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Habituation: a model phenomenon for the study of neuronal substrates of behavior
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“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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Emotional processing of fear: Exposure to corrective information.
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“consistent with the Thompson and Spencer (1966) usage of the term:”
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Emotion elicitation using films
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Habituation: a dual-process theory.
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“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-citationMolecular Biology of Learning: Modulation of Transmitter Release
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Plasticity and Primary Motor Cortex
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“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).”
BackgroundThe Neurobiology of Learning and Memory
Thompson, R. F. (1986) · Science · doi:10.1126/science.3738519 · Cited by 1,164
Self-citationMyers, K. M., & Davis, M. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001939 · Cited by 1,277
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Behavioral studies of Pavlovian conditioning
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“That course can be studied as a function of such primitive variables as stimulus intensity, modality, and spacing (e.g. Thompson & Spencer 1966).”
BackgroundContingent negative variation (CNV) and psychological processes in man
Tecce, J. J. (1972) · Psychological Bulletin · doi:10.1037/h0032177 · Cited by 671
Ward, S. (1973) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.70.3.817 · Cited by 572
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
“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).”
BackgroundMethodInfluentialThe 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 526
Locomotion in larval zebrafish: Influence of time of day, lighting and ethanol
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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 477
Neuroethology of releasing mechanisms: Prey-catching in toads
Ewert, J.-P. (1987) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00023128 · Cited by 463
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
“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 .”
BackgroundUnpredictable 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 457
Startle response models of sensorimotor gating and habituation deficits in schizophrenia
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Thompson, R. F. (1976) · American Psychologist · doi:10.1037//0003-066x.31.3.209 · Cited by 495
Self-citationAlger, B. E., & Teyler, T. J. (1976) · Brain Research · doi:10.1016/0006-8993(76)90858-1 · Cited by 449
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“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-citationState dependent activity in monkey visual cortex
Haenny, P. E., & Schiller, P. H. (1988) · Experimental Brain Research · doi:10.1007/bf00247569 · Cited by 451
“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…”
MethodDynamic systems theory and the complexity of change
Thelen, E. (2005) · Psychoanalytic Dialogues · doi:10.1080/10481881509348831 · Cited by 441
“habituation (Thompson and Spencer, 1966) ensure that infants fill their visual world with changing scenes.”
BackgroundHabituation 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
Differential prefrontal cortex and amygdala habituation to repeatedly presented emotional stimuli
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Impact of Maternal Stress, Depression and Anxiety on Fetal Neurobehavioral Development
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Behavioral functions of the reticular formation
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Anthropogenic noise affects risk assessment and attention: the distracted prey hypothesis
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“As anthropogenic sounds become more frequent, the strength of an animal’s response to them may decrease owing to habituation (Thompson & Spencer 1966).”
BackgroundStartle 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
“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.”
BackgroundCompeting 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
“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).”
BackgroundBassareo, V., & Chiara, G. D. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-02-00851.1997 · Cited by 375
“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.”
BackgroundIs 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 441
Zebrafish Larvae as a Behavioral Model in Neuropharmacology
Basnet, R. M., Zizioli, D., Taweedet, S., Finazzi, D., & Memo, M. (2019) · Biomedicines · doi:10.3390/biomedicines7010023 · Cited by 389
“Habituation is a non-associative form of learning in which a repeated stimulus leads to an attenuated response [58,68].”
BackgroundTIME 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
Inhibitory component of externally controlled covert orienting in visual space.
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A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use
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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
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“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.”
BackgroundInfluentialRiches, I. P., Wilson, F., & Mw, B. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-06-01763.1991 · Cited by 336
“They may therefore be distinguished from those of classical short-term habituation (Thompson and Spencer, 1966).”
BackgroundIs 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 344
Altered processing of sensory stimuli in patients with migraine
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“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.”
