An Analysis of Excessive Running in the Development of Activity Anorexia

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1 Pergamon (95)83-6 Physology & Behavor, Vol. 58, No. 3, pp , 1995 Copyrght 1995 Elsever Scence Ltd Prnted n the USA. All rghts reserved /95 $ An Analyss of Excessve Runnng n the Development of Actvty Anorexa WLLAM M. BENEKE, ~ SHARON E. SCHULTE AND JERRY G. VANDER TUG Human Nutrton Research Program, Lncoln Unversty of Mssour, Jefferson Cty, MO USA, E-Mal: wbeneke@mal.con.mssour.edu Receved 29 December 1993 BENEKE, W. M., S. E. SCHULTE AND J. G. VANDER TUG. An analyss of excessve runnng n the development of actvty anorexa. PHYSOL BEHAV 58(3) , Food restrcton combned wth actvty wheel access produces actvty anorexa: a combnaton of excessve runnng, reduced food ntake and rapd weght loss. Temporal dstrbutons of runnng n actvty anorexa were examned n a reversal desgn wth one of factoral combnatons (pelleted-vs-powdered food deprvaton wheel access) as the treatment condton. Wheel revolutons were recorded n 3 mn ntervals; body weghts, food and water ntakes were measured daly. Only wheel access combned wth food deprvaton relably produced actvty anorexa. Excessve runnng occurred n the absence of schedule-nduced polydpsa, was unaffected by food form, and showed dstrbutonal characterstcs of facultatve behavor. These results are nconsstent wth schedule-nduced behavor explanatons. Runnng dstrbutons appeared consstent wth chronobologcal models wth lght/dark onset and feedng servng as zetgebers. Actvty anorexa Actvty Temporal runnng dstrbuton Food deprvaton Schedule-nduced behavor Rats RATS (8,13,2,21), mce (8), and golden hamsters (4,5) allowed access to runnng wheels combned wth food deprvaton schedules (6-9 mn daly food access), ran excessvely, ate lttle and eventually starved. The phenomenon, labelled actvty anorexa (7), s characterzed by dramatc ncreases n actvty paradoxcally assocated wth decreased food consumpton, and has also been observed n some humans dagnosed wth anorexa nervosa (1,15,27) as well as some athletes (14,23,26,28). These observatons have led researchers (7,9) to suggest that actvty anorexa, nduced expermentally n rodents, mght serve as a useful model for the understandng of anorexa nervosa and ts treatment n humans. Consstent wth ths noton, Eplng and Perce (7) also observed dramatc ncreases n runnng mmedately before and after scheduled feedng. They suggested that the runnng mght be a schedule-nduced behavor. f water s contnuously avalable durng a varable nterval schedule of food renforcement, rats become polydpsc, drnkng several tmes ther normal daly water ntake (11). The behavor typcally manfests tself as an nterm schedule-nduced behavor, as descrbed by Staddon (24), and has also been obtaned wth fxed tme schedules of renforcement [e.g., (25)]. f one were to postulate water avalablty as somewhat analogous to avalablty of a runnng wheel, then one could also postulate the excessve wheel runnng as schedulenduced under the same condtons that produce schedule-nduced polydpsa (17,25). Although studes of schedule-nduced behavor have utlzed small food portons as renforcers and bref (commonly 1 mn) perodc schedules, at least by analogy, actvty anorexa mght be a specal case of schedule-nduced behavor, or the behavors mght share common underlyng mechansms. f true, varables nfluencng schedule-nduced behavors parametrcally should also have parametrc effects on actvty anorexa. One such parametrc effect mght offer an opportunty to explore the relatonshp between schedule-nduced behavor and actvty anorexa. Beck, et al. (3) recently demonstrated that changng from a pellet to a powder renforcer elmnated a broad spectrum of schedule-nduced behavors n rats, ncludng feeder pokng, rearng, runnng and nvestgatng. f there s a common lnk between schedule-nduced behavor and excessve runnng observed n the exercse-nduced anorexa paradgm, then food restrcton, combned wth access to a runnng wheel should produce excessve runnng and anorexa when the avalable food s n pellet form but not n powder form. The present study was desgned to examne the effect of pellet vs. powder food on actvty anorexa. n ths context we also set out to carefully descrbe changes n the daly pattern of wheelrunnng durng the development of actvty anorexa. Subjects METHOD Subjects were 84 male Sprague-Dawley rats (SASCO, Omaha, NE), 5-6 days old and weghng g at the To whom requests for reprnts should be addressed. 451

