. J., Ahern, S., Rémy, É., Nicklaus, S., Blundell-Birtill, P., & Hetherington, M. M. (2012) · British Journal Of Nutrition · doi:10.1017/s0007114512004126 · Cited by 219 · see citing works
“habituation to the neophobic response((27)).”
A Role in Learning for SRF: Deletion in the Adult Forebrain Disrupts LTD and the Formation of an Immediate Memory of a Novel Context
Etkin, A., Alarcón, J. M., Weisberg, S. P., Touzani, K., Huang, Y. Y., Nordheim, A., & Kandel, E. R. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.013 · Cited by 218 · see citing works
“Habituation is thus the behavioral reflection of mnemonic processes and is distinct from response fatigue, can occur over the course of a few minutes, and can be maintained over long periods of time (Thompson and Spencer, 1966; Cheal et al., 1982).”
Background
Cannabinoid CB1 Receptor Mediates Fear Extinction via Habituation-Like Processes
Kamprath, K., Marsicano, G., Tang, J., Monory, K., Bisogno, T., Marzo, V. D., Lutz, B., & Wotjak, C. T. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0153-06.2006 · Cited by 217 · see citing works
“On the other hand, repeated nonreinforced tone presentations may decrease the responsiveness to the tone in the stimulus–response pathways because of habituation-like processes (Thompson and Spencer, 1966; Groves and Thompson, 1970; McSweeney and Swindell, 2002; Kamprath and Wotjak, 2004).”
Background
An Analysis of Dishabituation and Sensitization of The Gill-Withdrawal Reflex In Aplysia
Carew, T. J., Castellucci, V. F., & Kandel, E. R. (1971) · International Journal of Neuroscience · doi:10.3109/00207457109146995 · Cited by 216 · see citing works
Habituation and migraine
Coppola, G., Pierelli, F., & Schoenen, J. E. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.07.006 · Cited by 215 · see citing works
“The latter, once again, tends towards the existence of a relation between stimulus repetition rates and habituation (criteria 4 in Thompson & Spencer, 1966).”
Influential
Identifying hormonal habituation in field studies of stress
Cyr, N. E., & Romero, L. M. (2009) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2009.02.001 · Cited by 210 · see citing works
“Later, Thompson and Spencer (1966) listed nine parametric characteristics of habituation for what they termed the operational definition of habituation.”
Background
LONG-TERM POTENTIATION AND LEARNING
Martinez, J. L., & Derrick, B. E. (1996) · Annual Review of Psychology · doi:10.1146/annurev.psych.47.1.173 · Cited by 215 · see citing works
“Habituation andsensitization were recognizedquite early to be separateprocesses, and dishabituation was viewed as sensitization inducedsimultaneouslywith habituation (Thompson & Spencer 1966).”
Background
Habituation as a determinant of human food intake.
Epstein, L. H., Temple, J. L., Roemmich, J. N., & Bouton, M. E. (2009) · Psychological Review · doi:10.1037/a0015074 · Cited by 210 · see citing works
“Response decrement to repeated stimulus presentation may be due to factors other than habituation, such as receptor or effector fatigue (Thompson & Spencer, 1966; Thorpe, 1966), but the demonstration that a dishabituator can result in recovery of responses to an habituated stimulus is unique to…”
BackgroundMethod
Intensity dependence of auditory evoked potentials is pronounced in migraine
Wang, W., Timsit-Berthier, M., & Schoenen, J. E. (1996) · Neurology · doi:10.1212/wnl.46.5.1404 · Cited by 211 · see citing works
Comorbid Subjective Health Complaints in Low Back Pain
Hagen, E. M., Svensen, E., Eriksen, H. R., Ihlebæk, C., & Ursin, H. (2006) · Spine · doi:10.1097/01.brs.0000219947.71168.08 · Cited by 210 · see citing works
“Sensitization is an increased reactivity to stimuli caused by repeated use.(12) Increased pain sensitivity has been documented to be associated with chronic LBP,(13) fibromyalgia,(14) and functional gastrointestinal complaints.”
Background
Chemical modulation of memory formation in larval zebrafish
Wolman, M. A., Jain, R. A., Liss, L., & Granato, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107156108 · Cited by 198 · see citing works
“Finally, to confirm that SLC response attenuation is indeed learning and not a result of sensory or motor fatigue, we tested whether SLC response attenuation is instantly reversible through cross-modal stimulation (9).”
BackgroundInfluential
Irritable bowel syndrome patients show enhanced modulation of visceral perception by auditory stress
Dickhaus, B., Mayer, E. A., Firooz, N., Stains, J., Conde, F. A., Olivas, T. I., Fass, R., Chang, L., Mayer, M., & Naliboff, B. D. (2003) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2003.07156.x · Cited by 204 · see citing works
Injury-Related Behavior and Neuronal Plasticity: an Evolutionary Perspective on Sensitization, Hyperalgesia, and Analgesia
Walters, E. T. (1994) · International Review of Neurobiology · doi:10.1016/s0074-7742(08)60307-4 · Cited by 206 · see citing works

Authors: Thompson, R. F., & Spencer, W. A.
Affiliations: University of Oregon (US)
Venue: Psychological Review
Publisher: American Psychological Association (APA)
Published: 1966
Volume: 73
Issue: 1
Pages: 16-43
ISSN: 0033-295X (ISSN-L)
1939-1471
DOI: 10.1037/h0022681
OpenAlex: W2055171682
Cited by: 2,608
References: 118
Citations by year: 2026: 75 · 2025: 79 · 2024: 67 · 2023: 76 · 2022: 76 · 2021: 95 · 2020: 80 · 2019: 80 · 2018: 63 · 2017: 58 · 2016: 68 · 2015: 66 · 2014: 64 · 2013: 59 · 2012: 82
FWCI: 22.17
Type: journal article
Language: en
Open access: closed
Locations: Psychological Review (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: habituation, neural basis of learning, psychobiology, associative learning
MeSH terms: Adaptation, Physiological, Animals, Behavior, Humans, Neurophysiology, Psychophysiology

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