‘Looping’—an exploration mechanism in a dark open field

Behavioural Brain Research 159 (2005) 27ndash36

Research report

lsquoLoopingrsquomdashan exploration mechanism in a dark open field

Pazit Zadicario1 Reut Avni1 Eyal Zadicario David Eilamlowast

Department of Zoology Tel-Aviv University Klauzner St Ramat-Aviv 69978 Israel

Received 23 September 2004 accepted 29 September 2004Available online 10 November 2004

Abstract

The behavior of Tristramrsquos jird (a species of gerbil) in an illuminated open field resembled that of other rodents comprising round tripsto a home base and alternating between periods of progression (locomoting) and of stopping In this study we compared the characteristicsof exploration in a dark arena with exploration by the same individuals in a lit arena In the dark arena stopping episodes were brief andfewer suggesting almost continuous locomotion by the rodents The clear distinction between progression and stopping that had characterizedlocomotion in an illuminated arena thus diminished in the dark There was also no apparent home base in the dark and traveling consisted inmoving in a circular path closing a loop to a recently traveled place that varied from one loop to the next Locomotion in the dark may thusb to a homeb ippocampalrcopy

K

1

ostdsmmevewi[s

typ-the

asteroralex-

thav-

thely onnd-

g re-tedone of

eentancet ofightht

0d

e regarded as a set of loops (round trips) to a continuously shifting home base whereas with lights on the round trips convergease using visible environmental landmarks We suggest that a similar looping mechanism may be applicable to the behavior of hats displaying hyperactivity and diversified locomotion reminiscent of that seen in jirds in a dark arena

2004 Elsevier BV All rights reserved

eywordsExploration Home base Stopping behavior Navigation Orientation Path integration Visual landmarks

Introduction

Exploration and navigation are important tools in the studyf animal cognition and the underlying brain mechanismsince these behaviors are highly structured reflecting the ul-imate output of brain activity and integration of proximalistal olfactory visual and self-generated idiothetic cues Foruch research open field is the most widely used tool in ani-al psychology offering a relatively simple testing environ-ent for a variety of species[49] Numerous studies have

xamined behavior in the open field with lights on whenisual cues are available to provide the animal with refer-nces for navigation With lights on locomotor behavior ofild and laboratory rodents placed in an unfamiliar arena

s organized in reference to a key locationmdashthe home base6ndash810114041] At this key location the rodent demon-trates typical behaviors (eg grooming and crouching) and

lowast Corresponding author Tel +972 3 6406471 fax +972 3 6406988E-mail addresseilamposttauacil (D Eilam)

1 Equally contributed in all phases of this study

sets out on round trips in the area These trips have aical structure of slow locomotion and frequent stops inoutward-bound journey compared with fewer stops and flocomotion in the homeward bound one This spatio-tempstructure of locomotor activity was shown to withstandtensive changes in the size of the environment[8] To date ihas been unknown whether this structure of open field beior with lights on is also preserved with lights off whenanimal has to navigate in total darkness and cannot revisible landmarks lsquoSelectiversquo perception may apply to lamarks with different animals depending on different cues[1]For example rats have a preferred hierarchy in cue usinlying first on visual then olfactory and finally self-generacues (path integration)[29] For this reason experimentsnavigation and exploration try to control or isolate the rolspecific sensory information

When tested in the dark ratsrsquo level of activity has bshown to be raised expressed mostly in greater distraveled Their level of anxiety is lower and the amounrotations (turning) is higher than in rats tested in the l[42333] Moreover in the dark or in reduced moonlig

166-4328$ ndash see front matter copy 2004 Elsevier BV All rights reservedoi101016jbbr200409022

28 P Zadicario et al Behavioural Brain Research 159 (2005) 27ndash36

there is also a change in spatial distribution of the activityexpressed in spending more time in the open[23643] Eventhough such a great difference exists in the behavior of ro-dents in the dark its exploratory characteristics have not yetbeen identified In the present study we compared the behav-ior of the same individuals when exploring an illuminatedand a dark open field in order to determine whether the well-documented structure in a lit open field is also applicable forthe behavior in a dark open field

Tristramrsquos jirds (Meriones tristrami) were selected as testanimals for two reasons (1) to expand previous findings inwild [11ndash13]and laboratory[6] rodents to another speciesand (2) because they are agile nocturnal rodents with rela-tively large eyes that attest to the utilization of visual cuesThis latter feature makes jirds highly appropriate for thepresent test in light and dark where the major manipulationrelates to the role of visual landmarks in navigation and explo-ration Rats or mice for example would be less appropriatesince compared with jirds they rely more on olfactory cues

We posed three questions in this study (i) In the dark dojirds establish a home base and from it explore the arena asthey do in an illuminated open field (ii) Is the spatio-temporalstructure of progression and stopping in an illuminated arenawith stops being the building blocks of trips also applicableto behavior in the dark (iii) If the structure of behavior inthe dark proves to be different what are the characteristics oft

tinc-t ris-t nedo for-m

2

2

eG on-g -d sw ptivec sl un-d ver-t helterS of ex-p n ofw d Ata witht archA ion

2

h4 quiet

air-conditioned (24C) room illuminated by one of the followinglight-sources (1) two 300 W light bulbs directed to the white ceil-ing in order to provide diffused illumination of the arena (lights ontest) (2) two infrared lights (Tracksys IR LED Illuminator UK)with 830 nm filters that emit light not visible to animals and areknown as lsquocovertrsquo IR (lights off test light level was 00425 lux asmeasured with Profisix SbcGossen) While we could not find infor-mation on spectral sensitivity in jirds in rats it is about 510 nm[34]which is well below the filters used here A video camera (IkegamiBW ICD-47E) was placed 25 m above the center of the arena pro-viding a top view of the arena and the tested jird The video signalwas recorded on a VCR (JVC HR-J737) In testing with lights onroom structure was visible to the jirds providing various landmarks(eg the location of monitor windows closet door etc) Duringtesting with lights off all light sources (eg all indicator lights inthe video camera air-conditioner etc) were sealed by opaque tapeand the room was entirely dark except for the invisible IR light

