The Effects of Telencephalic Lesions on Visually Mediated Prey Orienting Behavior in the Leopard...

© 1998 S. KargerAG, Basel

E-Mail [email protected]+41 61 306 12 34 This article is also accessible online at:www.karger.com http://BioMedNet.com/karger

Paul PattonPaul Grobstein

Mercer University School of Medicine,Division of Basic Sciences, Macon, Ga., andDepartment of Biology,Bryn Mawr College, Bryn Mawr, Pa., USA

Original Paper

Brain Behav Evol 1998;51:123–143

Dr. Paul PattonMercer University School of Medicine, Division of Basic Sciences1550 College Street, Macon, GA 31207 (USA)Fax (912) 752 5489E-Mail [email protected]

Key WordsTelencephalonForebrainFrogVisual orienting behaviorOptic tectumSensorimotor control

AbstractIn this paper, we report studies aimed at characterizing the relationship betweenforebrain and midbrain systems involved in the control of prey orienting behav-ior in the leopard frog. In frogs, unilateral forebrain lesions, like unilateral tectallobe lesions, have their most prominent effects in the contralateral monocularvisual field. Such lesions produce partial reductions in response frequency inthe binocular visual field as well. Similar sequelae follow unilateral tectal loberemoval. These findings suggest that the effects of unilateral forebrain removalcan be largely attributed to removal of a facilitating influence on the tectal lobeon the same side of the brain. In the case of both forebrain and midbrain lesions,behavior was assayed not only in terms of the frequency with which animalsresponded to stimuli at various locations in the visual field (as is usually done)but also in terms of the latency of whatever responses were observed. A strikinginverse relationship between response frequency and response latency was found,both in lesioned and in normal frogs. This relationship has not previously beennoticed, doesn’t appear to be an obvious consequence of any existing models ofthe neuronal circuitry underlying anuran orienting behavior, and is difficult toaccount for in terms of the time scales associated with axonal conduction timesand synaptic delays. It may be easier to account for in terms of the responses toperturbation of large interacting systems of neurons, and this possibility seemsworthy of further exploration.oooooooooooooooooooo

Introduction

Visual processing in mammals is increasingly beingthought of in terms of dynamic interactions among a num-ber of more or less simultaneously active brain regions,rather than in terms of sequential information processingsteps carried out by a hierarchy of brain regions. Thoughcurrent attention is focused primarily on the interplay of a

number of isocortical regions, another significant aspect ofparallel processing in mammalian visual systems, whichwas recognized earlier, is related to the existence and inter-action of ‘two visual systems’: one centered in the isocortexand the other in the midbrain. Lesion studies indicate thatthe midbrain and forebrain visual systems may play com-plementary roles in visual behavior [Schneider, 1967, 1969]and that the function of the midbrain system is significantly

The Effects of TelencephalicLesions on Visually Mediated PreyOrienting Behavior in theLeopard Frog (Rana pipiens)I. The Effects of Complete Removal of One Telencephalic Lobe, with a

Comparison to the Effects of Unilateral Tectal Lobe Lesions

influenced by that of the forebrain [Sprague, 1966; Sher-man, 1977; Wallace et al., 1989, 1990].

Although research on visual processing in amphibianshas traditionally focused on the midbrain, there is substan-tial and increasing evidence that the forebrain also plays animportant role: neuroanatomical evidence in frogs [Ves-selkin et al., 1971; Halpern, 1972; Northcutt, 1972; Grubergand Ambros, 1974; Kicliter and Northcutt, 1975; Northcuttand Royce, 1975; Scalia, 1976; Kicliter, 1979; Ronan andNorthcutt, 1979; Vesselkin et al., 1980; Wilczynski andNorthcutt, 1983a; Neary, 1984] and salamanders [Kokorosand Northcutt, 1977; Wicht and Himstedt, 1986, 1988];electrophysiological evidence [Karamian et al., 1966; Ves-selkin et al., 1971; Liege and Galand, 1972; Gruberg andAmbros, 1974; Grusser and Grusser-Cornehls, 1976; Fin-kenstädt et al., 1986; Finkenstädt and Ewert, 1988; Finken-städt, 1989; Merkel-Harff and Ewert, 1991], and behavioralevidence [Ewert, 1970, 1980; Ingle, 1991]. It appears that

some form of the ‘two visual systems’ paradigm probablyapplies to amphibians as well as to mammals [Ingle, 1973,1983].

Prior work from our laboratory has focused on visuallytriggered orienting behavior in frogs and on the organiza-tion of the midbrain optic tectum and of subsequent infor-mation processing structures and events that underlie theassociated directed movements [Grobstein et al., 1980;Comer and Grobstein, 1981a, b; Kostyk and Grobstein,1982, 1987a–c; Masino and Grobstein, 1989a, b, 1990].Considerations having to do with the relationship betweenthe visual fields of the two eyes and the left and right be-havioral hemifields, defined relative to the midsagittalplane, have been central to this work. Frogs have frontallyplaced eyes with a large frontal binocular field (roughly 45°degrees to either side of the midsagittal plane). Since theretina of each eye projects only to the opposite tectal lobe,each tectal lobe represents the entire contralateral visualhemifield plus an additional 45° of the ipsilateral visualhemifield. The binocular visual field is represented twice:once in each tectal lobe [Grobstein et al., 1980; Kostyk andGrobstein, 1982, 1987a]. Correlated with this, we have pre-viously reported that unilateral tectal lobe lesions producean orienting deficit, not for stimuli throughout the entirecontralateral visual hemifield, but primarily for those atlocations more peripheral than 45° of eccentricity [Kostykand Grobstein, 1982, 1987a]. Unilateral lesions in the de-scending tectofugal pathways produce a true hemifielddeficit (i.e. one bordered by the midsagittal plane), thoughthis deficit relates to the ipsilateral rather than the contralat-eral visual field.

In this and the following paper, we report studies di-rected at determining how a forebrain visual system in theleopard frog might interact with the previously exploredtectal and tectofugal system. Unilateral forebrain lesions incats produce an orienting deficit in the contralateral hemi-field. The finding that this deficit can be relieved by any ofseveral subsequent midbrain lesions has led to the sugges-tion that the deficit results from destruction of a facilitatoryinfluence exerted by each forebrain lobe on the midbrainsystem on the same side of the brain [Sprague, 1966; Sher-man, 1974, 1977; Wallace et al., 1989, 1990]. Unilateralforebrain lesions in amphibians (toads [Ewert, 1970, 1980]and salamanders [Finkenstädt and Ewert, 1983]) producecontralateral orienting deficits. The orienting deficit whichfollows bilateral telencephalic removal in toads can be re-lieved by a subsequent pretectal lesion [Ewert, 1970, 1980].This suggests that a forebrain influence on the midbrain ori-enting circuitry, similar to that postulated for cats, may beat work in amphibians. Work on toads did not distinguish

124 Brain Behav Evol 1998;51:123–143 Patton/Grobstein

Abbreviation Key for Anatomy Figures

at anterior thalamic nucleusa nucleus accumbensal amygdala pars lateralisam amygdala pars medialism bed nucleus of the stria medullarisb bed nucleus of the pallial commissured nucleus of the diagonal band of Brocadp dorsal palliumds dorsal striatume anterior entopeduncular nucleuso posterior entopeduncular nucleush dorsal habenular nucleushv ventral habenular nucleuslp lateral palliumld lateral pallium pars dorsalislv lateral pallium pars ventralisls lateral septumg magnocellular preoptic nucleusmp medial palliumms medial septumnb nucleus of Belloncioc optic chiasmon optic nervep anterior preoptic areasc suprachiasmatic nucleusr ventrolateral thalamic nucleus, dorsal partl ventrolateral thalamic nucleus, ventral partn ventromedial thalamic nucleusvs ventral striatumv superficial ventral thalamic nucleus

between a true hemifield deficit and one restricted to moreeccentric visual field locations. In frogs, the latter would beexpected if each forebrain lobe exerted a facilitating influ-ence directly on the tectal lobe on the same side of thebrain. The studies reported in this paper were undertakenprimarily to determine whether this is so, and more gener-ally to determine how similar any observed forebrain deficitin frogs is to that following a unilateral tectal lesion. Ourinitial observations on the effects of forebrain lesions moti-vated a new study of the effects of unilateral tectal lesions,which is reported here as well.

In the case of forebrain and tectal lesions, we havestudied orienting behavior, not only in terms of responsefrequency but also in terms of response latency, for eachstimulus location. Our own prior work and that of otherinvestigators has focused primarily on the presence or ab-sence of responses, since these are the outcomes one ex-pects to follow partial damage to information processingsystems that have a predominantly hierarchical and sequen-tial character. For exploring what may well be parallel, in-teractive systems, a more neutral and broader set of expec-tations seems appropriate. Latency, in particular, seemedparticularly relevant for this study, since Fite and Hayden[1985] reported that lesions to the basal optic nucleus infrogs do not abolish orienting responses but do produce ob-servable increases in response latency.

