Characterizing operant hyperactivity in the Spontaneously Hypertensive Rat.
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Background: Operant hyperactivity, the emission of reinforced responses at an inordinately high rate, has been reported in children with ADHD and in the Spontaneously Hypertensive Rat (SHR), the most widely studied animal model of ADHD. The SHR emits behavior at hyperactive levels, relative to a normoactive strain, only when such behavior is seldom reinforced. Because of its dependence on rate of reinforcement, operant hyperactivity appears to be driven primarily by incentive motivation, not motoric capacity. This claim was evaluated in the present study using a novel strategy, based on the organization of behavior in bouts of reinforced responses separated by pauses. Method: Male SHR, Wistar-Kyoto (WKY) and Wistar rats (WIS) were exposed each to a multiple variable-interval schedule of sucrose reinforcement (12, 24, 48, 96, and 192 s) between post-natal days (PND) 48 and 93. Responding in each schedule was examined in two epochs, PND 58-62 and 89-93. Parameters of response-reinforcement functions (Herrnstein's hyperbola) and bout-organized behavior were estimated in each epoch. Results: SHR emitted higher response rates than WKY and WIS, but only when rate of reinforcement was low (fewer than 2 reinforcers per minute), and particularly in the second epoch. Estimates of Herrnstein's hyperbola parameters suggested the primacy of motivational over motoric factors driving the response-rate differential. Across epochs and schedules, a more detailed analysis of response bouts by SHR revealed that these were shorter than those by WKY, but more frequent than those by WKY and WIS. Differences in bout length subsided between epochs, but differences in bout-initiation rate were exacerbated. These results were interpreted in light of robust evidence linking changes in bout-organization parameters and experimental manipulations of motivation and response-reinforcement contingency. Conclusions: Operant hyperactivity in SHR was confirmed. Although incentive motivation appears to play an important role in operant hyperactivity and motoric capacity cannot be ruled out as a factor, response-bout patterns suggest that operant hyperactivity is primarily driven by steeper delay-of-reinforcement gradients. Convergence of this conclusion with theoretical accounts of ADHD and with free-operant performance in children with ADHD supports the use of SHR as an animal model of ADHD.
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The findings of SHR operant and motor hyperactivity replicate previous research evaluating the use of the SHR strain as a model of ADHD.
“These findings of SHR operant and motor hyperactivity replicate previous research evaluating the use of the SHR strain as a model of ADHD (Wultz et al., 1990; Hill et al., 2012).”
From The Effects of Methylphenidate on Goal-directed Behavior in a Rat Model of ADHD (2015) · cites this paper as Hill et al., 2012
The Discussion reports that SHR operant hyperactivity replicated prior findings in adult rats, and the Conclusions say the results support using SHR as an ADHD model. The paper does not establish motor hyperactivity as a separate replicated finding: the Discussion treats elevated motoric capacity as a possible contributor that cannot be ruled out, while the Background says evidence for spontaneous hyperactivity is mixed. (LLM, conf=0.86)
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FARAONE, S. V., BIEDERMAN, J., & MICK, E. (2006) · Psychological Medicine · doi:10.1017/s003329170500471x · Cited by 2,267 · see citing works
Barkley, R. A. (1997) · Psychological Bulletin · doi:10.1037//0033-2909.121.1.65 · Cited by 580 · see citing works
Rodent Models of Attention-Deficit/Hyperactivity Disorder
Sagvolden, T., Russell, V. A., Aase, H., Johansen, E. B., & Farshbaf, M. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.02.002 · Cited by 448 · see citing works
Altered reinforcement mechanisms in attention-deficit/hyperactivity disorder
Sagvolden, T., Aase, H., Zeiner, P., & Berger, D. (1998) · Behavioural Brain Research · doi:10.1016/s0166-4328(97)00170-8 · Cited by 345 · see citing works
Luman, M., Tripp, G., & Scheres, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.11.021 · Cited by 335 · cited 1× · see citing works
“The characterization of ADHD in terms of steeper delay-of-reinforcement gradients is a core assumption of the dynamic developmental theory of ADHD [38,75,76].”