2 452 BENEKE, SCHULTE AND VANDER TUG TABLE 1 NUMBERS OF SUBJECTS N EACH TREATMENT CONDTON REACHNG CRTERA AND MEDAN DAYS TO SELF-STARVATON AND SURVVAL CRTERA Numbers Reachng Crtera Medan Days To Crtera Treatment Group n Self-Starved Survved Self-Starved Survved Pelleted Powdered Pelleted-Wheel Powdered-Wheel Pelleted-Deprved Powdered-Deprved Pelleted-Wheel-Deprved Powdered-Wheel-Deprved start of the study. The rats were housed ndvdually wth unlmted access to water throughout the study. Rats were mantaned on a photo perod of 12/12 h wth the lghts comng on each mornng at 63 h. Apparatus We used standard Wahmann actvty wheels (1.125 meters n crcumference) equpped wth sde cages and sldng doors that could be closed to prevent access to the runnng wheel. The actvty wheels were wred to electronc recordng equpment located n an adjacent room whch recorded wheel revolutons. One wheel revoluton was recorded when a rat made a complete revoluton n ether drecton. Procedure We ran the experment n four phases, wth rats randomly assgned to one of four condtons on a weght matched bass n each phase. The condtons were 2 2 factoral combnatons of wheel access/no wheel access, and food deprvaton/no deprvaton. n phases one and four, rats were fed a pelleted det. n phases two and three, rats were fed a powdered det. Thus, phases one and two combned represent the frst replcaton of a factoral desgn (wheel access deprvaton food type) and phases three and four represent a second replcaton. We recognzed that ths approach confounded food type sequence wth replcaton, but the counterbalanced order of pelleted and powdered det enabled systematc sequental effects to be detected as a sgnfcant dfference between the frst and second replcatons or a sgnfcant nteracton nvolvng replcatons. The basc procedure conssted of perods for baselne, treatment and recovery. Body weght to the nearest gram, and food and water ntakes to the nearest. 1 g were recorded daly n all perods. Rats n the pelleted food condton were fed standard Purna Lab Chow throughout the experment. Lab chow from the same lot was ground to a fne powder and fed to subjects n the powder condton throughout. The remanng varables were effectve only durng the treatment phase. Baselne perod. Rats had unlmted access to food n ther home cages. Weght and ntake measurements were begun at 9 h. Treatment perod. Rats wth wheel access (W) were housed n actvty wheels n a room separate from, but dentcal to that of the other rats. When deprved (D), rats were mantaned wthout food for 23 h daly and wth food contnuously from 1 h to 11 h. ntake for deprved rats was obtaned by weghng food cups before and after meal perods. Food ntake for the other rats was obtaned by weghng the food cups at the same tme each day and subtractng the postfeedng weght from the prefeedng weght. Care was taken to retreve any spllage so as not to nclude spllage wth ntake. Water ntake was obtaned for all rats n the same manner. Access to the wheel was prevented by closng the door between the wheel and sde cage durng the meal perod and durng the daly care performed n the precedng hour. Rats remaned n the treatment untl they ether self-starved or survved. Self-starvaton for a rat was defned as a 25% weght loss from ts average weght over the last three days of baselne. Survval was defned as a day-four weght of any four day perod that was greater than the day-one weght of the same four day perod--for example, a day 5 weght greater than day 2 weght or day 7 weght greater than day 4 weght. Ths procedure was followed n the frst three phases of the study. n phase four, each W rat was yoked to a WD rat so that the nondeprved rat remaned n treatment untl ts yoked partner reached one of the crtera. Ths change was made to elmnate the possblty that observed dfferences n amount of actvty between the wheel/deprvaton rats and the wheel/no deprvaton rats were due smply to number of days of exposure to the actvty wheel. Statstcal comparsons between replcatons utlzed the four days pror to reachng ndvdual crtera for these rats, removng any possble effect of the procedural change from the statstcal analyss. Recovery perod. When rats reached one of the crtera they were placed nto a recovery perod. Ths perod was equvalent to the baselne perod wth food and water contnuously avalable and anmal care begun at 9 h. RESULTS Two pellet-wd rats were elmnated from the study. One was elmnated because of an njured forepaw that mght have affected runnng, and the other because a handlng error mght have affected data. No effects nvolvng replcaton were observed (p >.5) for self-starvaton/survval rates, food ntake, or body weght. Analyss of runnng for the 38 W and WD rats performed on the mean hourly runnng of each rat over ts last 4 days of treatment also showed no replcaton effects (p >.5). We therefore collapsed all data across replcatons for subsequent analyses.