Materials and Methods

Adult leopard frogs, Rana pipiens, were used as subjects. Theywere obtained from commercial suppliers and maintained on a diet ofmealworms (larval Tenebrio). All animals used in this research weremaintained and treated in accordance with guidelines developed bythe National Institutes of Health and the Society for Neuroscience.Frogs were pre-screened for behavioral responsiveness, and thoseresponding promptly and accurately to mealworms presented in thebinocular and monocular visual fields were accepted.

Methods for Lesioning the Telencephalon and Optic TectumFrogs were anesthetized by dorsal lymph sac injection of a 1% so-

lution of tricane methanesulfonate (MS222) and were blanketed withsurgical gauze wet with dilute MS222 and frog Ringer’s solution. Thearea to be lesioned was visualized with a dissecting microscope. Thetelencephalon was approached via a window cut in the dorsal surfaceof the skull. Lesions to the optic tectum were made using a similarskull window over the midbrain. All lesions were made using suctionaspiration. The skull flap was then replaced and the skin flap sutured.Frogs were allowed up to one week to recover from surgery prior tobehavioral testing.

Visual Perimetry TestingFrogs were tested using a standard visual perimetry test to deter-

mine the effects of the lesion on their ability to make orienting turnstowards stimuli at various locations in their visual field. This test was

described in Kostyk and Grobstein [1987a]. Briefly, in each trial, afrog was placed beneath a transparent plastic dome which was cen-tered and aligned with respect to the animal’s midsagittal plane, Meal-worms were then presented in one of a series of cups located aroundthe periphery of the dome. In the tests reported here, frogs were al-lowed two minutes to respond to this stimulus. If the frog made a turn-ing movement, the angular direction toward which it’s snout faced atthe end of the turn was recorded to the nearest half cup. The latencytime from the beginning of the stimulus presentation to the frog’smovement was measured using a stop watch. If the frog failed to turnwithin the two minute period, a ‘no response’ was logged. If it made amovement that was clearly unrelated to prey orienting, the trial was re-peated. A turning movement was scored as an accurate response if, atthe end of the movement, the frog’s snout faced within one cup (10.6°)to either side of the cup containing the mealworms. After surgery,formal behavioral testing was begun when the frog showed respon-siveness to mealworms. Each frog was tested daily if responsivenesspermitted. Testing was continued until enough data had been accumu-lated to fully characterize any deficit. This required about ten tests.

Quantitative Analysis of Perimetry DataBehavioral responsiveness to mealworms was assessed both by

cup and by visual field region. The visual field of the leopard frog wasdivided into four regions based on the midsagittal plane and on theboundaries of the binocular visual field: the monocular visual field onthe side contralateral to the lesion – CMF; the half of the binocularfield on the side contralateral to the lesion – CBF; the half of the binoc-ular field on the side ipsilateral to the lesion – IBF, and the monocularfield on the side ipsilateral to the lesion – IMF. In unlesioned frogs, theanalogous visual field regions were designated with respect to thefrog’s left and right sides (i.e. LMF, LBF, RBF, and RMF). For eachcup and region, the total numbers of trials, of turning movements, andof accurately directed responses (see previous section) observed weredetermined. From these values the frequency of accurate responsesand the frequency of all turning movements were computed for eachcup and region. Accurate response latencies were also analyzed. Foreach frog tested, the mean and the standard deviation of the accurateresponse latencies were computed for each visual field region. Thepopulation mean and standard deviation of the accurate responsefrequencies and accurate response latencies were computed for eachvisual field region for each of the three populations of frogs studied:normal, unilateral telencephalic lobe removal, and unilateral tectal re-moval. Statistical comparisons were made between the regions usingthe Student’s t test. Wherever use of the t test is indicated, a 5% sig-nificance level was used. The t value, number of degrees of freedomdf, and significance p are reported.

Anatomical Determination of the Extent of the LesionFollowing behavioral testing, frogs were sacrificed under tricane

methanesulfonate (MS222) anesthesia, and lesion extent was deter-mined anatomically. The frogs were perfused through the heart with asolution of 0.01% MS222 in frog Ringer’s solution and fixed by injec-tion of Bouin’s solution. The head was removed and placed in Bouin’ssolution overnight. The next day, the brain was removed and replacedinto Bouin’s solution for another night. Each brain was then rinsed ina saturated solution of lithium carbonate in 70% alcohol until free ofBouin’s and was stored in 70% alcohol. After dehydration in alcoholand clearing in methyl salicylate, brains were embedded in paraffinand sectioned into 20 µm transverse sections. The sections wereplaced onto albumen coated slides and stained using cresyl violet.

125Frog Telencephalon and Visual Orienting I Brain Behav Evol 1998;51:123–143


Fig. 1. The visual prey orienting behav-ior observed in a normal leopard frog (#121)during ten behavioral tests. Angular locationin the frog’s visual field are as indicated in thecircular diagram at the top, where the circle iscentered about a point midway between thefrog’s eyes, and the dotted lines indicate theextent of the binocular visual field. In thegraph, the abscissa indicates the angular loca-tion of the stimulus, and the ordinate indi-cates the pointing direction of the frog’s snoutfollowing an orienting turn. The outcome ofeach trial is indicated by a dot. In cases wheremore than three trials at the same stimuluslocation produced the same outcome, thenumber of turns observed is indicated by anumeral. In cases where the frog failed toexecute a turn during the two minute durationof the trial, the trial is indicated by a dot ornumeral placed at the bottom of the graph inthe grey area.

Fig. 2. The results of the same ten behav-ioral tests of a normal leopard frog (#121) asin figure 1 shown in terms of the percentageof all trials on which accurate responses wereobtained for each stimulus location tested.The abscissa represents the angular locationof the stimulus as described for figure 1.

The completed slide set was examined, and the extent of the lesionwas determined for each frog. For telencephalon lesioned animals,this determination was made by plotting the lesion onto standardanatomical templates. The template drawings were made at 80 µm in-tervals in the telencephalon and at 40 µm intervals in the rostral dien-cephalon. Structures were identified using the atlases of Kicliter andEbbesson [1976] and Northcutt and Kicliter [1980] for the telen-cephalon, and Neary and Northcutt [1983] for the diencephalon.

The extent of tectal lesions was determined by examining a se-quence of tectal transverse sections and noting the presence and loca-tion of any remaining tectal tissue on the lesioned side.

A quantitative estimate of the amount of tectum removed wasmade. Transverse sections through the tectum of an unlesioned frogwere examined, and layer 8 of Székely and Lázár [1976] was identi-fied. At four section (80 µm) intervals, beginning with the most rostralsection in which layer 8 was visible, the tectum was drawn using a


Fig. 3. The visually mediated prey ori-enting behavior of each of the normal leopardfrogs tested in the standard perimetry test. Foreach frog, the percentage of stimulus trials onwhich accurate responses were obtained is in-dicated for each of four visual field regions asdefined in Materials and Methods. The frogsare presented in order of accurate responsive-ness, from greatest to least, for stimuli pre-sented in the LMF. The designations of theindividual frogs are given on the abscissa ofeach group.

Fig. 4. The accurate turning movementlatencies of a normal frog as a function ofstimulus location. The data used were de-rived from the same ten behavioral tests ofthe same frog (#121) as in figures 1 and 2.Each + indicates the latency time observed orone particular trial in which the frog made anaccurately directed orienting turn. The linelabeled ‘Mean lat’ indicates the mean of thelatency distribution for each stimulus loca-tion tested.

projection tube. Layer 8 was indicated by an arc on each drawing. Asa measure of the extent of the tectum at each level, the length of thisarc was measured using a map reader. A template was generated con-sisting of a series of parallel lines, with each line representing thelength of the layer 8 arc in one measured section. Sections at compa-rable rostrocaudal levels to the template sections were identified foreach lesioned frog, and the fraction of the layer 8 arc judged missingin each section was marked on the template lines. The total length ofthe template lines T was used as a measure of the extent of the tectum.The total unmarked extent of the lines t gives a measure of the extentof the tectum surviving the lesion for each animal. The percentage ofsurviving tectum was computed using these figures.

Results

The behavior of normal frogs and that of frogs followingunilateral removal of the telencephalon or of the optic tec-tum are reported here.

Visual Prey Orienting Behavior in Normal FrogsThe behavior of 7 normal frogs was studied using the

standard visual perimetry test (see Materials and Methods).Frequency of Prey Orienting Movements. The prey ori-

enting behavior of a representative normal frog (frog #121),for each stimulus location tested, is illustrated in figure 1.Note that although most of the turning movements are ac-curately directed, a few inaccurate movements do occur.These may be stimulus triggered but inaccurate turns or

spontaneous movements unrelated to the stimulus. Trials onwhich the frog failed to respond are rare.

Figure 2 represents the same behavioral data re-illus-trated in terms of accurate response frequency at each stim-ulus location. Accurate responses occurred on 80% or moreof all trials for each stimulus location tested and, in all buttwo positions, on 90% or more of all trials. For the remain-ing trials, frogs generally turned inaccurately, rather thanfailed to turn, since turning movements were observed foralmost all stimulus presentation trials.