23 Procedure

Jirds were caged individually in 60 cmtimes 40 cmtimes 20 cm metalcages and brought to a room adjacent to the testing room 10 h beforetesting At this time the animals were gently painted over their rumpand back with a large black ink marker to increase the contrastof their image to the background and improve the video imageComparing the behavior of the ink-marked jirds with others thatwere unmarked revealed that they behave the same (preliminaryo adedw m toh imalw to thec withl ast inga ightso by ac ghtso t thee bitionc

2

taa ldquonotm eedl thisl renaw

by

by

-oveisodee jird

his structureAs shown below behavior in the dark revealed a dis

ive structure of diversified locomotion whose characteics might contribute to a better understanding of lesior drugged animals displaying diversified locomotor perance

Methods

1 Animals

Tristramrsquos jird (Meriones tristrami) is a nocturnal rodent of therbillidae family with the same morphology and size as the Molian gerbil (Meriones ungiuculatus) It is a burrow-dwelling roent that feeds on seeds and green vegetation[30] Observationere carried out on eight adult male jirds obtained from a caolony Jirds were housed in 120 cmtimes 63 cmtimes 45 cm metal cageocated outdoors in the yard of Tel-Aviv University research zooer natural (uncontrolled) temperature and light conditions O

urned ceramic pots and wooden boxes in each cage provided seeds and diced fresh vegetables were provided daily Yearserience in maintaining jirds in our zoo have shown that provisioater is unnecessary if sufficient fresh vegetables are providell times animals were maintained and treated in accordance

he guidelines for animal care and for the use of animals in resell the animals used in the study were in good physical condit

2 Apparatus

Open field (=arena) was a 180 cmtimes 180 cm enclosure wit0 cm high walls and a smooth beige PVC floor located in a

bservations in this study and work in progress) Ink stains fithin 24 h were not perceptible after 48 h and did not seearm the jirds or to alter their behavior in any way A test anas removed from the cage to a jar and then gently released inenter of the arena Each jird was first videotaped for 10 minights off (IR lights on) The next day the same individual jird wested again for another 10 min this time with lights on allow

comparison between light and dark tests Behavior with ln was not affected by the preceding dark testing as shownomparison with the behavior of jirds that were tested with lin but without the preceding dark testing (data not shown) And of testing animals were returned to the breeding and exhiolonies at the research zoo

4 Data acquisition and analyses

A tracking system (Ethovisionby Noldus NL) was used for dacquisition The tracking system was set to score the jird asovingrdquo (=stopping) when its center of gravity moved at a sp

ower than 2 cms or as ldquomovingrdquo when the speed exceededimit during tracking at a sampling rate of 125 framess The aas divided into 25 zones each comprising a 36 cmtimes 36 cm square

The following parameters were acquired via Ethovision

Total traveled distance (m) Overall metric distance traverseda jird during 10 min observationAverage traveling speed (ms) Total traveled distance dividedthe total traveling timeNumber duration and location of stops Incidence of nonlocomoting periods in which the jirdrsquos center of mass did not mmore than 2 cms The duration of each such stopping epwas also scored alongside the name of the zone in which thstopped

P Zadicario et al Behavioural Brain Research 159 (2005) 27ndash36 29

Momentary speed (ms) and turn angle (degreess) During eachdata point (008 s) these parameters were calculated by the track-ing system as the traveling speed and the change in the directionof progression (respectively)Distance to center (m) Metric distance of the jirdrsquos center of massto the center of the arena was measured at intervals of 008 s (125timess)Loops Inspection of the videotapes revealed that the locomotorbehavior of the jirds comprised loops in which the animals per-formed round trips back to different places in which they had re-cently traveled To identify and measure loops a custom-designedprogram (PathAnalyse by EZ) was used This program used theoutput of the tracking system (x y coordinates and time) to furtheranalyze the routes and provided the total number of loops theirlocation length (m) and duration (s) of each loop The programalso provided thenodemdashx y coordinates of starting and endingpoint of each loop

Loop analysis algorithm provided interactive means such as theminimal and maximal loop length and duration and the spatial res-olution criteria required to consider a loop as closed For these anal-yses the algorithm created a 2D matrix as bounding box of thesampled points within the analyzed loop In general the matrix res-olution could be arbitrary however we used a 1 mmtimes 1 mm gridData points of each jird were sequentially entered into the matrixWhen entering each data point the program checked for a possi-ble hit with a previous data point When such a hit occurred theloop criteria were checked and if metmdasha new loop was registeredO pro-v lgo-

rithm were extracted from playback of the videotapes and set asfollows

Maximum loop distance= 800 cm This was slightly little longerthan the perimeter of the arena and we assumed that it reflects thelongest loop in the 180 mtimes 180 m arenaMinimum loop duration= 23 s This was the shortest loop foundupon examining of the videotapesMaximum loop duration= 60 s This was the longest loop foundupon examining the videotapesMinimum loop bounding= 15 cm (length of the jird body) Thiswas the minimum loop distance a jird could perform as any shorterdistance would be simply turning in place Loops smaller than thisvalue were therefore ignored

Once loops were identified we further calculated the metric dis-tance (m) between the nodes of successive loops defined the direc-tion of progression in the loop as clockwise or counterclockwiseand classified the loop into one of the following types (Fig 1)

Simple loop A simple round trip that started and ended in the samelocationNested loop A loop that started and ended before the end of thepreceding loop with the trajectory of the first loop encompassingthe second loop8-Shaped loop A loop that started and ended before the end of thepreceding loop (as in nested loop) but with the trajectory of thesecond loop being outside the trajectory of the preceding loopOthers Loops that did not match the above forms were grouped

or

F starts In loop 2t unterclo travet ted onl istantc p and b ner( it start th loopsr ion of a fore ther2od

nce all data points were entered the registered loops wereided as the result of the algorithm The criteria used in the a

ig 1 Sketch of loop types (a)Simple loops two loops are shown loop 1he rodent first travels to the bottom left corner and there makes a coo the top left corner (home base) In that case loop length is calculaomprises both loop length and the return journey between the left tonode and lsquohome basersquo) but before closing a loop back to this locationodent is traveling counterclockwise (c)8-Shaped loop this is a modificat

odent returns to the node of the primary loop 1 (d)lsquoHybridrsquo loop the overall struand 3) Note that the form of loops is established in reverse order first loof two subsequent loops with same node and alternate traveling directions cark (f)Biased loops two subsequent loops with the same node both with co

here typically consisting of hybrid forms of ldquofusedrdquo simple8-shaped loops

and ends at the top left corner that is the node of this clockwise loopckwise loop back to the node at the bottom left corner From there itls again

y from and back to the node and thus differs from the total traveled dce thaottom corners (b)Nested loop the rodent starts to travel from the top left cors another loop (2) that ends before the end of the major loop 1 In bo theldquonested looprdquo where again the secondary loop 2 starts and ends be

cture is of two 8-shaped loops connected at one point (node between loops

p 4 then 3 then 2 and finally 1 is formed (e)Alternating loops the mechanismlockwise (2) and counterclockwise (1) This was a common form in looping in theunterclockwise traveling direction This was rare in looping in the dark