3 ACTVTY ANOREXA 453 c- t3~ ~ Baselne Deprvaton Recovery &- ~ ~.~ Rat # Baselne Deprvaton ' A" J -- Recovery ~.~.~.~ Rat #75 c O '1.. '. : " " ; 1 " , 3 r o t : :,. _ ~ ~ ' ' Days J "", Rat, #74, J 2 1 " "_1 : O Days FG. 1. Body weghts, food and water ntake durng baselne, treatment and recovery perods for two typcal survvng rats and two rats reachng self-starvaton crtera n the deprvaton only condtons. Water ntake s shown as flled crcles and food ntake as open crcles. ncdence of Self-Starvaton Table 1 shows the ncdence of self-starvaton and survval n each of the eght treatment combnatons. Maxmum lkelhood analyss of varance was performed on self-starvaton and survval rates usng the SAS Categorcal Data Modelng procedure (22). Ths analyss ndcated that food type had no effect on selfstarvaton/survval rates (p >.5); all nteractons nvolvng food type were also nonsgnfcant (p >.5). Sgnfcant man effects were observed for both wheel access, X 2 (1) = p <.12, and deprvaton, X 2 (1) = p <.1. The wheel access deprvaton nteracton was also sgnfcant, X 2 (1) = p <.29. Wheel access dd not affect the ncdence of self-starvaton n rats who were not food restrcted: all of these rats contnued to gan weght durng the treatment phase and met the crtera for survval n the mnmum possble perod of four days. Self-starvaton developed n four of the 2 deprvaton-only (D) rats, and 14 of 18 wheel + deprvaton (WD) rats. Separate

4 454 BENEKE, SCHULTE AND VANDER TUG 3 (/) 25 2 W WD-Anorexc WD-survved 3 Z ~W ~WO-Anorexc ~lwd-survved 15..d > ee 3 -J Ld Ld "r 1 5 >;,,,( C3 _.1,,( TME [3 rnn bns] FG. 2. Dstrbutons of wheel revolutons n consecutve 3 mn perods. Because of substantal dfferences n runnng between survvng and anorexc rats, the four survvng WD rats were plotted separately; due to ther small n, standard errors are not shown. Plotted data are based on means from the last 4 days for each rat, averaged across rats n each groupng. Feedng and anmal care preceded perod begnnng at 11 h and shown as total at 113 h. Lghts were off from 183 to 63 h, shown as totals from 19 h to 6:3 h. Mean daly totals for the same groups. analyss of self-starvaton/survval rates n those groups experencng food restrcton ndcated that wheel access sgnfcantly ncreased the lkelhood of self-starvaton, X 2 (1) = p <.1. Development of Self-Starvaton~Survval Sxteen of the 2 D rats showed a pattern of gradually ncreasng food ntake accompaned by deceleraton of weght loss, wth weght stablzng at 82.5% +- 1.% (mean _+ SEM ) of weght at end of baselne. ndvdual data from two typcal rats (Fg. la) shows the same pattern. Food ntake decreased ntally, then gradually ncreased; body weght also dropped ntally and then stablzed. The four self-starvng rats (Fg. lb) showed a sharp ntal declne n food ntake followed by a gradual ncrease n daly ntake. Although food ntake gradually ncreased and weght loss slowed, the rats reached the 75% ad lb weght crtera for selfstarvaton before ther weght stablzed. The WD combnaton resulted n self-starvaton n 14 of 18 rats. Self-starvng rats completed revolutons (mean +_ SEM), more than four