BackgroundAase, H., & Sagvolden, T. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2005.01468.x · Cited by 92 · see citing works
Johansen, E. B., Killeen, P. R., & Sagvolden, T. (2007) · Behavioral and Brain Functions · doi:10.1186/1744-9081-3-60 · Cited by 56 · see citing works
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Research works printed but not linked: 67
- Froehlich T Lanphear BP Epstein JN Barbaresi WJ Katusic SK Kahn RS Prevalence, recognition, and treatment of attention-deficit/hyperactivity disorder in a national sample of US children Arch Pediatr Adolesc Med 2007 161 9 857 864 10.1001/archpedi.161.9.857 17768285 · DOI
- Polanczyk G de Lima Horta B Biederman J Rohde L The worldwide prevalence of ADHD: a systematic review and metaregression analysis Am J Psychiatry 2007 164 942 948 10.1176/appi.ajp.164.6.942 17541055 · DOI · Paper page
- Kessler RC Adler L Barkley R Biederman J Conners K Demler O Faraone SV Greenhill LL Howes MJ Secnik K Spencer T Ustun TB Walters EE Zaslavsky AM The prevalence and correlates of adult ADHD in the United States: results from the national comorbidity survey replication Am J Psychiatry 2006 163 716 723 10.1176/appi.ajp.163.4.716 16585449 PMC2859678 · DOI · Paper page
- Faraone SV Sergeant J Gillberg C Biederman J The worldwide prevalence of ADHD: is it an American condition? World Psychiatry 2003 2 2 104 113 16946911 PMC1525089
- Barry TD Lyman RD Klinger LG Academic under-achievement and attention-deficit/hyperactivity disorder: the negative impact of symptom severity on school performance J School Pscyhol 2002 40 3 259 283 10.1016/S0022-4405(02)00100-0 · DOI · Paper page
- Spira EG Fischel JE The impact of preschool inattention, hyperactivity, and impulsivity on social and academic development: a review J Child Psychol Psych 2005 46 755 773 10.1111/j.1469-7610.2005.01466.x 15972069 · DOI
- Loe IM Feldmen HM Academic and educational outcomes of children with ADHD Ambul Pediatr 2007 7 1 82 90 10.1016/j.ambp.2006.05.005 17261487 · DOI · Paper page
- Russell V Neurobiology of animal models of attention-deficit hyperactivity disorder J Neurosci Methods 2007 161 185 198 10.1016/j.jneumeth.2006.12.005 17275916 · DOI
- Bari A Robbins TW Animal models of ADHD Molecular and Functional Models in Neuropsychiatry: Curr Top Behav Neurosci 2011 7 149 185 10.1007/7854_2010_102 21287324 · DOI
- Sanabria F Killeen PR Evidence for impulsivity in the Spontaneously Hypertensive Rat drawn from complementary response-withholding tasks Behav Brain Funct 2008 4 7 24 10.1186/1744-9081-4-7 18261220 PMC2276225 · DOI
- Fox AT Hand DJ Reilly MP Impulsive choice in a rodent model of attention-deficit/hyperactivity disorder Behav Brain Res 2008 187 146 152 10.1016/j.bbr.2007.09.008 17950930 · DOI
- Evenden J Meyerson B The behavior of Spontaneously Hypertensive and Wistar Kyoto rats under a paced fixed consecutive number schedule of reinforcement Pharmacol Biochem Behav 1999 63 71 82 10.1016/S0091-3057(98)00222-6 10340526 · DOI
- Berger DF Sagvolden T Sex differences in visual discrimination behaviour in an animal model of attention deficit hyperactivity disorder Behav Brain Res 1998 94 73 82 10.1016/S0166-4328(97)00171-X 9708841 · DOI
- Sagvolden T Behavioral validation of the spontaneously hypertensive rat (SHR) as an animal model of attention-deficit/hyperactivity disorder (AD/HD) Neurosci Biobehav Rev 2000 24 31 39 10.1016/S0149-7634(99)00058-5 10654658 · DOI · Paper page
- Alsop B Problems with spontaneously hypertensive rats (SHR) as a model of attention-deficit/hyperactivity disorder (AD/HD) J Neurosci Methods 2007 162 42 48 10.1016/j.jneumeth.2006.12.002 17241669 · DOI
- van den Bergh FS Bloemarts E Chan JSW Groenink L Olivier B Oosting RS Spontaneously hypertensive rats do not predict symptoms of attention-deficit hyperactivity disorder Pharmacol Biochem Behav 2006 83 380 390 10.1016/j.pbb.2006.02.018 16580713 · DOI