Figure 3 summarizes the behavior of each normal frogthat was tested in terms of accurate response frequency foreach of the four field regions (see Materials and Methods).It shows that most of the normal animals tested behavedsimilarly to the representative normal frog (#121) of figure2. None show a systematic difference in accurate responsefrequency between the binocular visual field and the mon-ocular fields. Note, however, that normal frogs do varyfairly dramatically in their overall level of responsiveness.

Accurate Response Latencies. The observed populationof accurate response latencies for a representative normalfrog (#121 – same animal as fig.2), for each stimulus loca-tion tested, is represented in figure 4. The figure shows thatthis frog tended to respond promptly when presented with amealworm in any part of its visual field. There is no obvi-ous difference between the latencies generally observed inthe binocular visual field and those observed in the monoc-


Fig. 5. The behavior, with respect to re-sponse latency, of each of the normal leopardfrogs tested in this study. The mean accurateturn latency for all of the accurately directedorienting turns observed in each of four vi-sual field regions (see Materials and Meth-ods) is indicated for each frog. The standarddeviation for each mean value is indicated bythe error bar associated with each column. Incases where the frog made an accurate orient-ing turn on fewer than five occasions for stim-uli presented in a particular visual field re-gion, a mean latency was not computed, andno column is shown. The designations of thetested frogs are given on the abscissa.

ular fields. The animal showed at least one turn latency ofless than three seconds for each stimulus location tested. Thelongest latencies noted in this animal were under 40 seconds.In several of the normal frogs, latencies tended to clusterabout a short value. The shortest accurate response latenciesobserved in the normal frogs tested were one second or less.The longest observed latencies were for accurate responsesat the end of the 2-minute trial period. Accurate responselatencies were most commonly less than 10 seconds.

The mean and standard deviation of the latencies foreach visual field region of each normal frog tested are dis-played in figure 5. The figure shows no apparent systematicdifference between mean latencies in the binocular and themonocular visual fields. As with accurate response fre-quency, however, there is a notable variation between frogsin accurate response latency. The two frogs exhibiting thelongest regional mean latencies also exhibited the lowestaccurate response frequencies. This suggests a correlationbetween accurate response frequency and latency.

Effects of Unilateral Telencephalic Lobe RemovalUnilateral telencephalon removals were performed in a

total of 43 frogs. This surgery proved very traumatic to theanimals. Nineteen (44%) died during or after surgery. Six-teen (37%) were behaviorally unresponsive or erraticallyresponsive following surgery and could not be tested. Eightanimals (19%) were sufficiently responsive to prey itemsfollowing surgery for their orienting responses to be char-acterized using the standard perimetry test.

The Extent of the Lesion in Behaving Animals. In alleight frogs studied, detectable damage was confined to oneside of the brain, and all or almost all of the lesioned telen-cephalic lobe was removed. A typical lesion is illustrated infigure 6 (frog U#28B). In this animal, a small amount of te-lencephalic tissue on the lesioned side survived. Differentlylocated small areas of surviving tissue occurred in five ad-ditional animals. In three animals (frogs U#1P, U#1B, andU#5), no trace of the removed lobe remained. The lesionsalso showed a varying degree of incursion into the dien-cephalon. Frogs U#10, U#16, and U#28B showed the leastdegree of damage, with any observable diencephalic inva-sion confined solely to the far rostral white matter. FrogsU#1B, U#1P, U#3, and U#5 showed a somewhat greaterdegree of damage, with some noticeable invasion of dien-cephalic gray matter, as well as white matter, present. Thelargest invasion of the diencephalon was that exhibited byfrog U#25. In this animal, the damage clearly extends intothe region of the retinorecipient thalamic neuropil and itsunderlying grey matter structures, as these are depicted byScalia [1976].


Fig. 6. A series of representative transverse sections through thetelencephalon of a leopard frog. The crosshatched area indicates thearea removed in a typical unilateral forebrain removal lesion. The le-sion shown is that of frog U#28B, whose behavior is represented infigures 9 and 11. To create this figure, the frog’s lesion was first plot-ted onto a standard anatomical template series. A subset of these sec-tions was chosen for display in this figure. Anatomical abbreviationsare as given in the Abbreviation Key for Anatomy Figures.


Fig. 7. The prey orienting behavior of aleopard frog (frog U#5) as observed in 17 be-havioral tests following unilateral removal ofthe telencephalon. The tests were conductedbetween 10 and 84 days after the lesion. Theconventions are as described for figure 1.

Fig. 8. The behavioral data of figure 7are rerepresented in terms of the percentageof all trials in which accurate responses wereobtained for each stimulus location tested.The conventions are as described for figure 2.

Frequency of Prey Orienting Movements. Following uni-lateral removal of the telencephalon, frogs showed a clearcontralateral deficit in visual prey orienting. The behavior ofa typical animal (U#5) is shown in figures 7 and 8. The fig-ures summarize the results of seventeen tests made within 84days after lesioning. Note that accurate responses are fre-

quent in the IMF and persist through both halves of thebinocular field also. Only in the CMF are accurate responsesvirtually absent. The effects of the lesion are not entirelyconfined to the CMF. The percentage of trials on which ac-curate responses were elicited is also substantially reduced inthe binocular visual field measured relative to the IMF.


Fig. 9. The visually mediated prey ori-enting behavior of each unilateral telen-cephalon removal leopard frog successfullytested. Conventions are as described for fig-ure 3. The frogs are presented in order of theseverity of their deficit, as determined by ac-curate response frequency in the CMF.

Fig. 10. The accurate response latenciesof a typical unilateral telencephalon removalleopard frog (U#5) as a function of stimuluslocation. The data used were derived from thesame seventeen behavioral tests as figures 7and 8. Conventions used are as described forfigure 4.

Figure 9 displays the accurate response frequency foreach visual field region of each unilateral telencephalon re-moval frog tested. In all cases the data are derived fromtests made within 90 days after surgery. All showed a se-vere behavioral deficit for stimuli presented in the CMF,with accurate responses made on less than 10% of all trialsin all frogs. In the figure, the frogs are presented in order ofthe severity of this deficit. The contralateral deficit exhib-ited by frogs with little apparent diencephalic damage is noless severe than for those where significant damage wasnoted. In fact, the three frogs showing least diencephalic in-vasion exhibited the most severe deficits, with no accurateresponses in their CMFs. All five frogs in which the dien-cephalic gray matter was invaded showed a few such accu-rately directed turns. All but one of the tested frogs madeaccurate or inaccurate turns less than 25% of the time dur-ing CMF stimulus presentations. The deficit is thus due pri-marily to a reduction in the frequency of triggered move-ments rather than simply to a reduction in accuracy. Thesole exception, frog U#25, exhibits an anomalous lesion asdiscussed above. Although the tendency to make turns dur-ing contralateral monocular stimulus presentations wasonly pronounced in the case of frog U#25, all of the otherfrogs did exhibit a few turns during such trials.

In addition to a severe decline in the frequency of accu-rate orienting responses in the CMF, a lesser reduction inthe frequency of accurate turns in the binocular visual fieldis also a general feature of the unilateral telencephalon re-moval deficit. In seven of the eight frogs studied, the per-centage of trials on which accurate responses were elicitedwas reduced in both binocular field halves relative to thatobserved in the IMF (fig.9). The population mean accurateresponse frequency for the binocular visual field was sig-nificantly reduced below that of the IMF of unilateral tel-encephalon removal frogs (t=2.6, df=14, p=0.024) andthe binocular visual field of normal frogs (t=–2.6, df=13,p=0.021). In six of the eight frogs, accurate response fre-quency was lower for stimulus presentations in the CBFthan in the IBF.

In all cases, the reduction in accurate response frequencyin the binocular visual fields of unilateral telencephalonremoval frogs is due primarily to a reduction in the over-all frequency of turning movements rather than to a ten-dency to turn inaccurately. In four animals, the percentageof all turns that were accurately directed at the stimulus re-mained above 90% for both halves of the binocular visualfield. In the other four, however, this percentage declinedbelow 70% for at least one binocular field half, an thus atendency to turn inaccurately may play a small role in thedeficit.

In seven of the eight frogs, accurate response frequen-cies reached their highest level in the IMF. Although theeffect does not reach the level of statistical significance, itshould be noted that accurate response frequencies as highas those observed in the monocular fields of the most re-sponsive normal frogs were not seen in the IMFs of unilat-eral telencephalon removal frogs. Only one of these eightanimals turned accurately in response to more than 80% ofall prey stimuli presented in the IMF (fig.9). Five of theseven normal frogs showed this level of performance intheir right monocular fields. This difference raises the pos-sibility of a slight behavioral effect of the lesion for stimulipresented in the IMF.