tmes the mean of 736 +_ 126 revolutons completed daly by W rats (Fg. 2). The four survvng WD rats ran very lttle; ther average daly wheel revolutons was slghtly less than comparable data for the W rats who survved. At the begnnng of the treatment perods food ntake decreased and then began to gradually ncrease for self-starvng WD rats. ntally lttle runnng was observed, and gradual weght loss contnued (Fgs. 3 and 4). Ths appears smlar to the pattern of D rats (see Fg. 1). As runnng began to accelerate above 5, revolutons/day, food ntakes declned. The combned effects of reduced ntake and the energy cost of runnng accounts for ncreased weght loss untl rats reached the self-starvaton crtera. Once rats were returned to baselne, food and water ntakes and body weght ncreased rapdly. Water ntake Group data dd not reveal dramatc ncreases assocated wth excessve runnng. The 13.2 g daly average water consumpton durng treatment for all deprved rats was actually less than the 25.6 g average for all nondeprved rats, F(1, 67) = 58.23, p <.1. Ths also represented a substantal reducton from baselne daly water consumpton of 27.9 g n the rats experencng deprvaton. ndvdual data (Fgs. 3 and 4) also dd not ndcate dramatc ncreases above baselne n water consumpton when relatvely large runnng ncreases were occurrng. To stattcally adjust water ntake for reduced food consumpton, we calculated the regresson equaton to predct water ntake from food ntake usng mean treatment food and water consumpton for each nondeprved rat n the study. We appled that equaton to predct water consumpton durng treatment for deprved rats, and statstcally removed the effect of food restrcton by calculatng resdual consumpton (obtaned-predcted) for each rat. Subse-

5 ACTVTY ANOREXA 455 Baselne Treatment Recovery 3,,,, ~ 25 ~= 2 next anmal care/feedng. These ncreases were also observed n runnng dstrbutons of self-starvng rats who, unlke ther survvng counterparts, also ran excessvely from around 123 h and through the remander of the lght perod. Perods of mnmal runnng (pror to 123 h and between 4 h and 5 h) occurred between ths perod of hghly excessve ncrease and the precedng and followng feedng/care perods. Data from ndvdual rats also showed these mnmal runnng perods, The dramatc ncrease n runnng on day 6 for rat '1 Baselne Treatment Recovery 3,,, l 2! ~-~ 25 1 W 8 15 Rot #45 Cn o_ 2 3 ns r ' o_ % Rat #182 6 ~" 4-2O ',,,.4"-,. Water ~tyo-o'o'.o..o o Food ~1oooo 5ooo S Day (c) FG. 3. Data for WD Rat, fed pelleted food. Daly anmal weghts. Total daly wheel revolutons. (c) Daly food and water ntake..o,o.,,.--"x, ka,. * Water quent ANOVA faled to show any effect of deprvaton on resdual water ntake (p >.5). Dstrbuton of Runnng Over Tme Temporal runnng dstrbutons were smlar n survvng rats regardless of treatment wth most runnng occurrng durng the dark perod from 183 h to 63 h. ncreases occurred n the frst 3 mn followng feedng and the 2 h between 7 h and the d 't =(Y"~ = Doy (c) FG. 4. Data for WD Rat fed powdered food. Daly anmal weghts. (h) Total daly wheel revolutons. (c) Daly food and water ntake.