- Paulus M Geyer M Three independent factors characterize spontaneous rat motor activity Behav Brain Res 1993 53 11 20 10.1016/S0166-4328(05)80262-1 8466655 · DOI
- Hsieh Y Yang C Age-series characteristics of locomotor activities in spontaneously hypertensive rats: a comparison with the Wistar-Kyoto strain Physiol Behav 2008 93 777 782 10.1016/j.physbeh.2007.11.032 18155738 · DOI
- Knardah S Sagvolden T Open-field behavior of spontaneously-hypertensive rats Behav Neural Biol 1979 27 187 200 10.1016/S0163-1047(79)91801-6 508216 · DOI · Paper page
- Gentsch C Lichtsteiner M Feer H Open field and elevated plus-maze: A behavioral comparison between spontaneously hypertensive (SHR) and Wistar-Kyoto (WKY) rats and the effects of chlordiazepoxide Behav Brain Res 1987 25 101 107 10.1016/0166-4328(87)90003-9 3675823 · DOI
- Sagvolden T Hendley ED Knardahl S Behavior of hypertensive and hyperactive rat strains: hyperactivity is not unitarily determined Physiol Behav 1992 52 49 57 10.1016/0031-9384(92)90432-2 1529013 · DOI
- Myers M Musty R Hendley E Attenuation of hyperactivity in the spontaneously hypertensive rat by amphetamine Behav Neural Biol 1982 34 42 54 10.1016/S0163-1047(82)91397-8 7073635 · DOI
- Danysz W Plaźnik A Pucilowski O Plewako M Obersztyn M Kostowski W Behavioral studies in spontaneously hypertensive rats Behav Neural Biol 1983 39 22 29 10.1016/S0163-1047(83)90569-1 6686441 · DOI
- Cierpial M M McCarty R Maternal effects on the development of spontaneous hypertension Health Psychol 1988 7 125 135 3371305
- Ferguson S Cada A A longitudinal study of short- and long-term activity levels in male and female spontaneously hypertensive, Wistar-Kyoto, and Sprague-Dawley rats Behav Neurosci 2003 117 271 282 12708524
- Amini B Swann A Dafny N Differential locomotor responses in male rats from three strains to acute methylphenidate Int J Neurosci 2004 114 1063 1084 10.1080/00207450490475526 15370174 · DOI
- Sagvolden T Pettersen M Larsen M Spontaneously hypertensive rates (SHR) as a putative animal model of childhood hyperkinesis: SHR behavior compared to four other rat strains Physiol Behav 1993 54 6 1047 1055 10.1016/0031-9384(93)90323-8 8295939 · DOI · Paper page
- Sagvolden T Metzger MA Sagvolden G Frequent rewards eliminates differences in activity between hyperkinetic rats and controls Behav Neurol Biol 1993 59 225 229 10.1016/0163-1047(93)90986-R 8503827 · DOI
- Williams J Sagvolden G Taylor E Sagvolden T Dynamic behavioral changes in the Spontaneously Hypertensive Rat 1. Control by place, timing, and reinforcement rate Behav Brain Res 2009 198 273 282 10.1016/j.bbr.2008.08.044 18824036 · DOI
- Johansen E Sagvolden S Kvande G Effects of delayed reinforcers on the behavior of an animal model of attention-deficit/hyperactivity disorder (ADHD) Behav Brain Res 2005 162 1 47 61 10.1016/j.bbr.2005.02.034 15922066 · DOI
- Sagvolden T Aase H Zeiner P Berger DF Altered reinforcement mechanisms in ADHD Behav Brain Res 1998 33 387 398 9708840
- Douglas V Parry P Effects of reward on delayed reaction time task performance in hyperactive children J Abnorm Child Psych 1983 11 313 326 10.1007/BF00912094 6619440 · DOI
- Sagvolden T Johansen EB Aase H Russell VA A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes Behav Brain Sci 2005 28 397 419 16209748
- Herrnstein RJ On the law of effect J Exp Anal Behav 1970 13 2 243 266 10.1901/jeab.1970.13-243 16811440 PMC1333768 · DOI · Paper page
- Blough DS Interresponse time as a function of continuous variables: a new method and some data J Exp Anal Behav 1963 6 237 246 10.1901/jeab.1963.6-237 16811278 PMC1404277 · DOI
- Shull RL Gaynor ST Grimes JA Response rate viewed as engagement bouts: effects of relative reinforcement and schedule type J Exp Anal Behav 2001 75 247 274 10.1901/jeab.2001.75-247 11453618 PMC1284817 · DOI
- Shull RL Grimes JA Bennett JA Bouts of responding: the relation between bout rate and the rate of variable-interval reinforcement J Exp Anal Behav 2004 81 65 83 10.1901/jeab.2004.81-65 15113134 PMC1284972 · DOI