Recovery from the Deficit with Time. In seven of theeight frogs, responsiveness had returned sufficiently tobegin formal testing between 7 and 17 days after surgery.One frog (U#1P) was too unresponsive to begin testinguntil 59 days after surgery. In four animals, testing wascompleted within 40 days after surgery. Each showed a se-vere contralateral orienting deficit. In the other four, behav-ioral testing was continued until 98 days (U#3), 118 days(U#5), 123 days (U#1P), and 282 days (U#1B). The firsttwo animals showed no significant evidence for recoveryfrom the deficit. Frog #1B, however, did show clear evi-dence of recovery in its last testing series, conducted be-tween 153 and 282 days after surgery. In this series 38% ofall stimulus presentations in the CMF prompted an accurateturn, whereas less than 5% did so in the initial series. Thisimprovement is statistically significant (t=–6.4, df=34,p=0.000). The data suggest a partial recovery from thedeficit by about seven months after surgery.

Accurate Response Latencies. Accurate response laten-cies in a typical frog (U#5) following unilateral removal ofthe telencephalon are presented in figure 10. For all visualfield locations, this frog’s turn latencies are longer and morewidely scattered than those observed in most normal frogs.The tendency of latencies to cluster about a short value,which is observed in the more responsive normal frogs, isabsent in this animal and in all of the unilateral telen-cephalon removal frogs studied. Note also that more longlatency accurate turns are present in the binocular visualfield than in the IMF. This tendency towards increased la-tencies corresponds to the depression in accurate responsefrequency also (see fig.8) observed for stimuli presented inthis area.

The mean and standard deviation of the latencies wascomputed for each visual field region where more than fiveaccurately directed turns were observed for each of theeight frogs tested. Figure 11 shows that in many testedfrogs accurate response latency is clearly affected by uni-



Fig. 11. The behavior, with respect toresponse latency, of each unilateral telen-cephalon removal leopard frog successfullytested. The mean latency for all of the accu-rately directed orienting turns observed ineach of four visual field regions is shown foreach frog. Conventions are as described forfigure 5. CMF values are not shown, because,in each case, fewer than five responses wereobtained.

Fig. 12. The visual prey orienting behav-ior observed for stimulus presentations invarious parts of the visual field for a leopardfrog (T#118) from which one tectal lobe hasbeen removed. The data were obtained in atotal of 20 behavioral tests, conducted be-tween 12 and 24 days after lesioning. Con-ventions used are as described for figure 1.

lateral removal of the telencephalon. Mean accurate re-sponse latencies tend to be longer than those observed innormal frogs. For all four visual field regions, the popula-tion regional mean latencies are significantly longer for uni-lateral telencephalon removal frogs than for normal frogs.More importantly, mean accurate response latencies forstimuli in the binocular visual field tend to be longer than inthe IMF. In all five frogs where adequate data were ob-tained, mean accurate response latency is longer in bothbinocular field halves than in the IMF. In four of these five,the mean turn latency is greater in the CBF than in the IBF.The mean accurate response latency for the population ofunilateral telencephalon removal frogs in the binocular vi-sual field is significantly greater than that observed in theIMF (t= —6.4, p=0.000). Mean accurate response latencythus varies as a function of visual field location in a fashionthat corresponds to the observed variation in accurate re-sponse frequency in unilateral telencephalon removal frogs.

Effects of Unilateral Tectal Lobe RemovalTests of visual orienting behavior were conducted in 12

frogs, following unilateral removal of the optic tectum, forthe purpose of comparison with the effects of unilateral tel-encephalon removal.

The Extent of Tectal Lobe Removal in Behaving Frogs.The extent of each lesion was determined by examinationof transverse sections through the tectum. In six frogs,T#113, T#118, T#120, T#121, T#122, T#123, and T#128,all traces of the tectum on the lesioned side were removed.In two animals, T#124 and T#129, extremely small piecesof the lateral rim of the tectum on the lesioned side survivedthe surgery. In the remaining three frogs, T#125, T#126,and T#127, somewhat larger portions of the lateral rimsurvived the surgery. In no case did more than about 11%of the tectal lobe survive the lesion. Small differences inlesion size had no obvious correlates in behavior.

Frequency of Prey Orienting Movements. Each frog thatwas successfully tested following unilateral removal of theoptic tectum exhibited a clear contralateral deficit in visu-ally mediated orienting behavior. Figures 12 and 13 repre-sent the results of 19 behavioral tests made between 12 and24 days after lesioning in a typical case (T#118). Theseshow that leopard frogs exhibit an ability to make accu-rately directed orienting turns for stimuli placed in theirIMF (right) and IBF, as well as most of their CBF. Accurateturns are virtually absent in the CMF.

The orienting behavior of each unilateral tectal removalfrog tested is shown in figure 14. All data were derivedfrom tests made less than 40 days after surgery. The frogsare presented in the order of the severity of their CMF

deficit. In all cases, the deficit was severe, with accuratelydirected turns occurring on less than 10% of all trials inthis region for all but one frog. This is comparable to theseverity of the contralateral monocular deficit exhibited byunilateral telencephalon removal frogs. There is no notice-able difference between the severity of the deficit of frogsin which the tectal lobe was fully removed (T#113, T#118,T#120, T#121, T#122, T#123, and T#128) and those inwhich some tectal tissue survived the lesion (T#124,T#125, T#126, T#127, and T#129).

The CMF deficit exhibited by the unilateral tectal re-moval frogs tested is largely attributable to a decline in thefrequency with which the stimulus triggers turning move-ments. More inaccurately directed turns, however, weregenerally observed to occur during contralateral monoculartrials in unilateral tectal removal frogs than in unilateraltelencephalon removal frogs. Half of the tectal removalanimals turned during more than 40% of all contralateralmonocular trials. In general, as can be seen for frog T#118in figure 12, the majority of these turns tend to be directedinto the hemifield containing the stimulus. Most of theseturns were not accurately directed at the stimulus. In fivefrogs, however, more than 20% of them were. Four of thesefive animals were ones in which the tectal lobe was fullyremoved.

To determine whether this behavior indicates a residualcapacity for stimulus triggered orienting movements, sixunilateral tectal removal frogs were tested in a series ofsham trials where the prey stimulus was omitted. The num-ber of turns occurring during the sham trials was, in allcases, quite sizable. The mean turn frequency obtained forthe six frogs during sham trials was not significantly differ-ent from that obtained when a CMF stimulus was present(t=0.8, df=10, p=0.465). The mean percentage of turnsdirected into the contralateral hemifield during sham trialswas not significantly different from that obtained for thesame animals when a stimulus was present (t=1.1, df=10,p=0.279). Thus, the turning movements observed duringCMF stimulus presentations in these frogs are likely to bedue to a spontaneous tendency to turn into the contralateralhemifield rather than to a residual capacity to respond tosuch stimuli.

Figure 14 shows that in the CBF, accurate response fre-quency was reduced over that observed in the IMF ineleven of the twelve frogs tested. In the IBF, 7 of the 12frogs showed such a reduction, although in some cases thereduction is not large. When the binocular field is consid-ered as a whole, the reduction in the population mean accu-rate response frequency for this region, with respect to theIMF, does not quite reach the level of statistical significance


(t=1.4, df=22, p=0.172). When the population mean re-sponse frequency for the two visual field halves is com-puted separately, however, the reduction in the CBF is sta-tistically significant (t=8.0, df=22, p=0.000). A reductionin accurate response frequency in at least a portion of thebinocular visual field is thus a general feature of the behav-ior of unilateral tectal removal frogs. This reduction is gen-erally a product of both a decrease in the percentage of tri-

als on which turning movements occurred and a reductionin the fraction of such movements that were accurately di-rected.

Seven of the twelve unilateral tectal removal frogs stud-ied show their highest accurate response frequencies forstimuli presented in the IMF. In this respect, the frogs re-semble unilateral telencephalon removal frogs. The IMFaccurate response frequencies of both these groups of ani-


Fig. 13. The behavioral data of figure 12,replotted in terms of the percentage of trialson which accurate responses were observedfor each stimulus location tested. The plot-ting conventions used are as given in figure 2.

Fig. 14. The visual prey orienting behav-ior of each member of the entire group ofleopard frogs that were tested following uni-lateral removal of the optic tectum. The frogsare presented in the order of the severity oftheir deficit as determined by CMF accurateresponse frequency. The conventions of theseplots are otherwise as given for figure 3.

mals are generally similar to those seen in the monocularfields of normal frogs. The population mean accurate re-sponse frequency for trials in this region for unilateral tec-tal removal frogs does not differ significantly from thatobtained for the right monocular fields of normal frogs(t=–0.7, df=17, p=0.481). Unlike unilateral telencephalonremoval frogs, however, the population includes five ani-mals (of the twelve tested) that turned accurately for 90%or more of the stimuli presented in this region. This sub-population was not particularly distinctive in terms of theextents of its members’ lesions. It included three of the sixfrogs in which the tectum was totally removed and two inwhich small portions of the lateral rim of the tectum sur-vived.