25 Statistics

Unless noted otherwise statisticalt-test for dependent samples(=pairedt-test) was used in comparing measurements for the samejirds in illuminated vs dark arena Some of the data may not bestrictly independent Therefore a Bonferroni correction was appliedto set alpha level to 00036 (005 divided by the 14 parameters thatwere compared for each jird)

3 Results

Fig 2 describes trajectories of locomotion of the samethree jirds as performed first in the dark (top) and again thenext night at the same time but with lights on (bottom) Asshown trajectories in the light converged to a home baseand could be viewed as a set of loops that started and endedin that home base In contrast trajectories in the dark didnot show these features instead conveying an impression ofchaos This difference in path shape was also evident in theparameters that characterize open field activity (Table 1) Asshown jirds in the dark traveled longer distances at slowertraveling speed During progression the overall number ofstops made during lights off was not significantly differentfrom the number performed during lights on but the meand duet ught differb fs k Oft d offi edw

asesi ioral

changes observed in jirds moving in a dark compared to anilluminated arena in the dark jirds traveled at a slow speedwith only brief stopping episodes whereas in the illuminatedarena they alternated between relatively long stops and fastrunning bouts In other words behavior in the dark took theform of continuous slow locomotion whereas behavior withlights on comprised alternations between stopping and fastprogression These different behavioral patterns are shownin the frequency of traveling speed (Fig 3) where the inci-dence of stopping bouts (speed = 0) and high traveling speed(more than 1 ms) were high in jirds traveling with lights onwhereas the incidence of traveling at low speed (less than1 ms) were higher in the dark

Slow progression and diminished stop-duration werelinked to another difference jirds in the illuminated arenahad a lsquohome basersquo a corner where they spent extended pe-riods and stopped more often than in other places whereasno lsquohome basersquo was discernible in the dark arena Indeed inthe dark time spent at the various places and incidences ofstopping at these places were in a narrow range without thedistinct level that characterized home base (Fig 4) Home-base behavior is also illustrated inFig 2 where convergenceof trajectories of progressions to a home base corner is appar-ent in the illuminated but not in the dark open field In all thelack of home base behavior in the dark as revealed in the lostdistinction of one place from the others and the divergenceo ctionb oder-a aviora cablet a

oka edo ersa hts

F for thre ttw y same

uration of a stop was significantly shorter in the darko a decline in the number of long stops Indeed althohe mean number of short stops (less than 3 s) did notetween testing with lights on or off (Table 1) the number otops longer than 3 s significantly decreased in the darhese longer stops those longer than 10 s virtually levelen the dark comprisingsim05 of the total stops comparith sim3 with lights on (Table 1)The longer traveled distance together with decre

n stop duration and traveling speed reflected behav

ig 2 Trajectories of locomotion during 10 min observation depictedere tested on two successive days first day in the dark and next da

f trajectories of progression as well as the faded distinetween progressing and stopping and traveling at a mte steady speed indicated that regarding open field behs a set of trips (or loops) to a home base was not appli

o the apparently chaotic behavior of jirds in a dark arenThe spatial distribution of activity in the dark also to

distinctive form compared with activity in an illuminatpen fieldFig 5depicts the time that jirds spent at cornlong walls and in the center of the open field With lig

e jirds (columns) in a dark arena (top) and in an illuminated arena (boom) Jirdstime with lights on


Table 1Parameters (meanplusmn SEM) of locomotor behavior in lit and dark arenas

Light Dark t7 p

Total distance (m) 651plusmn 105 1498plusmn 142 minus853 00006Traveling speed (ms) 045plusmn 005 029plusmn 003 387 0006 (ns)

StopsTotal number 26513plusmn 3809 3115plusmn 2736 minus1054 03271 (ns)Mean duration (s) 1298plusmn 067 459plusmn 031 511881 00014No of stops shorter than 3 s 2570plusmn 392 31012plusmn 275 minus119 0273 (ns)No of stops longer than 3 s 2562plusmn 135 8125plusmn 236 8910564 000005No of stops longer than 10 s 8125plusmn 156 1375plusmn 067 5891883 00006

Results of pairedt-tests are given for a comparison of the same eight voles in lit and dark arenas

on jirds spent more than 79 of the time at the corners andless than 7 in the center whereas in the dark there was asignificant increase in the time spent in the center and alongthe walls with a concomitant decrease in time spent in thecorners

To quantify this shift of activity to the center in the darkarena we defined an imaginary center point and measuredthe distance of the jird from this center in each data point(125 data points per s) The mean distance to the center de-clined from 109plusmn 003 m with lights on to 076plusmn 025 m inthe dark (t7 = 1975plt 000001) These values demonstratethat with lights on the jirds spent virtually all their time alongthe walls located about 1 m from the center of the open fieldwhereas in the dark they moved away from the walls (075 mfrom the center which meanssim020 m from the walls) Thisshift is also apparent inFig 2 The typical structure of ex-

F ateda d eachj om 0t calei wash arenajt0

ploration as a set of round trips to a home base was thuspreserved with lights on but vanished with lights off Al-though behavior in the dark appeared chaotic playback ofthe videotapes revealed that the jirds were repeatedly return-ing to a recently traveled place a mechanism that we termedldquoloopingrdquo In other words the jirds traveled along a circulartrajectory closing their path as a loop to a nodemdasha recentlytraveled place that varied among subsequent loops[9]