6 456 BENEKE, SCHULTE AND VANDER TUG v Baselne Treatment Recovery 3, l,,, 25 less, ts greatest runnng occurred between 223 h and 33 h, wth a shorter burst of runnng occurrng n the hour precedng the followng days' care/feedng. f any dfference n the relatve dstrbuton exsts t s that self-starvng rats begn to run early n the lght perod followng feedng/care. DSCUSSON C O > O Rat #25 1,, v 4 ' ' * Water g) O -- 2 o Food 1 l ~ ' (c) Day FG. 5. Data for W Rat, fed pelleted food. Daly anmal weghts. Total daly wheel revolutons. ( ) Daly food and water ntake. (Fg. 3) occurred prmarly n two perods (183 h to 213 h and 24 h to 33 h) wth an ntervenng rest perod. Smlarly the excessve runnng for rat 182 (Fg. 4) on days 17 and 18 (1 and 11 of treatment) was due to runnng between 183 h and 33 h. Very lttle runnng occurred mmedately after feedng for ether rat. Both rats showed much lower peaks mmedately pror to the next days' care and feedng (6 h to 73 h). These patterns are comparable n dstrbuton (but not magntude) to runnng of W rats. Though rat 25 (Fg. 5) ran much Our results are consstent wth the actvty anorexa model (7). The pattem of changes over tme n food ntake, weght and daly runnng are also comparable to patterns shown n other studes (8) ncludng that wth humans (11,27) and wth reports of anorexa n endurance athletes (14,23,26,28) and excessve actvty n anorexc patents (15). The excessve amount of daly runnng observed here and elsewhere also s consstent wth the hypotheses that the excessve runnng s schedule-nduced by perodc feedng and that schedule-nduced behavor and the actvty n actvty anorexa share a common underlyng mechansm. However, other data from our study are not consstent wth ether hypothess. Frstly, f schedule-nduced behavors occur only wth pelleted food, and are elmnated by provdng food n a powdered form (3), actvty anorexa s not schedule-nduced. Provdng food n powdered form dd not elmnate the excessve runnng. Secondly, f the excessve runnng n actvty anorexa s schedule-nduced, other schedule-nduced behavors should also be present. Daly water consumpton represents a measure of one such behavor and nether group nor ndvdual data showed evdence of schedule-nduced polydpsa. The mean daly water consumpton durng treatment for deprved rats was actually less than that for nondeprved rats. Snce food and water ntakes are postvely correlated (6), reducton n food ntake produced by deprvaton could mask polydpsa. Ths mght be mportant n actvty anorexa because ncreased deprvaton accompanes the excessve runnng. When we examned ths further by statstcally adjustng water ntakes for reduced food consumpton we faled to fnd any effect of deprvaton on resdual water consumpton. The reduced water ntake n deprved rats was probably the result of reduced food ntake. That relatonshp has been demonstrated n other contexts (6,16). Thus, actvty anorexa developed n the absence of evdence for schedule-nduced polydpsa. Thrdly, dstrbuton of runnng n the nter-food nterval s uncharacterstc of schedule-nduced behavors. n the group runnng dstrbutons (Fg. 2), the area between the W and WD-- Anorexc curves can be seen as representng the excessve runnng attrbutable to the perodc food access. A schedule-nduced behavor hypotheses would predct that the majorty of excessve runnng would be nterm and termnal, fallng nto perods mmedately after and before feedng (18,24). However, lttle runnng occurred n the frst hour after feedng. We therefore suggest that schedule-nduced behavor does not provde an adequate model for the ncreased runnng n actvty anorexa, and t appears unlkely that applyng knowledge ganed from schedule-nduced behavor research wll contrbute to the understandng of anorexa n anmals or humans. Although chronobologcal theory appears to contrbute lttle to understandng the amount of runnng, the observed patterns of daly runnng n our study are consstent wth a chronobologcal model of runnng becomng entraned to both lght/dark cycles and perodc feedng (1,2,12,18,19). We observed a substantal ncrease n runnng 2 h pror to feedng/ anmal care n deprved rats and a smaller ncrease n raks wth unlmted access to food. One study whch ncluded both a