Time Course of Testing and Deficit Properties. Unilat-eral tectal removal frogs were responsive enough for testing1 to 6 days after surgery. In all 12 cases, behavioral testingwas completed by 37 days after surgery. To facilitate com-parison with unilateral telencephalon removal frogs, whichwere tested on a somewhat longer time scale, three tectal le-sioned frogs were retested from 65 to 81 days after surgery.The basic characteristics of the deficit, including a severedecline in accurate responsiveness for CMF stimuli and alesser decline for the CBF, remained essentially the sameduring the second test series as in the first. Valid compar-isons can thus be made between unilateral tectal removaldata collected up to 37 days after lesioning and unilateraltelencephalon removal data collected up to 90 days afterlesioning.

Accurate Response Latencies. Figure 15 shows that, fora representative frog (T#118), accurate response latenciesare affected by unilateral removal of the optic tectum. La-tencies in the binocular field are longer and more widelyscattered than in the IMF. In the IMF, latencies tends tocluster about a short value, just as they do for the entire vi-sual fields of the more responsive normal frogs.

For each tectal lobe removal frog tested, the mean andthe standard deviation of the accurate turn latencies werecomputed for each visual field region where more than fiveaccurate turns occurred (fig.16). A clear response latencydeficit occurs in most animals tested. In eight of the elevenfrogs for which data were available, the mean latencies inboth binocular field halves were longer than those in theIMF. In ten of the eleven, the mean latency was longer inthe CBF than in the IMF. For all four visual field regions,population mean accurate turn latency is increased overthat observed in the corresponding regions of normal frogs.The population mean accurate turn latency computed forthe binocular field is also significantly (t=–6.2, p=0.000)greater than that for the IMF. The lengthening of mean la-

tencies in the binocular field is additional evidence that thetectal lobe removal deficit is not confined to the CMF. Asin unilateral telencephalon removal frogs, a coordinateddecrease in accurate response frequencies and increase inmean latencies occurs in the binocular visual field of unilat-eral tectal removal frogs.

Discussion

Unilateral telencephalon removal in the leopard frog re-sults in a contralateral visual prey orienting deficit. Here wecompare the behavior of unilateral telencephalon removalfrogs with that of normal frogs and that of frogs from whichone lobe of the optic tectum was removed. The results arecompared with similar findings in mammals, and the signif-icance of the observed alteration in response latencies isconsidered.

The Visual Orienting Behavior of Normal FrogsThe prey capture behavior of normal anurans has been

described by many past workers [Ingle, 1968, 1970; Ewert,1970; Comer and Grobstein, 1981b; Ewert et al., 1981;Kostyk and Grobstein, 1982, 1987a]. Our findings confirmpast reports [Kostyk and Grobstein, 1982, 1987a] that nor-mal Rana pipiens can make orienting turns to visual stimuliat locations throughout a full 360 degrees around the ani-mal in the horizontal plane. They show, as well, that thereis no obvious systematic variation in the frequency of accu-rate turns with changes in visual field location in normalfrogs. Normal frogs were found to vary substantially fromone another in their overall response frequency to preystimuli. It should be pointed out that the reported results donot encompass the full range of this variation, since frogswere pre-screened for responsiveness to prey, and unre-sponsive animals were excluded from the sample. Fite andHayden [1985] reported that the mean of the three shortestresponse latencies observed for each of a series of visualfield locations, similarly does not vary systematically withvisual field location. Our findings are consistent with thisand show more generally that the entire distribution ofresponse latencies is, like response frequency, largely orentirely independent of visual field location. At any givenlocation, latency distributions tend to be skewed, with mostresponses as ten to twenty seconds or less and a tail oflonger latency responses.

In addition to providing a baseline against which to de-scribe the effects of lesions, our observations on normalfrogs are of some interest in their own right. Each tectallobe of the leopard frog contains a complete representation


of the visual field of the contralateral eye. The binocular vi-sual field is thus distinct from the monocular fields not onlyin that it is seen by both eyes but also in that it is repre-sented twice, once in each tectal lobe [Grobstein et al.,1980]. The lack of significant differences between responsefrequencies and latencies in binocular as opposed to mono-cular fields indicates that neither the fact of binocular vision

nor the double representation of binocular field in the tec-tum has any dramatic significance for these aspects of ori-enting behavior.

The motor patterns used by frogs in orienting to preystimuli vary with the angular location of the stimulus. Formore frontally located stimuli, frogs characteristically re-spond with a directed head movement, without moving


Fig. 15. The accurate orienting turn la-tencies for stimulus presentations in variousportions of the visual field of a typical leopardfrog (T#118) following unilateral removal ofthe optic tectum. The data were collected aspart of the same 20 behavioral tests as figures12 and 13. Conventions are as described forfigure 4.

Fig. 16. The behavior, with respect to ac-curate turning movement latency, of eachunilateral optic tectum removal leopard frogtested. The conventions used are as describedfor figure 5.

their limbs. For increasingly eccentric stimuli, the move-ment patterns change to involve, first, more involvementof the forelimbs and then stepping sequences involvingall four limbs [Comer and Grobstein, 1981b; Grobstein,1990a]. In this regard too, it is noteworthy that there is nosystematic variation in response frequency or latency withstimulus location. The processes involved in the selectionof particular motor patterns are apparently also not tightlycoupled to those determining response frequency and la-tency.

Effects of Unilateral Forebrain LesionsFollowing unilateral removal of the telencephalon, eight

frogs were sufficiently responsive to prey stimuli to un-dergo formal perimetry testing for characterization of theirorienting deficit. An additional sixteen animals survived thelesion but were too unresponsive for formal testing. The re-duced responsiveness of these animals cannot be due to theremoval of circuitry necessary for orienting behavior, sincethe remaining frogs, after similar lesions, continued to re-spond appropriately for stimulus presentations over signifi-cant portions of their visual fields. It seems likely, instead,to be due to some more general factor, such as the state ofhealth of the animal. Even normal unlesioned frogs exhibitperiods when they are not sufficiently responsive for test-ing. The reasons for this are poorly understood but may in-volve a wide variety of factors, such as the state of healthand reproductive state of the animal in question. Full re-moval of one telencephalic lobe is apparently quite trau-matic, since it resulted in the death of nearly half of the op-erated animals. It thus seems likely to have had a majorimpact on the state of health of the survivors. For this rea-son only the eight testable animals will be considered incharacterizing the deficit.

Clear structured disturbances in orienting behavior wereobserved in all tested animals subjected to unilateral fore-brain lesions. While these lesions were intended to sparethe thalamus, and, in particular, anterior thalamic regionsthat receive both retinal and tectal input [Scalia, 1976],there were inevitable varying incursions into the thalamusin many of the animals studied. We are nonetheless quiteconfident that the behavior disturbances described resultedfrom forebrain rather than thalamic damage. We observedno correlation between the degree of observed incursioninto thalamus and the severity of the behavioral deficit. Fur-thermore, Kicliter [1973] has reported that large bilaterallesions of the anterior thalamus do not affect the ability offrogs to respond to visually presented prey items. Finally,in an accompanying study [Patton and Grobstein, 1997],we report that small lesions restricted to the ventromedial

region of one telencephalic lobe are sufficient to produce adeficit which closely resembles that in the animals de-scribed here.

Ewert [1970, 1980] was the first to study orienting be-havior following unilateral forebrain lesions in amphibians,reporting contralateral orienting deficits in the toad Bufobufo. Finkenstädt and Ewert [1983] described similar re-sults for the salamander Salamandra salamandra. Our find-ings that a contralateral orienting deficit likewise occursfollowing unilateral forebrain removal in Rana pipiens con-firms this finding for this species and adds important detailsabout the spatial extent of the deficit not available from ear-lier studies.

A primary concern of our studies was to determinewhether unilateral forebrain lesions yielded a hemifielddeficit bordered by the midsagittal plane or a more limiteddeficit restricted to the contralateral monocular visual field.Our findings clearly favor the latter characterization overthe former but with some unanticipated complexities. In alltested animals, there was a profound and consistent loss ofaccurate orienting responses, not over the entire contralat-eral hemifield, but rather in a more restricted region corre-sponding to the contralateral monocular field. In addition,however, we observed a significant but less dramatic reduc-tion in orienting responses in the binocular visual field(usually greater in the contralateral than in the ipsilateralhalf) relative to the ipsilateral monocular field. A smallreduction in response frequencies in the ipsilateral monoc-ular field, relative to normal frogs, was also noted. Thesereduced response frequencies were accompanied by in-creased response latencies.

It is clear from our findings, as from those of earlierworkers, that the forebrain plays a role in visual orientingbehavior in amphibians, as it does in mammals. Ewert[1970, 1980] showed that toads do not respond to preyitems after bilateral removal of the forebrain but that thisdeficit could be relieved by additional pretectal lesions.This suggests that in amphibians, as in mammals [Sprague,1966; Sherman, 1974, 1977; Wallace et al., 1989, 1990],the forebrain is not essential for visual orienting behaviorbut does exert an important modulating influence on mid-brain or subsequent circuitry adequate to support such be-haviors. Though we have no direct evidence on this point,we presume this generalization holds for frogs and take theobserved orienting deficits as evidence for a loss of somefacilitatory influence of the forebrain on midbrain or subse-quent circuitry.