BackgroundPathways of the Past: the Imprint of Memory
Horn, G. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1324 · Cited by 308
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
Failure in treating obsessive–compulsives
Foa, E. B. (1979) · Behaviour Research and Therapy · doi:10.1016/0005-7967(79)90031-7 · Cited by 305
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
The smell of danger: A behavioral and neural analysis of predator odor-induced fear
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“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).”
BackgroundInfluentialCodispoti, M., Ferrari, V., & Bradley, M. M. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.4.577 · Cited by 288
“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,…”
BackgroundEffects 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
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
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 278
“However, habituation wanes rapidly with increases in the retention interval (Thompson & Spencer 1966), whereas the CS-preexposure effect does not (Hall & Schachtman 1987).”
BackgroundPhytochemicals and Insect Control: An Antifeedant Approach
Koul, O. (2008) · Critical Reviews in Plant Sciences · doi:10.1080/07352680802053908 · Cited by 275
“Habituation differs from sensory adaptation in its ability to be terminated or reversed immediately by a novel or noxious stimulus (Thompson and Spencer, 1966).”
BackgroundMoral 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 283
Neuroconstructivism - IHow the brain constructs cognition
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Psychic cost of adaptation to an environmental stressor.
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Reduced Neural Habituation in the Amygdala and Social Impairments in Autism Spectrum Disorders
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Neuronal Activity in Medial Frontal Cortex During Learning of Sequential Procedures
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“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
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
“The processes must be working whether the stimuli have rich " cognitive " content or much simpler aversive consequences (Thompson & Spencer, 1966).”
BackgroundQUANTITATIVE 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
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 257
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“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).”
Bilewicz, M., & Soral, W. (2020) · Political Psychology · doi:10.1111/pops.12670 · Cited by 283
Physiological plasticity in auditory cortex: rapid induction by learning.
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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
“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).”
BackgroundResultInfluentialDetecting 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 270
“This concurs with the phenomenon of habituation, describing the reduction of the physiological responses elicited by repeated exposure to a monotypic stressor [80].”
BackgroundPitman, D. L., Ottenweller, J. E., & Natelson, B. H. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90097-2 · Cited by 295
Vestibulospinal and Reticulospinal Systems
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Mechanisms underlying spontaneous recovery in autoshaping.
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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 243
“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].”
BackgroundPace-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
“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
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 232
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“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
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
“In the DM2 glomerulus, two-way ANOVA yielded a significant difference between EB/mock treatments [F(1,82) = 11.”
BackgroundMethodInfluentialCaton, 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 228
“habituation to the neophobic response((27)).”
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 224
“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).”
BackgroundCannabinoid 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
“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).”
BackgroundAn 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
Coppola, G., Pierelli, F., & Schoenen, J. E. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.07.006 · Cited by 218
“The latter, once again, tends towards the existence of a relation between stimulus repetition rates and habituation (criteria 4 in Thompson & Spencer, 1966).”
InfluentialIdentifying 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 225
“Later, Thompson and Spencer (1966) listed nine parametric characteristics of habituation for what they termed the operational definition of habituation.”
BackgroundLONG-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 219
“Habituation andsensitization were recognizedquite early to be separateprocesses, and dishabituation was viewed as sensitization inducedsimultaneouslywith habituation (Thompson & Spencer 1966).”
BackgroundHabituation 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 223
“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…”
BackgroundMethodIntensity 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
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
“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.”
BackgroundChemical 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 203
“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).”
BackgroundInfluentialIrritable 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
Walters, E. T. (1994) · International Review of Neurobiology · doi:10.1016/s0074-7742(08)60307-4 · Cited by 206
Metadata
- Authors
- Thompson, R. F., & Spencer, W. A.
- Affiliations
- University of Oregon (US)
- Venue
- Psychological Review
- Published
- 1966
- Volume
- 73
- Issue
- 1
- Pages
- 16-43
- ISSN
- 0033-295X (ISSN-L)
- 1939-1471
- 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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