7 ACTVTY ANOREXA 457 lght/dark cycle and perodc feedng (18) showed that a feedng opportunty served as a zetgeber (tme gver), producng smlar antcpatory runnng. As n the present study, food avalablty was scheduled n the mddle of the lght cycle on a standard 12/12 lght/dark cycle. Antcpatory runnng descrbed n other actvty anorexa research (7) s also consstent wth the noton of feedng opportunty as a zetgeber. nformaton obtaned from runnng dstrbutons over the nter-food nterval n conjuncton wth the bologcal rhythm lterature may prove useful n the plannng and desgn of fu- ture research to uncover the causal relatonshps n actvty anorexa. ACKNOWLEDGEMENTS Lncoln Unversty Cooperatve Research manuscrpt number A Ths research was supported by USDA/CSRS projects MOX- OH and MOX-OH awarded to Lncoln Unversty. The authors wsh to thank Robert A. Hancock and W. Frank Eplng for ther suggestons and crtcal comments on earler drafts of ths manuscrpt, and Russ Rednger for hs suggestons on revsng the manuscrpt. REFERENCES 1. Bauer, M. S. ntensty and precson of crcadan wheel runnng n three outbred rat strans. Physol. Behav. 47:397-41; Brody, S. Boenergetcs and growth. New York: Renhold; Beck, C. H. M.; Huh, T. J. S.; Mumby, D. G.; Fundytus, M. E. Schedule-nduced behavor n rats: Pellets vs. powder. Anm. Learn. Behav. 17:49-62; Borer, K. T. Absence of weght regulaton n exercsng hamsters. Physol. Behav. 12: ; Borer, K. T. The nonhomeostatc motvaton to run n the golden hamster, lr= Morrson, A. R.; Strck, P. L., eds. Changng concepts of the nervous system. New York: Academc Press; Coller, G. Body weght loss as a measure of motvaton n hunger and thrst..ann. N.Y. Acad. Sc. 157:594-69; Eplng, W. F.; Perce, W. D. Solvng the anorexa puzzle: A scentfc approach. Toronto: Hogrefe & Huber; Eplng, W. F.; Perce, W. D.; Stefan, L. Schedule-nduced self-starvaton. n: Bradshaw, C. M.; Szabad, E.; Lowe, C. F. eds. Quantfcaton of steady-state operant behavour. Amsterdam: Elsever/ North Holland Bomedcal Press; Eplng, W. F.; Perce, W. D.; Stefan, L. A theory of actvty-based anorexa. nt. J. Eatng Ds. 3:27-46; Epsten, L. H.; Masek, B.; Marshall, W. Prelunch exercse and lunchtme calore ntake. Behav. Ther. 1 : 15; Falk, J. L. Producton of polydpsa n normal rats by an ntermttent food schedule. Scence 133: ; Honma, K.; Von Goetz, C,; Aschoff, J. Effects of restrcted daly feedng on freerunnng crcadan rhythms n rats. Physol. Behav. 3: ; Kanarek, R. B.; Coller, G. Self-starvaton: A problem of overrdng the satety sgnal? Physol. Behav. 3:37-311; Katz, J. L. Long dstance runnng, anorexa nervosa and bulma: A report of two cases. Comp. Psychatry 27:74-78; Kron, L.; Katz, J. L.; Gorzynsk, G.; Wener, H. Hyperactvty n anorexa nervosa: a fundamental clncal feature. Comp. Psychatry 19:433-44; Levtsky, D. A. Feedng patterns of rats n response to fasts and changes n envronmental condtons. Physol. Behav. 5:291-3; Levtsky, D.; Coller, G. Schedule-nduced wheel runnng. Physol. Behav. 3: ; Mstlberger, R. Crcadan ptfalls n expermental desgns employng food restrcton. Psychobology 18:23-29; Peng, M. T.; Kang, M. Crcadan rhythms and patterns of runnngwheel actvty, feedng and drnkng behavors of old male rats. Physol. Behav. 33:615-62; Routtenberg, A. Self-starvaton of rats lvng n actvty wheels: adaptaton effects. J. Comp. Physol. Psychol. 66: ; Routtenberg, A.; Kuznesof, A. W. "Self-starvaton" of rats lvng n actvty wheels on a restrcted feedng schedule. J. Comp. Physol. Psychol. 64: ; SAS nsttute nc. SAS/STAT User's Gude, Verson 6, 4th ed. vol. 1, Cary, NC:SAS nsttute nc.; ; Smth, N. J. Excessve weght loss and food averson n athletes smulatng anorexa nervosa. Pedatrcs 66: ; Staddon, J. E. R. Schedule-nduced behavor. n: Hong, W. K.; Staddon, J. E. R., eds. Handbook of operant behavor. Englewood Clffs, NJ: Prentce Hall; Staddon, J. E. R.; Ayers, S. L. Sequental and temporal propertes of behavor nduced by a schedule of perodc food delvery. Behavour 54: Temple, C. Athletcs nervosa. Athletcs Weekly: Oct 15; Woo, R.; Garrow, J. S.; P-Sunyer, F. X. Effects of exercse on spontaneous calore ntake n obesty. Am. J. Cln. Nutr. 36:47-477; Yates, A.; Leehey, K.; Shsslack, C. M. Runnng--an analogue of anorexa? N. Engl. J. Med. 38: ; 1983.