Two types of visual orienting deficits have been de-scribed in previous work on the organization of midbrainand descending circuitry in frogs. Unilateral removal of the


optic tectum [Ingle, 1973; Kostyk and Grobstein, 1982,1987a] produces a contralateral orienting deficit most se-vere in the contralateral monocular visual field. Unilateralinterruption of descending tectofugal pathways produces ahemifield deficit in the ipsilateral visual field. Both in theirlaterality and in their extent, the forebrain deficits describedhere most closely resemble those resulting from unilateraltectal lesions, and it thus seems reasonable to suggest thatthey result from the loss of a facilitating influence of onelobe of the forebrain on the tectal lobe on the same side ofthe brain, or at least at some point prior to a change in or-ganization evident in the tectofugal pathways. The deficitfollowing unilateral forebrain lesions does, however, pos-sess some additional characteristics that have not previ-ously been emphasized or noted in studies of tectal lobelesions. These include a reduction in response frequency inthe binocular visual field and, to a lesser extent, in the ipsi-lateral monocular visual field as well. They also includeincreases in response latencies in these two regions. Theeffects of unilateral tectal lesions were restudied in order todetermine whether or not these features were also charac-teristic of such lesions.

Effects of Tectal Lobe Lesions and Their Implicationsfor Understanding Forebrain LesionsPrior work [Ingle, 1973; Kostyk and Grobstein, 1982,

1987a] on unilateral tectal lobe lesions in Rana pipiens hasfocused largely on the question of their effects on the exis-tence and accuracy of orienting turns made to stimuli atdifferent locations in the visual field. Our current findingsare entirely consistent with this work in indicating that ac-curate turns persist not only in the ipsilateral hemifield butthroughout the entirety of the binocular field as well andare abolished only in the contralateral monocular field.Earlier studies did not involve large enough numbers ofstimulus trials to address the question of variation in re-sponse frequency as a function of stimulus location. Wehave shown here that a reduction in response frequency forstimuli presented in the binocular field is characteristic ofthe behavior of animals with unilateral tectal lobe lesionsjust as it is for animals with unilateral forebrain lesions.This implies that while the dual tectal representation of thebinocular field is irrelevant for considerations of responseaccuracy, it is more significant for considerations of re-sponse frequency. We are less certain about relations be-tween the two sets of lesions with regard to reduction of re-sponse frequencies in the ipsilateral monocular field. Thedata in this regard are quite variable, but they seem to sug-gest a greater reduction in the case of forebrain as opposedto tectal lesions.

Prior studies on unilateral tectal lobe lesions did notinclude consideration of response latencies. Our findingsclearly show that the reduced response frequency in thebinocular visual field that is produced by unilateral tec-tal lobe lesions is accompanied by an increase in averageresponse latency in the same visual field region. The in-creased response latency in the binocular field is evidentfrom comparison with normal animals as well as in com-parisons of latencies in the binocular field with those in theipsilateral monocular field in normal animals. The latter isone of several pieces of evidence in our observations thatindicate a general correlation between response frequencyand response latency, the significance of which is dis-cussed further below. The differing latencies in binocularand ipsilateral monocular fields in lesioned animals alsoshow that the increased latencies have some visual fieldspecificity and, hence, like reduced response frequency inparticular visual field regions, cannot be simply attributedto changes in general factors like state of health or motiva-tion. As with response frequency, our observations leave ussomewhat uncertain as to whether unilateral tectal lesionsalter response latency in the ipsilateral monocular field. Ifthere is such an effect, it would appear to be of lesser mag-nitude than that observed following unilateral forebrainlesions.

In general, our findings on animals with unilateral tectallobe lesions show somewhat greater effects than have pre-viously been described. In particular, such lesions clearlyproduce not only abolition of accurate orienting to stimuliin the contralateral monocular field but also reductions inresponse frequency and increases in response latency in thebinocular field as well. The overall syndrome is quite simi-lar to that we have observed following unilateral forebrainlesions and, hence, provides strong support for the hypoth-esis that deficits in visual orienting behavior following uni-lateral telencephalic lesions are due primarily to the loss ofa facilitatory influence on the tectal lobe on the same sideof the brain. At the same time, there are two differencesbetween the effects of forebrain and tectal lobe lesions. An-imals with tectal lesions exhibited somewhat more sponta-neous turning into the deficit region, and those with fore-brain lesions had greater reductions in response frequencyand latency in the ipsilateral monocular field. A facilitatoryinfluence from the forebrain might be exerted by a directforebrain-tectal projection or indirectly via some otherstructure or structures [Wilczynski and Northcutt, 1983b;Neary, 1990; Northcutt and Ronan, 1992]. We will considerthis question and the related question of small differencesbetween the effects of forebrain and tectal lesions in the fol-lowing paper [Patton and Grobstein, 1997].


Forebrain Lesions and Visual Field Deficits inFrogs and CatsNow classic work in cats attributed contralateral ori-

enting deficits following unilateral visual cortex lesionsto inactivation of the tectal lobe on the same side of thebrain [Sprague, 1966; Sherman, 1974; Wallace et al., 1989,1990]. Our findings suggest a forebrain/midbrain interac-tion in frogs that is quite similar. However, the origins ofa hypothetical facilitating influence of the forebrain on themidbrain in frogs require further exploration, since visualcortex is not a prominent component of forebrain organi-zation in frogs, if it is present at all. The following paper[Patton and Grobstein, 1997] addresses this issue.

In thinking about comparisons between cats and frogs,one additional point that emerges from our studies is rele-vant. In cats, the contralateral orienting deficit has a borderon the midsagittal plane [Sprague, 1966; Sherman, 1977;Wallace et al., 1989], whereas in frogs, as we have shown,the most profound deficit is restricted to the contralateralmonocular field. The latter makes sense, given that eacheye in ranid frogs projects only to the opposite tectal lobe[Grobstein et al., 1980]. Since the binocular visual field onboth sides of the midline is represented in both tectal lobes,one would expect, and in fact one observes, sparing of re-sponsiveness in this region following unilateral tectal lobelesions as well as loss of a postulated facilitating influencesfrom the ipsilateral forebrain.

What is less clear is why an orienting deficit in catsshould affect not only the contralateral monocular fieldbut an additional part of the binocular field, so as to yielda deficit bordered by the midsagittal plane. In cats, as infrogs, each tectal lobe contains a representation of the entirevisual field of the contralateral eye [Guillery, 1982], so thatthe binocular field is similarly represented on both tectallobes. Unlike in frogs, however, unilateral tectal lesionsin cats have been reported to produce hemifield deficits[Sprague and Meikle, 1965; Wallace et al., 1989] for rea-sons yet to understood [Sherman, 1977]. In the primary vi-sual cortex, on the other hand, each side of the brain con-tains a representation of only the contralateral hemifield.Whether a comparable hemifield organization occurs in theforebrain of frogs is unknown, but the antecedent retino-thalamic projections in frogs do not exhibit the characteris-tic topographically organized partial decussation that cre-ates the hemifield representation in the visual cortex of cats[Scalia and Fite, 1974]. It thus seems likely that the differ-ing field extents of unilateral lesions in frogs and cats mayreflect modifications in the latter associated with the evolu-tion of partial decussation in the retinothalamic pathway.This raises interesting questions about the comparative or-

ganization of projections from forebrain to midbrain as wellas questions about descending tectofugal pathways in frogsand cats that are worthy of further exploration.

Response Frequencies, Response Latencies, and anObserved Inverse CorrelationOrienting deficits in frogs, as in other organisms, are

most commonly characterized in terms of the absence ornear absence of directed movements in response to appro-priate stimuli. Such deficits were observed in the presentstudies, but we also obtained clear evidence for less com-plete deficits, characterized not by an absence of responsesbut rather by a reduction in response frequency. This kindof deficit, most commonly seen for stimulus presentationsin the binocular visual field, clearly cannot be accounted forby removal of circuitry essential for the triggering of nor-mal behavior [Grobstein, 1990b], nor by removal of addi-tional structures or pathways essential to facilitating suchcircuitry. The lesions must instead somehow be acting toreduce the likelihood of activation of circuitry adequate tosupport normal behavior.

Fite and Hayden [1985] have previously described adifferent sort of orienting deficit in the frog which alsorequires explanation in terms other than the removal ofessential circuitry. Basal optic tract lesions do not abolishvisually triggered orienting movements, but they do pro-duce significant increases in the latencies of responses forstimuli in particular areas of the visual field. Increased re-sponse latencies were also apparent in our findings follow-ing both forebrain and midbrain lesions. Moreover, weobserved a general inverse correlation between responsefrequency and response latency. Response latencies weremost clearly increased in the binocular visual field in le-sioned animals, the same area where response frequencieswere most reduced while being still above zero. Responselatencies were also elevated in the ipsilateral monocularfield in forebrain lesioned animals, where there were clearreductions in response frequency. Response latencies wereless obviously elevated in the ipsilateral monocular fieldfollowing tectal lesions; here there was also a less apparenteffect on response frequency in the ipsilateral monocularfield. Finally, we observed some evidence of a correlationbetween response frequency and response latency in theoverall behavior of normal frogs: those which tended torespond more frequently often also tended to respond morerapidly.