When the algorithm that defines a loop (Section2) wasapplied to open field behavior in either the dark or the illu-minated arena the mean number of loops was significantlyhigher in the dark (339plusmn 48) compared with the illumi-nated (131plusmn 24) arena (Pairedt-testt=minus787p= 00001)However this higher number of loops accorded with the in-

F uaresi eachj sc s offAs shown duration of staying (top) and incidence of stopping with lights on(thick line) were distinctively higher in the first rank and declined steeply

ig 3 Frequency distribution of momentary speed in dark and illuminrena For each jird traveling speed was measured 125 timess an

ird contributed 7500 data points These were pooled and ranked fro 2 ms The frequency of these ranks is plotted on a logarithmic sllustrating that with lights on frequency of stopping bouts (speed = 0)igher as well as traveling at a speed higher than 1 ms In the dark

irds typically traveled at a speed lower than 1 ms whereas frequency ofraveling at a higher speed declined steeply and stopping frequency (speed) was lower than in the lit arena

two

ig 4 Duration of staying and stop incidence in each of the equal 25 sqn illuminated and dark arenas In tests with lights on 25 data points ofird were ranked from high to low and the mean (plusmnSEM) of each rank waalculated Similar procedure was applied to data obtained with light

hereafter Even the high ranks in the dark (thin line) were relatively lowithout any one rank prominent above or below unlike in testing with lightsn


Fig 5 Duration of time spent at each section of the open field is illustrated forcorners along walls (excluding corners) and center (away from corners andwalls) A two-way ANOVA with repeated measures reveled that the effectof light was not significant (F17 = 198p= 018) the effects of section andthe interaction of lighttimes section were significantly different (F17 = 7981plt 00001 andF17 = 12025plt 00001 respectively for section and inter-action)

creased activity in the dark the ratio between traveled dis-tance and number of loops was almost identical in both illu-minated and dark open fields Consequently loop length wasnot significantly different between testing in light or dark(319plusmn 064 m and 282plusmn 022 m respectivelyt7 = 073p= 049) and for both total loop length comprised 65 ofthe total traveled distance Nonetheless despite this quanti-tative similarity there was a substantial difference betweenlooping in dark or lit arenas as shown below

The nodes (ldquoclosing locationrdquo) of loops in the illuminatedarena were located along or in the vicinity of walls whereasnodes in the dark arena occurred mainly at the center of thearena (Fig 6a) The vast majority of loops (886) in the illu-minated arena were ldquosimple loopsrdquo (Fig 1) and their nodestypically converged at or in the vicinity of the home baseAnother 95 were ldquonested loopsrdquo (Fig 1) where at a cer-tain point in the round trip to home base the jird formedanother shorter loop with its node on the trajectory of thelonger loop (round trip) to the home base Only a few loops(sim2) in the illuminated arena displayed a more complexform In the dark 75 of the loops were simple loops andanother 15 were lsquo8-shapedrsquo loops (Fig 1) The remaining10 were of the more complex form While looping withlights on converged to the same few locations (typicallycorners) looping in the dark diverged and kept shiftingacross successive loops spreading activity over the arena( ona e-t amej i-t ar lo-c odesk ens onw off(

Fig 6 Spatial distribution of loop nodes in lit and dark arenas (a) Nodes ofall loops in the eight jirds are depicted in for (left and dark (right) arenas Ineach the square represents the arena and the dots the location of the nodesof loops As shown nodes in testing in light mainly aggregated at cornersand along walls in contrast to being scattered through the center in testingwith lights off (b) The nodes of loops for one individual jird tested in light(left) and dark (right) open field Nodes are connected with lines in the orderof occurrence As shown when tested with lights on nodes converged at thehome base (bottom left corner) where they overlap with a minimal distanceOther nodes were at far corners with large inter-node distance (see alsoFig 1a) Nodes of the same jirds in the dark arena were spaced at moderatedistances in the center (c) Mean frequency (plusmnSEM) of inter-node distance(as plotted in b) in lit and dark arenas Frequencies in dark arena were highfor up to 100 cm declining steeply for longer inter-node distances In litarenas inter-node distances were relatively high for up to 40 cm and for160 cm or more

Loops in the dark were further structured to gradually ex-tend to cover the entire arena This is illustrated inFig 7where the first loops are confined to a small sector of the arenaand then gradually extend to encompass the entire arena Thegenerality of this expansion is shown inFig 8 where looplength gradually increased in the dark but decreased in the litarena

Finally the mean ratio between clockwise and coun-terclockwise loops was similar in both illuminated anddark arenas (132plusmn 013 and 127plusmn 011 respectively)However the incidence of looping in a direction opposite

Fig 6b) and resulting in a diversified form of progressis shown inFig 2 The difference in location of nodes b

ween illuminated and dark arenas is shown for the sird (Fig 6b left) illustrating how with lights on nodes eher aggregated at the same corner or occurred at a fation (typically another corner) whereas in the dark nept shifting (Fig 6b right) The mean distance betweuccessive nodes was either short or long with lightshile being short or moderate (but not long) with lights

Fig 6c)


Fig 7 Trajectories of traveling under lights off and lights on are shown for the same individual jird For each test trajectories are plotted for consecutiveperiods of 150 s In the dark (top) the jird initially confined its locomotion to the center right part of the arena (150primeprime) then expanded locomotion to the righttop and bottom corners (300primeprime) then to the left half of the arena (450primeprime) ultimately covering the entire arena (600primeprime) In the lit arena (bottom) the jird movedalong the entire perimeter irregularly crossing the center with an overall decrease in traveling in the course of observation

Fig 8 Increased loop length in a dark arena compared with decreased looplength in lit arena Mean (plusmnSEM) were calculated for each five consecutiveloops of each jird Loop length in dark () and lit () arenas was almostequal in the 1st bars representing the first five loops in each jird Similarvalues also characterize the next five loops (2nd) However loop lengthdecreased in the lit arena but kept increasing in the dark arena resulting ina large difference in length of loop 20 and on (5th bars)

to that of the preceding loop was significantly higher in thedark compared with maintaining the direction of the formerloop (Pairedt-test t7 = 409p= 0004) In the illuminatedarena the difference in these incidences was not significant(Paired t-test t7 = 147 p= 018) Alternating loopingdirection in the dark arena also resulted in a minimal meanamplitude of turn angle (minus67 plusmn 09) compared with awider turn angle in the illuminated arena (minus463 plusmn 68Pairedt-test t7 =minus673p= 000027) reflecting an overallbias to counterclockwise turns with lights on in contrast toequivalent turning in the dark