- Shull RL Grimes JA Bouts of responding from variable-interval reinforcement of lever pressing by rats J Exp Anal Behav 2003 80 159 171 10.1901/jeab.2003.80-159 14674726 PMC1284951 · DOI
- Brackney RJ Cheung TH Neisewander JL Sanabria F The isolation of motivational, motoric, and schedule effects on operant performance: a modeling approach J Exp Anal Behav 2011 37 1 9 PMC3136892 21765544
- Reed P An experimental analysis of steady-state response rate components on variable ratio and variable interval schedules of reinforcement J Exp Psychol [Anim Behav] 2011 39 27 35 20718555
- Conover KL Fulton S Shizgal P Operant tempo varies with reinforcement rate: implications for measurement of reward efficacy Behav Process 2001 56 85 101 10.1016/S0376-6357(01)00190-5 11672935 · DOI
- Sagvolden T Johansen E Woien G Walaas SI Storm-Mathisen J Bergerson LH Hvalby O Jensen V Aase H Russell V Killeen PR DasBanerjee T Middleton F Faraone SV The spontaneously hypertensive rat model of ADHD- The importance of selecting the appropriate reference strain Neuropharmacology 2009 57 619 626 10.1016/j.neuropharm.2009.08.004 19698722 PMC2783904 · DOI
- Fleshler M Hoffman HS A progression for generating variable-interval schedules J Exp Anal Behav 1962 5 529 530 10.1901/jeab.1962.5-529 13945507 PMC1404199 · DOI
- Spear LP Brake SC Periadolescence: Age-dependent behavior and pyschopharmacological responsivity in rats Dev Psychobiol 2009 16 83 111 6339302
- Herrnstein RJ Relative and absolute strength of responses as a function of frequency of reinforcement J Exp Anal Behav 1961 4 267 272 10.1901/jeab.1961.4-267 13713775 PMC1404074 · DOI · Paper page
- Shull RL The sensitivity of response rate to the rate of variable-interval reinforcement for pigeons and rats: a review J Exp Anal Behav 2005 84 99 110 10.1901/jeab.2005.03-05 16156139 PMC1243899 · DOI
- Fantino E Davison M Choice: some quantitative relations J Exp Anal Behav 1983 40 1 1 13 10.1901/jeab.1983.40-1 16812333 PMC1347840 · DOI
- Bradshaw CM Ruddle HV Szabadi E Relationship between response rate reinforcement frequency in variable-interval schedules: III. the effect of d-amphetamine J Exp Anal Behav 1981 36 1 29 39 10.1901/jeab.1981.36-29 7241036 PMC1333050 · DOI
- Martens BK Lochner DG Kelly SQ The effects of variable interval reinforcement on academic engagement: a demonstration of matching theory J Exp Anal Behav 1992 25 1 143 151 PMC1279662 1582963
- Dallery J Soto PL Herrnstein's hyperbolic matching equation and behavioral pharmacology: review and critique Behav Pharmacol 2004 15 443 459 10.1097/00008877-200411000-00001 15472567 · DOI
- Burnham KP Anderson DR Model selection and multimodel inference: A practical information-theoretic approach 2002 New York NY, Springer-Verlag
- Myung I Tutorial on maximum likelihood estimation J Math Psychol 2003 47 90 100 10.1016/S0022-2496(02)00028-7 · DOI · Paper page
- Bowers MT Hill J Palya WL Interresponse time structures in variable-ration and variable-interval schedules J Exp Anal Behav 2008 90 345 362 10.1901/jeab.2008.90-345 19070341 PMC2582208 · DOI
- Johnson JE Pese EF Newland MC High-rate operant behavior in two mouse strains: a response-bout analysis Behav Process 2009 81 309 315 10.1016/j.beproc.2009.02.013 19429225 · DOI
- Podlesnik CA Jimenez-Gomez C Ward RD Shahan TA Resistance to change of responding maintained by unsignaled delays to reinforcement: a response-bout analysis J Exp Anal Behav 2006 85 329 347 10.1901/jeab.2006.47-05 16776055 PMC1459851 · DOI
- Sidman M Stebbins WC Satiation effects under fixed-ratio schedules of reinforcement J Comp Physiol Psychol 1954 47 114 116 13152223
- Killeen P Reinforcement frequency and contingency as factors in fixed-ratio behavior J Exp Anal Behav 1969 12 3 391 395 10.1901/jeab.1969.12-391 16811362 PMC1338599 · DOI
- Killeen PR Fantino E Unification of models for choice between delayed reinforcers J Exp Anal Behav 1990 53 1 189 200 10.1901/jeab.1990.53-189 2299288 PMC1323034 · DOI