We know of no models of the neuronal organization un-derlying anuran orienting behavior (or of neuronal functiongenerally) that provide obvious explanations of variationsin either response frequency or response latency, to say


nothing of a correlation between the two. From this per-spective, it is worth entertaining the possibility that theobserved phenomenon has its origins outside the nervoussystem. Prey recognition, for example, might require preymovement of greater than some threshold amplitude [cf.Ewert, 1970]. More sluggish worms might take longer, onthe average, to exhibit a sufficiently large amplitude move-ment and would more frequently fail to do so. Variations inthe input signal could thus account for variations in re-sponse latency seen in individual frogs. If the threshold ishigher in some frogs than in others and is increased by bothforebrain and midbrain lesions, such variations in the inputsignal could account as well for both correlated differencesin normal frogs and our observed lesion effects.

Such an explanation is testable using artificial stimuli.At the same time, we have observed no striking correlationbetween response latency and prey movement amplitude innormal frogs, and some explanation would have to be givenfor why the amplitude threshold differs for different visualfield regions in lesioned animals. In addition, the explana-tion presumes the phenomena are specific to idiosyncrasiesof frog orienting, whereas we suspect that the correlationwe are calling attention to will be familiar to investigatorsin a variety of different systems. Finally, recent studies sug-gest that a significant amount of the variability observed inbehavior actually has its origins inside the nervous systemrather than in input signals [Grobstein, 1992, 1994]. It thusseems worth considering the possibility that our entire setof observations may have its explanation in organizationalfeatures of the nervous system itself, features which haveyet to be incorporated in models of the neuronal circuitryunderlying anuran orienting.

The most obvious interpretation of response latencies isthat they reflect a combination of conduction times andsynaptic delays in going directly from photoreceptors tomuscle contractions. Even the shortest response latenciesreported here (a few seconds), however, are far too long tobe accounted for in terms of such delays alone. An alternateperspective on latencies, stemming from increasing aware-ness of the properties of heavily interconnected neuralnetworks [Arbib, 1985; Hertz et al., 1991; Kelso, 1995;Peretto, 1992], is that they might largely reflect the time ittakes for populations of neurons to settle into characteristicfiring patterns in the face of both internal variability inactivity and perturbing sensory input signals. This perspec-tive may have the advantage not only of accounting forboth the length and the variability of latencies in normal an-imals but also that of suggesting some natural links be-tween response latency and response frequency. Relativelystable networks would be expected to settle into stable fir-

ing patterns both rapidly and reliably, while relatively un-stable networks might take longer and hence more fre-quently fail to reach their characteristic firing pattern withincriterion times. Our intuition is that network stability maybe a function of both internal variability in unit activity(perhaps accounting for differences between animals) andnetwork size (perhaps accounting for the effects of lesions).Neural modelling studies to test these intuitions are inprogress.

Though we are unable at present to provide a definitiveanswer to the question of what underlies correlations be-tween response frequency and latency, the correlation itselfis quite striking in our observations and clearly warrantsfurther study along several directions.

Acknowledgements

This work was supported by research grants NIH 1 R15 NS 24968,NSF BNS 8311929, and a research grant from the Whitehall Founda-tion to Paul Grobstein. We would like to thank Tom Masino, ElizabethThomas and Jim Kinerim, and two anonymous reviewers, for readingand commenting on versions of this manuscript. Partial preparation ofthis manuscript was also supported by NSF IBN-9420525 to AnandaWeerasuriya.



Arbib, M.A. (1985) Brain theory and cooperativecomputation. Hum. Neurobiol., 4: 201–218.

Comer, C., and P. Grobstein (1981a) Organizationof sensory inputs to the midbrain of the frog,Rana pipiens. J. Comp. Physiol. A, 142:161–168.

Comer, C., and P. Grobstein (1981b) Tactuallyelicited prey acquisition behavior in the frog,Rana pipiens, and a comparison with visuallyelicited behavior. J. Comp. Physiol. A, 142:151–160.

Ewert, J.-P. (1970) Neural mechanisms of prey-catching and avoidance behavior in the toad(Bufo bufo L.). Brain Behav. Evol., 3: 36–56.

Ewert, J.-P. (1980) Neuroetholoy: An Introductionto the Neurophysiological Fundamentals ofBehavior. Springer-Verlag, Berlin, Heidelberg,New York.

Ewert, J.-P., H. Burghagen, and E. Schurg-Pfeiffer(1981) Neuroethological analysis of the innatereleasing mechanism for prey-catching behav-ior in toads. In Advances in Vertebrate Neu-roethology (ed. by J.-P. Ewert, R. Capranica,and D.J. Ingle), NATO ASI Series, PlenumPress, New York, London, pp. 413–475.

Finkenstädt, T. (1989) Visual associative learning:searching for behaviorally relevant brain struc-tures in toads. In Visuomotor Coordination –Amphibians, Comparisons, Models, and Ro-bots (ed. by J.-P. Ewert, R. Capranica, and D.J.Ingle), Plenum Press, New York, London,pp. 799–832.

Finkenstädt, T., N.T. Adler, T.O. Allen, and J.-P.Ewert (1986) Regional distribution of glucoseutilization in the telencephalon of toads inresponse to configurational visual stimuli: acarbon 14 2 deoxyglucose study. J. Comp.Physiol. A, 158: 457–467.

Finkenstädt, T., and J.-P. Ewert (1983) Visual pat-tern discrimination through interactions ofneural networks: a combined electrical brainstimulation, brain lesion, and extracellularrecording study in Salamandra salamandra.J. Comp. Physiol. A, 153: 99–110.

Finkenstädt, T., and J.-P. Ewert (1988) Effects ofvisual associative conditioning on behaviorand cerebral metabolic activity in toads. Natur-wissenschaften, 75: 95–97.

Fite, K.V., and D. Hayden (1985) The accessoryoptic system and temporal correlates of visuo-motor orientation. Brain Behav. Evol., 27:48–56.

Grobstein, P. (1990a) Strategies for analyzing com-plex organization in the nervous system II. Acase study: directed movement and spatial rep-resentation in the frog. In Systems Develop-ment Foundation Benchmark Series in Compu-tational Neuroscience (ed. by E. Schwartz),MIT Press, Cambridge, Massachusetts, pp.19–37.

Grobstein, P. (1990b) Strategies for analyzingcomplex organization in the nervous system I.Lesion experiments, the old rediscovered. InSystems Development Foundation BenchmarkSeries in Computational Neuroscience (ed. byE. Schwartz), MIT Press, Cambridge, Massa-chusetts, pp. 242–255.

Grobstein, P. (1992) Directed movement in thefrog: motor choice, spatial representation,free will? In Neurobiology of Motor ProramSelection (ed. by J. Kien, C.R. McCrohan, andW. Winlow), Pergamon Press, New York,pp. 251–279.

Grobstein, P. (1994) Variability in brain functionand behavior. In Encyclopedia of Human Be-havior (ed. by V. Ramachandran), AcademicPress, New York, pp. 447–458.

Grobstein, P., C. Comer, and S. Kostyk (1980) Thepotential binocular field and its tectal represen-tation in Rana pipiens. J. Comp. Neurol., 190:175–185.

Gruberg, E.R., and V.R. Ambros (1974) A fore-brain visual projection in the frog (Rana pipi-ens). Exp. Neurol., 44: 187–197.

Grusser, O.J., and U. Grusser-Cornehls (1976)Neurophysiology of the anuran visual system.In Frog Neurobiology: A Handbook (ed. by R.Llinas and W. Precht), Springer-Verlag, Berlin,Heidelberg, New York, pp. 297–385.

Guillery, R. (1982) The optic chiasm of the ver-tebrate brain. Contrib. Sensory Physiol., 7:39–73.

Halpern, M. (1972) Some connections of the tel-encephalon of the frog, Rana pipiens. BrainBehav. Evol., 6: 42–68.

Hertz, J., A. Krogh, and R.G. Palmer (1991) Intro-duction to the Theory of Neural Computation.Addison-Wesley Publishing Co.

Ingle, D. (1968) Visual releasers of prey-catchingbehavior in frogs and toads. Brain Behav.Evol., 1: 500–518.

Ingle, D. (1970) Visuomotor functions of the frogoptic tectum. Brain Behav. Evol., 3: 57–71.

Ingle, D. (1973) Evolutionary perspectives on thefunction of the optic tectum. Brain Behav.Evol., 8: 211–237.

Ingle, D.J. (1983) Brain mechanisms of visual lo-calization by frogs and toads. In Advances inVertebrate Neuroethology (ed. by J.-P. Ewert,R. Capranica, and D.J. Ingle), NATO ASISeries, Plenum Press, New York, London,pp. 177–221.