As implied inFig 7 looping in both the illuminated andthe dark arena was in fact structured and the jirds kept re-

turning to recently traveled and therefore relatively familiarlocations

4 Discussion

In this study we set out to determine the organization ofopen field behavior in the dark Previous studies had shownthat open field behavior in an illuminated arena comprisesbouts of progression and stopping with frequent and extendedstops at a lsquohome basersquo that is established soon after a rodentis introduced into the open field[11] At the home base therodent spends cumulatively the largest amount of time and itis also the most visited location From this home base the ro-dent embarks upon round trips that comprise up to eight stopswhether in a small or a large arena[1024] Open field be-havior in an illuminated arena is stable withstanding drasticchanges in arena size a stability that further corroborates thehome base round trips (loops) and stopsround trip as build-ing blocks of the spatio-temporal structure of exploration inrodents In the present study we found that this structure ispreserved when jirds move in an open field with lights on butvanishes with lights off In the dark jirds slowly and con-tinuously progress in loops mainly in the center of the darkarena with loop nodes (start and end points) not convergingto a home base but instead changing between loops

omt owi meb e oft anceo cuesa imalr arks

Looping behavior in the dark is intriguing especially frhe perspective of a possible lsquofunctionalrsquo explanation of ht may explain exploration and navigation without a hoase In order to orient a jird may rely on at least on

wo mechanisms (1) perception of the direction and distf spatial cues and (2) path integration Familiar spatialssociated with a specific location function to help the aneturn to such locations In the present study visual landm


were available when the jirds were tested in the light butinvisible when they were tested in the dark With lights offthe jirds enter a homogenous environment where they mustrely on cues that change as a function of the animalsrsquo ownmovements[37] their olfactory traces[28] and the physicalstructure of the arena The latter cue however seem lessrelevant in dark testing where jirdsrsquo activity was mainly inthe center of the arena away from the walls and corners

The capacity of a navigator to deduce its location fromself-movements in relation to its point of departure even inthe lack of external references is termed path integration(or dead reckoning[1415192031]) Path integration pro-vides the animal with a self-generated vector that points to thestarting point of the integrator it does not depend on learnedreferences but purely on internal signals such as vestibular orproprioceptive afferences[1415] Unless supported by land-marks path integration is effective only for short excursions[31726] and becomes increasingly inaccurate (as is deadreckoning in ship navigation) One obvious way to decreasethe uncertainty in location is to repeat the measurements Forthis to be effective path integration has to be re-initializedperiodically[16] which means that the animal has to returnto the origin of computation that is to the arbitrary node (ar-bitrary but recognizable visually olfactorily etc as well asby the fact that it is approximately coincident with the zeroof path integration)

atiall tionT stab-l isualr si so orya ndedl re-d gres-s thatc onseq n thel ed ina ppo-s tanceaO -i uall

Thej on-m rninge sings eirm ajorp im-p ntilc here-f y be

retained also for the following loop (see below) after whichit changes so that the node of the next loop is in a differentplace The result of such a continuous shift in loop nodes canbe divergence of activity over the arena and seeming chaosNode drifting in the dark is not likely to be a result of thelack of visual cues and inaccuracy in navigation since thejirds accurately returned to the same node in 8-shaped loops[9] Therefore this drift appears to be an element of naviga-tion and exploration in the dark Indeed the present resultssuggest that jirds are well organized even in total darkness(Fig 7) Three characteristics apparently account for the or-ganization of progression in the dark (i) alternating loopingdirections (ii) intermediate distance between nodes and iii)gradual increase in loop length Alternating looping directionis a mechanism that brings the animal back to the vicinity ofrecently traveled places[9] A reminiscent mechanism wasdescribed in desert ants (Cataglyphis fortis) that turn as fre-quently to the right as they do to the left making an overalldirectional bias unlikely to develop[32] In the dark nodesdo not converge (minimal distance) as in home base but theyalso do not shift greater distances away as in the light insteadremaining in the vicinity of previous nodes This mechanismkeeps the jird temporarily within a section of the open fieldallowing it to gradually increase loop length until covering theentire open field (Figs 7 and 8) Altogether these may reflecta built-in night-adapted strategy involving more crossing oft ops

be-h tedi thew ffT atedo to bea e be-h ntlyi thew idedb of thea

be-h asei stopsl rousfi n thed ghtF reaset ha-b sd thusr

nceb enass oundt thed s top red

In the illuminated arena the jirds could use both spandmarks and path integration in navigation and explorahis is probably reflected in the shown preference to e

ish the home base in a corner which facilitates precise vecognition and from this home corner[21] to set out in loopn the open field relying on path integration[4447]and cueriginating from a variety of sources (eg visual olfactuditory etc) Frequent returns to home base and bou

oop length[1024] therefore ldquoresetrdquo path integration anduce possible cumulative navigation error Indeed proion in an illuminated open field comprised round tripsonverged to the home base and whose nodes were cuently close to each other Those nodes of round trips i

it arena that did not occur at the home base were locatnother visually identifiable location such as a corner oite the home corner (and hence at a long inter-node diss shown inFig 6) or along the walls of the arena (Fig 1)verall as suggested previously[1045] locomotor behav

or in an illuminated open field probably relies on both visandmarks and path integration

In the dark open field visual cues were not availableirds that were introduced to this dark unfamiliar envir

ent nonetheless explored it in structured loops retuach time to a different recently traveled place progreslowly with only brief stops and gradually spreading thovement to encompass the entire dark open field A mart of a jirdrsquos progression in the dark was comprised of ldquosle loopsrdquo which is a progression along a circular path urossing a recently traveled path The crossing point is tore the beginning and end of the loop (node) and it ma

-

he field slower locomotion fewer stops and shifting loTwo other substantial differences between open field

avior with lights off compared with lights on are reflecn the higher level of activity in the dark and clinging toalls with lights on but moving in the center with lights ohe greater time spent close to the walls in an illuminpen field is unsurprising However this does not seemmere thigmotactic response since it should affect th

avior in the dark open field in a similar way Consequet is probably linked to the sense of security provided byalls in an illuminated arena whereas the security provy the darkness allows greater movement in the centerrena as also shown in other rodent species[258183842]