- Killeen PR Models of trace decay, eligibility for reinforcement, and delay of reinforcement gradients, from exponential to hyperboloid Behav Process 2011 87 57 63 10.1016/j.beproc.2010.12.016 21215304 · DOI
- Lattal KA Delayed reinforcement of operant behavior J Exp Anal Behav 2010 93 129 139 10.1901/jeab.2010.93-129 20676272 PMC2801538 · DOI
- Hand DJ Fox AT Reilly MP Response acquisition with delayed reinforcement in a rodent model of attention-deficit/hyperactivity disorder (ADHD) Behav Brain Res 2006 175 337 342 10.1016/j.bbr.2006.09.001 17034874 · DOI
- Johansen EB Sagvolden T Slower extinction of responses maintained by intra-cranial self-stimulation (ICSS) in an animal model of attention-deficit/hyperactivity disorder (ADHD) Behav Brain Res 2005 162 22 31 10.1016/j.bbr.2005.02.035 15922064 · DOI
- Sutherland KR Alsop B McNaughton N Hyland BI Tripp G Wickens JR Sensitivity to delay of reinforcement in two animal models of attention deficit hyperactivity disorder (ADHD) Behav Brain Res 2009 205 372 376 10.1016/j.bbr.2009.07.011 19616039 · DOI
- Johansen EB Killeen PR Russell VA Tripp G Wickens JR Tannock R Williams J Sagvolden T Origins of altered reinforcement effects in ADHD Behav Brain Funct 2009 5 7 10.1186/1744-9081-5-7 19226460 PMC2649942 · DOI · Paper page
- Taylor D Lincoln AJ Foster SL Impaired behavior regulation under conditions of concurrent variable schedules of reinforcement in children with ADHD J Attention Disord 2010 13 358 368 10.1177/1087054708329974 19520999 · DOI
- Hart EL Lahey BB Loeber R Applegate B Green SM Frick PJ Developmental change in attention-deficit hyperactivity disorder in boys: a four-year longitudinal study J Abnorm Child Psych 1995 23 729 749 10.1007/BF01447474 8609310 · DOI · Paper page
- Faraone SV Biederman J What is the prevalence of adult ADHD? Results of a population screen of 966 adults J Attention Disord 2005 9 384-391 16371661
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Delisle, J., & Braun, C. M. J. (2011) · Archives of Clinical Neuropsychology · doi:10.1093/arclin/acr043 · Cited by 49 · see citing works
The Effects of Methylphenidate on Goal-directed Behavior in a Rat Model of ADHD
Natsheh, J. Y., & Shiflett, M. W. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00326 · Cited by 21 · see citing works
- Authors
- Hill, J. C., Herbst, K., & Sanabria, F.
- Affiliations
- Arizona State University (US)
- Corresponding author
- Sanabria, Federico
- ORCID
- Sanabria, Federico
- Venue
- Behavioral and Brain Functions
- Published
- 2012-01-26
- Volume
- 8
- Issue
- 1
- Pages
- 5-5
- ISSN
- 1744-9081 (ISSN-L)
- PMC
- PMC3292830
- OpenAlex
- W2130187545
- Cited by
- 41
- References
- 7
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 2 · 2022: 1 · 2020: 1 · 2019: 2 · 2018: 3 · 2017: 4 · 2016: 6 · 2015: 6 · 2014: 4 · 2013: 2 · 2012: 5
- FWCI
- 3.68
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Behavioral and Brain Functions (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Arizona State University Library Digital Repository (Arizona State University) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Arizona State University
- College of Liberal Arts and Sciences, Arizona State University
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Attention Deficit Hyperactivity Disorder
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Social Sciences › Psychology › Developmental and Educational Psychology › Behavioral and Psychological Studies
- Keywords
- spontaneously hypertensive rats, animal model of ADHD, incentive motivation, delayed reinforcement, sucrose reinforcement, Wistar-Kyoto rats, Wistar rats
- MeSH terms
- Aging, Algorithms, Animals, Conditioning, Operant, Hyperkinesis, Male, Psychomotor Performance, Rats, Inbred SHR, Rats, Inbred WKY, Reinforcement Schedule, Rats
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