Ingle, D. (1991) The striatum and short term spatialmemory: from frog to man. In Visual Struc-tures and Integrated Functions (ed. by M.A.Arbib and J.-P. Ewert), Springer, Berlin,pp. 273–280.

Karamian, A.I., N.P. Vesselkin, M.G. Belekhova,and T.M. Zagorulko (1966) Electrophysiologi-cal characteristics of tectal and thalamo-corti-cal divisions in the visual system in lower ver-tebrates. J. Comp. Neurol., 127: 559–576.

Kelso, J.A.S. (1995) Dynamic Patterns: The SelfOrganization of Brain and Behavior. MITPress, Cambridge, Massachusetts.

Kicliter, E. (1973) Flux, movement, and wave-length discrimination in frogs: forebrain andmidbrain contributions. Brain Behav. Evol., 8:340–365.

Kicliter, E. (1979) Some telencephalic connectionsin the frog, Rana pipiens. J. Comp. Neurol.,185: 75–86.

Kicliter, E., and S.O.E. Ebbesson (1976) Nonolfac-tory cortex: organization of the ‘non-olfactory’telencephalon. In Frog Neurobiology: A Hand-book (ed. by R. Llinas and W. Precht),Springer-Verlag, Berlin, Heidelberg, NewYork, pp. 946–972.

Kicliter, E., and R.C. Northcutt (1975) Ascendingafferents to the telencephalon of ranid frogs: ananterograde degeneration study. J. Comp. Neu-rol., 161: 239–254.

Kokoros, J.J., and R.G. Northcutt (1977) Telen-cephalic efferents of the tiger salamander Am-bystoma tigrinum tigrinum (Green). J. Comp.Neurol., 173: 613–628.

Kostyk, S., and P. Grobstein (1982) Visual orient-ing in frogs with various unilateral lesions. Be-hav. Brain Res., 6: 379–388.

Kostyk, S., and P. Grobstein (1987a) The neuronalorganization underlying visually elicited preyorienting in the frog Rana pipiens. I. Effects ofvarious unilateral lesions. Neuroscience, 21:41–55.

Kostyk, S.K., and P. Grobstein (1987b) Neuronalorganization underlying visually elicited preyorienting in the frog: II. Anatomical studieson the laterality of central projections. Neuro-science, 21(1): 57–82.

Kostyk, S.K., and P. Grobstein (1987c) Neuronalorganization underlying visually elicited preyorienting in the frog: III. Evidence for the exis-tence of an uncrossed descending tectofungalpathway. Neuroscience, 21(1): 83–96.

Liege, B., and G. Galand (1972) Single-unit visualresponses in the frog’s brain. Vision Res., 12:609–622.

Masino, T., and P. Grobstein (1989a) The organiza-tion of the descending tectofugal pathwaysunderlying orienting in the frog, Rana pipiens.I. Lateralization, parcellation, and an interme-diate spatial representation. Exp. Brain Res.,75: 227–244.

Masino, T., and P. Grobstein (1989b) The organiza-tion of the descending tectofugal pathwaysunderlying orienting in the frog, Rana pipiens.II. Evidence for the involvement of a tecto-teg-mento-spinal pathway. Exp. Brain Res., 75:245–264.

Masino, T., and P. Grobstein (1990) Tectal connec-tivity in the frog Rana pipiens: tectotegmentalprojections and a general analysis of topo-graphic organization. J. Comp. Neurol., 291:103–127.

References

Merkel-Harff, C., and J.-P. Ewert (1991) Learningrelated modulation of toad’s responses to preyby neural loops involvin the forebrain. In Vi-sual Structures and Integrated Functions. Re-search Notes in Neural Computing (ed. byM.A. Arbib and J.-P. Ewert), Springer-Verlag,Berlin, Heidelberg, New York, Paris, Tokyo,pp. 417–426.

Neary, T.J. (1984) Anterior thalamic nucleus pro-jections to the dorsal pallium in ranid frogs.Neurosci. Lett., 51: 213–218.

Neary, T.J. (1990) The pallium of anuran amphib-ians. In Cerebral Cortex Vol. VIII A (ed. byE.G. Jones and A. Peters), Plenum Press, NewYork, pp. 107–138.

Neary, T.J., and R.G. Northcutt (1983) Nuclearorganization of the bullfrog diencephalon.J. Comp. Neurol., 213: 262–278.

Northcutt, R.G. (1972) Afferent projections of thetelencephalon of the bullfrog (Rana cates-beiana). Anat Rec., 172: 374.

Northcutt, R.G., and E. Kicliter (1980) Organiza-tion of the amphibian telencephalon. In Com-parative Neurology of the Telencephalon (ed.by S.O.E. Ebbesson), Plenum Press, New York,London, pp. 203–255.

Northcutt, R.G., and M. Ronan (1992) Afferent andefferent connections of the bullfrog medial pal-lium. Brain Behav. Evol., 40: 1–16.

Northcutt, R.G., and G.R. Royce (1975) Olfactorybulb projections in the bullfrog Rana cates-beiana. J. Morphol., 145: 251–268.

Patton, P., and P. Grobstein (1998) The effects oftelencephalic lesions on visually mediated preyorienting behavior in the leopard frog (Ranapipiens). II. The effects of limited lesions tothe telencephalon. Brain Behav. Evol., 51:144–161.

Peretto, P. (1992) An Introduction to the Modelingof Neural Networks. Cambridge UniversityPress, Cambridge, England.

Ronan, M.C., and R.G. Northcutt (1979) Afferentand efferent connections of the bullfrog medialpallium. Soc. Neurosci. Abstr., 5: 146.

Scalia, F. (1976) The optic pathway of the frog:nuclear organization and connections. In frogNeurobiology: A Handbook (ed. by R. Llinasand W. Precht), Springer-Verlag, Berlin, Hei-delberg, New York, pp. 386–406.

Scalia, F., and K. Fite (1974) A retinotopic analysisof the central connections of the optic nerve inthe frog. J. Comp. Neurol., 158: 455–478.

Schneider, G.E. (1967) Contrasting visuomotorfunctions of tectum and cortex in the goldenhamster. Psych. Forsch., 31: 52–62.

Schneider, G.E. (1969) Two visual systems. Sci-ence, 163: 895–902.

Sherman, S.M. (1974) Visual fields of cats withcortical and tectal lesions. Science, 185:355–357.

Sherman, S.M. (1977) The effect of superior col-liculus lesions upon the visual fields of catswith cortical ablations. J. Comp. Neurol., 172:211–230.

Sprague, J.M. (1966) Interaction of cortex andsuperior colliculus in mediation of visuallyguided behavior in the cat. Science, 153:1544–1547.

Sprague, J.M., and T.H. Meikle (1965) The roleof the superior colliculus in visually guidedbehavior. Exp. Neurol., 11: 115–146.

Székely, G., and G. Lázár (1976) Cellular andsynaptic architecture of the optic tectum. InFrog Neurobiology: A Handbook (ed. by R.Llinas and W. Precht), Springer-Verlag, Berlin,Heidelberg, New York, pp. 407–434.

Vesselkin, N.P., A.L. Agayan, and L.M. Nomo-konova (1971) A study of thalamo-telence-phalic afferent systems in frogs. Brain Behav.Evol., 4: 295–306.

Vesselkin, N.P., T.V. Ermakova, N.B. Kenigfest,and M. Goikovic (1980) The striatal connec-tions in the frog Rana temporaria: an HRPstudy. J. Hirnforsch., 21: 381–392.

Wallace, S.F., and A.C. Rosenquist, and J.M.Sprague (1989) Recovery from cortical blind-ness mediated by destruction of nontectotectalfibers in the commissure of the superior col-liculus of the cat. J. Comp. Neurol., 284:429–450.

Wallace, S.F., A.C. Rosenquist, and J.M. Sprague(1990) Ibotenic acid lesions of the lateral sub-stantia nigra restore visual orientation behaviorin the hemianopic cat. J. Comp. Neurol., 269;222–252.

Wicht, H., and W. Himstedt (1986) Two thalamo-telencephalic pathways in a urodele, Triturusalpestris. Neurosci. Lett., 68: 90–94.

Wicht, H., and W. Himstedt (1988) Topologic andconnectional analysis of the dorsal thalamus ofTriturus alpestris (Amphibia, Urodela, Sala-mandridae). J. Comp. Neurol., 267; 545–561.

Wilczynski, W., and R.G. Northcutt (1983a) Con-nections of the bullfrog striatum: afferent orga-nization. J. Comp. Neurol., 214: 321–332.

Wilczynski, W., and R.G. Northcutt (1983b) Con-nections of the bullfrog striatum: efferent pro-jections. J. Comp. Neurol., 214: 333–343.


The Effects of Telencephalic Lesions on Visually Mediated Prey Orienting Behavior in the Leopard...

Documents

Transcript of The Effects of Telencephalic Lesions on Visually Mediated Prey Orienting Behavior in the Leopard...