A high level of activity is an obvious characteristic ofavior in a dark arena with a more than two-fold incre

n traveled distance alongside decreased incidence ofonger than 3 s Higher activity was described in numeeld and laboratory studies of nocturnal species tested iark compared with their activity when tested under lior example when tested in the dark laboratory rats inc

heir activity and display behaviors that indicate reducedituation fear and anxiety[33] The present finding that jirdemonstrate a higher level of locomotion in the darkeinforces previous results on the effect of light level

It should be noted that basically the substantial differeetween open field behavior in illuminated and dark artems from one major difference the convergence of rrip nodes to home base in a lit arena in contrast withrifting location of loop nodes in a dark arena This sufficeroduce the distinctive form of behavior in a dark compa


with an illuminated arena In other words a single changemay account for the subsequent apparently chaotic form[22]of locomotor behavior

Another albeit smaller difference between behavior withlights on and lights off is the decreased stop duration andthe relative decrease in the incidence of stopping (as com-pared with the increased traveled distance) In intermittentprogression stops increase the capacity of the sensory sys-tems to detect relevant stimuli and may be related to velocityblur relative motion detection foveation attention and inter-ference between sensory systems[27] Indeed looping at aslow steady velocity in the dark exerts a continuous vestibu-lar stimulation that is asymmetrical due to the circular pathThis with probably some spatial cues such as scent mark-ing allows accurate path integration of jirds in the dark (seevideo-clips in[9]) Since this vestibular information differsfrom that exerted by switching between galloping and stop-ping in testing with lights on it calls for attention to a possiblydistinct modulation of path integration by various modes ofthe vestibular cues

The incessant progression that we recorded in jirds in adark arena compared with their intermittent activity in a litarena was recorded during 10 min of observation Over alonger observation period the animals will probably pausefor rest It will thus be intriguing to determine whether theprospective increase in stop duration will involve establish-m in al ands andt tionp y

o be-h truc-t st lab-o herr e-h in ad ethero rena( f be-h

od-e logies[ erlys be-h diesw peract incet omeb -p s oft re forj T thed hav-

ior in terms of ldquoloopingrdquo may shed new light on the structureof this seemingly disordered behavior and therefore providenew information on the role of the hippocampus in the orga-nization of behavior in time and space

Acknowledgements

We are grateful to Emanuel Baker for his help in testingand data acquisition to Naomi Paz for editing the manuscriptBarak Levy and the zookeepers of the I Meier Segals Gardenfor Zoological Research for maintenance of the jirds Thisresearch was supported by The Israel Science FoundationGrant 47104

Appendix A Supplementary data

Supplementary data associated with this article can befound in the online version at101016jbbr200409022

References

[1] Birke LI DrsquoUdine B Albonetti ME Exploratory behavior of twospecies of murid rodentsAcomys cahirinusand Mus musculus a

e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation

ent of a home base at which loops might converge asit arena Further studies are required to reveal the timingtructure of later phases of behavior in a dark open fieldheir emergence from the initial exploration and navigarocesses that have been described in the present stud

Another issue is the generality of the present results tavioral organization in the dark The spatio-temporal s

ure of jird exploration in an illuminated open field followhe spatio-temporal organization described in wild andratory rats and mice[7] suggested as applicable to otodent species[8] It is possible that similarity in rodent bavior in an illuminated open field extends to behaviorark arena too and further studies should examine whther rodents that share the behavioral structure in a lit aeg laboratory rats and mice) also share the structure oavior that jirds display in dark

Lastly looping bears a possible relevance to animal mls that use open-field behavior to assess psychopatho

35394649] The present results demonstrate an ordtructure apparent in the seemingly chaotic locomotoravior in a dark arena This calls for attention in other stuhere apparent chaos has been found Of these the hy

ive behavior of hippocampal rats is of special interest shese rats were impaired in their return trajectories to hase in exploratory round trips[2545] Moreover when hipocampal rats were tested with light on or off trajectorie

heir locomotion appeared similar to those described heirds tested respectively with lights on or off ([48] p 169)hese rats were described to ldquolocomote at random inarkrdquo and we suggest that analyzing their locomotor be

-

comparative study Behav Neural Biol 198543143ndash61[2] Brillhart DB Kaufman DW Influence of illumination and surfac

structure on space use by prairie deer mice (Peromyscus maniculatbairdii) J Mamm 199172764ndash8

[3] Cain DP Beiko J Boon F Navigation in the water maze the roproximal and distal visual cues path integration and magneticinformation Psychobiology 199825286ndash93

[4] Crawley JN Attenuation of dark induced hyperlocomotioncholecystokinin antagonist in the nucleus accumbens Brain1988473398ndash400

[5] Diaz M Rodent seed predation in cereal crop areas of cespainmdasheffects of physiognomy food availability and predationEcography 19921577ndash85

[6] Drai D Golani I See a tool for the visualization and analysis odent exploratory behavior Neurosci Biobehav Rev 200125409

[7] Drai D Kafkafi N Benjamini Y Elmer G Golani I Rats and mshare common ethologically relevant parameters of exploratorhavior Behav Brain Res 2001125133ndash40

[8] Eilam D Open-field behavior withstands drastic changes in asize Behav Brain Res 200314253ndash62

[9] Eilam D Video clips of a jird in illuminated arean and a jird indark arenahttpwwwtauacilsimeilam 2004

10] Eilam D Dank M Maurer R Voles scale locomotion to the sizthe open-field by adjusting the distance between stops A polink to path integration Behav Brain Res 200314173ndash81

11] Eilam D Golani I Home base behavior of rats (Rattus norvegicus)exploring a novel environment Behav Brain Res 198934199ndash

12] Eilam D Golani I Home base behavior in amphetamine-treatedwild rats (Rattus norvegicus) Behav Brain Res 199036161ndash70

13] Eilam D Golani I Amphetamine induced stereotypy in ratsmorphogenesis in locale space from normal exploration In CoSJ Hendrie CA editors Ethology and pharmacology ChicheWiley 1994 p 241ndash66

14] Etienne AS Berlie J Georgakopoulos J Maurer R Role ofreckoning in navigation In Healy S editor Spatial representin animals Oxford Oxford University Press 1998 p 54ndash68


[15] Etienne AS Maurer R Berlie J Reverdin B Rowe T Georgakopou-los J et al Navigation through vector addition Nature 1998396 p161ndash4

[16] Etienne AS Maurer R Boulens V Levy A Rowe T Resetting thepath integrator a basic condition for route-based navigation J ExpBiol 20042071491ndash508

[17] Etienne AS Maurer R Seguinot V Path integration in mammals andits interactions with visual landmarks J Exp Biol 1996199201ndash9

[18] Falkenberg JC Clarke JA Microhabitat use of deer mice effects ofinterspecific interaction risks J Mamm 199879558ndash65

[19] Gallistel CR The organization of learning Cambridge Brad-fordMIT Press 1990

[20] Gallistel CR Cramer AE Computations on metric maps in mam-mals getting oriented and choosing a multi-dimension route J ExpBiol 1996199211ndash7

[21] Geyer MA Russo PV Masten VL Multivariate assessments of loco-motor behavior pharmacological and behavioral analyses PharmacolBiochem Behav 198625277ndash88

[22] Gleick J Chaos making a new science London Penguin Books1988

[23] Glick SD Cox RD Nocturnal rotation in normal rats correlationwith amphetamine-induced rotation and effects of nigrostriatal le-sions Brain Res 1978150149ndash61

[24] Golani I Benjamini Y Eilam D Stopping behavior constraintson exploration in rats (Rattus norvegicus) Behav Brain Res19935321ndash33

[25] Gorny JH Gorny B Wallace DG Whishaw IQ Fimbria-fornix le-sions disrupt the dead reckoning (homing) component of exploratorybehavior in mice Learn Memory 20029387ndash94

[26] Griffin AS Etienne AS Updating the path integrator through visualfix Psychobiology 199826240ndash8

[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats

[34] Neitz J Jacobs GH Reexamination of spectral mechanisms in therat (Rattus norvegicus) J Comp Psychol 198610021ndash9

[35] Paulus MP Geyer MA Environment and unconditioned mo-tor behavior influences of drugs and environmental geome-try on behavioral organization in rats Psychobiology 199725327ndash37

[36] Price MV Waser NM Bass TA Effects of moonlight on microhabitatuse by desert rodents J Mamm 198465353ndash6

[37] Save E Poucet B Thinus-Blanc C Landmarks use and the cognitivemap in the rat In Healy S editor Spatial representation in animalsOxford Oxford University Press 1998

[38] Sonnino S Spatial activity and habitat use of crested porcupineHys-trix cristata l 1758 (rodentia hystricidae) in central Italy Mammalia199862175ndash89

[39] Szechtman H Sulis W Eilam D Compulsive checking behavior inthe rat chronic treatment with the dopamine agonist quinpirole asan animal model of obsessive-compulsive disorder Behav Neurosci19981121475ndash85

[40] Tchernichovski O Benjamini Y The dynamics of long term ex-ploration in the rat Part ii An analytical model of the kine-matic structure of rat exploratory behavior Biol Cybern 199878433ndash40

[41] Tchernichovski O Benjamini Y Golani I The dynamics of longterm exploration in the rat Part i A phase plane analysis of therelationship between location and velocity Biol Cybern 199878423ndash32

[42] Topping MG Millar JS Goddard JA The effects of moonlight onnocturnal activity in bushy-tailed wood rats (Neotoma cinerea) CanJ Zool 199977480ndash5

[43] Vasquez RA Patch utilization by three species of chilean ro-dents differing in body size and mode of locomotion Ecology

[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior

27] Kramer DL McLaughlin RL The behavioral ecology of intermittlocomotion Am Zool 200141137ndash53

28] Lavenex P Schenk F Olfactory traces and spatial learning inAnim Behav 1998561129ndash36

29] Maaswinkel H Whishaw IQ Homing with locale taxon and dreckoning strategies by foraging rats sensory hierarchy in snavigation Behav Brain Res 199999143ndash52

30] Mendelssohn H Yom-Tov Y Fauna palaestina mammalia of ised TIAoSa Humanities Jerusalem Keterpress Enterprises

31] Mittelstaedt H Mittelstaedt ML Homing by path integration inmammal Naturwissenschaften 198067566

32] Muller M Wehner R Path integration in desert antsCataglyphisfortis Proc Natl Acad Sci USA 1988855287ndash90

33] Nasello AG Machado C Bastos JF Felicio LF Sudden darkinduces a high activity low anxiety state in male and femalePhysiol Behav 199863451ndash4

1996772343ndash5144] Wallace DG Gorny B Whishaw IQ Rats can track odors o

rats and themselves Implications for the study of spatial behBehav Brain Res 2002131185ndash92

45] Wallace DG Hines DJ Whishaw IQ Quantification of a singleploratory trip reveals hippocampal formation mediated dead recing J Neurosci Methods 2002113131ndash45

46] Walsh RN Cummins RA The open field test a critical revPsychol Bull 197683482ndash504

47] Whishaw IQ Brooks BI Calibrating space exploration is imporfor allothetic and idiothetic navigation Hippocampus 19999659

48] Whishaw IQ Kolb B The analysis of behavior in the laboratoryIn Robinson TE editor Behavioral approaches to brain reseNew York Oxford University Press 1983 p 141ndash211

49] Wilson RC Vacek T Lanier DL Dewsbury DA Open-field behain muroid rodents Behav Biol 197617495ndash506


there is also a change in spatial distribution of the activityexpressed in spending more time in the open[23643] Eventhough such a great difference exists in the behavior of ro-dents in the dark its exploratory characteristics have not yetbeen identified In the present study we compared the behav-ior of the same individuals when exploring an illuminatedand a dark open field in order to determine whether the well-documented structure in a lit open field is also applicable forthe behavior in a dark open field

Tristramrsquos jirds (Meriones tristrami) were selected as testanimals for two reasons (1) to expand previous findings inwild [11ndash13]and laboratory[6] rodents to another speciesand (2) because they are agile nocturnal rodents with rela-tively large eyes that attest to the utilization of visual cuesThis latter feature makes jirds highly appropriate for thepresent test in light and dark where the major manipulationrelates to the role of visual landmarks in navigation and explo-ration Rats or mice for example would be less appropriatesince compared with jirds they rely more on olfactory cues

We posed three questions in this study (i) In the dark dojirds establish a home base and from it explore the arena asthey do in an illuminated open field (ii) Is the spatio-temporalstructure of progression and stopping in an illuminated arenawith stops being the building blocks of trips also applicableto behavior in the dark (iii) If the structure of behavior inthe dark proves to be different what are the characteristics oft

tinc-t ris-t nedo for-m

2

2

eG on-g -d sw ptivec sl un-d ver-t helterS of ex-p n ofw d Ata witht archA ion

2

h4 quiet

air-conditioned (24C) room illuminated by one of the followinglight-sources (1) two 300 W light bulbs directed to the white ceil-ing in order to provide diffused illumination of the arena (lights ontest) (2) two infrared lights (Tracksys IR LED Illuminator UK)with 830 nm filters that emit light not visible to animals and areknown as lsquocovertrsquo IR (lights off test light level was 00425 lux asmeasured with Profisix SbcGossen) While we could not find infor-mation on spectral sensitivity in jirds in rats it is about 510 nm[34]which is well below the filters used here A video camera (IkegamiBW ICD-47E) was placed 25 m above the center of the arena pro-viding a top view of the arena and the tested jird The video signalwas recorded on a VCR (JVC HR-J737) In testing with lights onroom structure was visible to the jirds providing various landmarks(eg the location of monitor windows closet door etc) Duringtesting with lights off all light sources (eg all indicator lights inthe video camera air-conditioner etc) were sealed by opaque tapeand the room was entirely dark except for the invisible IR light

23 Procedure

Jirds were caged individually in 60 cmtimes 40 cmtimes 20 cm metalcages and brought to a room adjacent to the testing room 10 h beforetesting At this time the animals were gently painted over their rumpand back with a large black ink marker to increase the contrastof their image to the background and improve the video imageComparing the behavior of the ink-marked jirds with others thatwere unmarked revealed that they behave the same (preliminaryo adedw m toh imalw to thec withl ast inga ightso by ac ghtso t thee bitionc

2

taa ldquonotm eedl thisl renaw

by

by

-oveisodee jird

his structureAs shown below behavior in the dark revealed a dis

ive structure of diversified locomotion whose characteics might contribute to a better understanding of lesior drugged animals displaying diversified locomotor perance

Methods

1 Animals

Tristramrsquos jird (Meriones tristrami) is a nocturnal rodent of therbillidae family with the same morphology and size as the Molian gerbil (Meriones ungiuculatus) It is a burrow-dwelling roent that feeds on seeds and green vegetation[30] Observationere carried out on eight adult male jirds obtained from a caolony Jirds were housed in 120 cmtimes 63 cmtimes 45 cm metal cageocated outdoors in the yard of Tel-Aviv University research zooer natural (uncontrolled) temperature and light conditions O

urned ceramic pots and wooden boxes in each cage provided seeds and diced fresh vegetables were provided daily Yearserience in maintaining jirds in our zoo have shown that provisioater is unnecessary if sufficient fresh vegetables are providell times animals were maintained and treated in accordance

he guidelines for animal care and for the use of animals in resell the animals used in the study were in good physical condit

2 Apparatus

Open field (=arena) was a 180 cmtimes 180 cm enclosure wit0 cm high walls and a smooth beige PVC floor located in a

bservations in this study and work in progress) Ink stains fithin 24 h were not perceptible after 48 h and did not seearm the jirds or to alter their behavior in any way A test anas removed from the cage to a jar and then gently released inenter of the arena Each jird was first videotaped for 10 minights off (IR lights on) The next day the same individual jird wested again for another 10 min this time with lights on allow

comparison between light and dark tests Behavior with ln was not affected by the preceding dark testing as shownomparison with the behavior of jirds that were tested with lin but without the preceding dark testing (data not shown) And of testing animals were returned to the breeding and exhiolonies at the research zoo

4 Data acquisition and analyses

A tracking system (Ethovisionby Noldus NL) was used for dacquisition The tracking system was set to score the jird asovingrdquo (=stopping) when its center of gravity moved at a sp

ower than 2 cms or as ldquomovingrdquo when the speed exceededimit during tracking at a sampling rate of 125 framess The aas divided into 25 zones each comprising a 36 cmtimes 36 cm square

The following parameters were acquired via Ethovision

Total traveled distance (m) Overall metric distance traverseda jird during 10 min observationAverage traveling speed (ms) Total traveled distance dividedthe total traveling timeNumber duration and location of stops Incidence of nonlocomoting periods in which the jirdrsquos center of mass did not mmore than 2 cms The duration of each such stopping epwas also scored alongside the name of the zone in which thstopped








or











25 Statistics


3 Results


asesi ioral



oka edo ersa hts











Light Dark t7 p













two












Fig 6c)







4 Discussion





















-















Acknowledgements




References


e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation








-




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior






















or











25 Statistics


3 Results


asesi ioral



oka edo ersa hts











Light Dark t7 p













two












Fig 6c)







4 Discussion





















-















Acknowledgements




References


e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation








-




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior
















25 Statistics


3 Results


asesi ioral



oka edo ersa hts











Light Dark t7 p













two












Fig 6c)







4 Discussion





















-















Acknowledgements




References


e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation








-




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior

















Light Dark t7 p













two












Fig 6c)







4 Discussion





















-















Acknowledgements




References


e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation








-




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior
























Fig 6c)







4 Discussion





















-















Acknowledgements




References


e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation








-




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior





















4 Discussion





















-















Acknowledgements




References


e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation








-




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior































-















Acknowledgements




References


e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation








-




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior






















Acknowledgements




References


e-us

le offield

byRes

ntralrisk

f ro-ndash26

icey be-

rena

a

[ e ofssible

[211

[ tame

[ itsoperster

[ deadation








-




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior




























[ ent

[ rats

[ eadpatial

[ rael1999

[ a

[

[ nessrats











[ theravior

[ ex-kon-

[ iew

[ tantndash67

[ ratarch

[ vior















‘Looping’—an exploration mechanism in a dark open field

Documents

Transcript of ‘Looping’—an exploration mechanism in a dark open field