Archistriatal lesions enhance tonic immobility in the chicken (Gallus gallus)

physiology and Behavior, Vol. 11, pp. 729-733.

Brain Research Publications Inc., 1973. Printed in the U.S.A.

BRIEF COMMUNICATION Archistriatal Lesions Enhance Tonic Immobility in the Chicken (Callus gallus) JACK D. MASER, JOAN W. KLARA AND GORDON G. GALLUP, JR. Department ofPsychology, Tulane University, New Orleans, Louisiana 70118

(Received 19 March 1973)

MASER,

J. D., J. W. KLARA AND G. G. GALLUP, JR. Archistriatal lesions enhance tonic immobility in the chicken BEHAV. 11(5) 729-733, 1973.-Chickens sustaining lesions in the archistriatum intermedium

(Callus gallus) PHYSIOL.

showed an I-fold increase in the duration of tonic immobility as compared with control birds. Septal lesions had no significant effect when compared with sham operates. It was assumed that the tractus occipitomesencephalicus, a possible avian variant of the primate pyramidal tract was damaged. The behavioral effect found here supports the notion that the avian archistristum is “conjunctive” cortex and that the archistriatum cannot be described as a homolog of the mammalian amygdala without qualifications. Animal hypnosis Tonic immobility Efferent organization Septal area

Archistriatum Amygdala

Neural homology

Defensive behavior

ly correlated with prolonged responses. When the bird is immobilized in the standing position, wing-drooping (which resembles injury feigning) is frequent. There is considerable evidence implicating the amygdala and septal region of mammals as important components of the response mechanism mediating operant behaviors [6, 13, 16, 241. Comparable data exist for similar structures in the avian brain [26,27,281. Although Kappers, Huber and Crosby [ 8 I consider the archistriatum to be an avian homolog of the mammalian amygdala, functional [27] and morphological qualifications [ 29 I appear necessary. The present study was designed to investigate the possible role of the avian archistriatum and septal region in the mediation of a species-typical response tendency, tonic immobility.

THE tonic immobility response (IR), commonly called animal hypnosis, is well documented in a variety of species at different phyletic levels [ 11 ,19 I and considerable evidence exists that the behavior is potentiated by fear manipulations [3, 4, 151. The common denominator of most situations designed to elicit IR is some form of externally imposed tactile and proprioceptive input (i.e. manual restraint). The present experiments were prompted by our interest in the neural basis of response mechanisms related to species-typical behavioral patterns [ 141. Motor mechanisms may be distinguished from response mechanisms in that the latter subserve innate and learned movements relative to stimulus incentives, while the former are assumed to regulate muscle tonus, postural reflexes, and guidance adjustments during movement. Tonic immobility is an interesting dependent variable in this regard because: (1) in the absence of specific past experience, or learned associations, the behavior is evoked the first time that the appropriate complex of aversive stimuli are presented; (2) it occurs under natural conditions and may function as a predator defense [24] ; and, (3) it may be viewed as the active suppression of movement relative to an aversive environmental stimulus. In the IR state 151, the chicken’s eyes are closed about 50% of the time and the legs may be flexed or extended (exhibiting some signs of catatonic-like waxy flexibility), but there is frequent tremor in either case. Vocalizations are initially suppressed, usually occurring just prior to IR termination. Defecation during or following IR is moderate-

METHOD

Animals

Thirty-five straight run (i.e., not categorized by sex) Production Red chickens (Gallus gallus) obtained from a local hatchery at one day of age, were used. The chickens were maintained in commercial brooders equipped with thermostatically controlled temperature devices for 4 weeks prior to surgery. The animals were given continuous access to water and Purina Chick Chow (Growena) throughout rearing and the photoperiod consisted of 14 hr of artifical light per day. 729

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Surgery

The birds were randomly assigned to a surgical group at 28-30 days of age. All birds were anesthetized with pentobarbital sodium solution injected intraperitoneally. One group of 9 birds received bilateral archistriatal lesions and another 9 received septal lesions through a stainless steel electrode placed sterotaxically 1231. Lesions were accomplished by passing a d.c. current (0.5 mA for 30 set) through the uninsulated tip (0.2 mm in dia.) of the electrode. The cathode was a large indifferent electrode inserted in the cloaca. Seventeen animals served as sham lesioned controls. Nine received electrode track lesions to a point 2 mm above the archistriatum and 8 septal shams were similarly treated. After surgery each bird was injected with 0.1 cc Cornbiotic and placed in a warm recovery area.. Two to three hr after full recovery they were returned to the brooder. Two days following completion of the behavioral test the animals were anesthetized and perfused intracardially with 0.9% saline, followed by 10% formalin. The brains were removed from the cranium and fixed in formalin for 2 days. They were then frozen in a cryostat and sectioned at 30 ~1. Every third section was stained with cresylechtviolett and examined microscopically. Apparatus

All animals were immobilized on a table in a separate experimental room. A stopwatch was used to record the duration of IR. Wooden boxes, situated outside the experimental room were used as pre and posttest holding chambers. Procedure

Two days postoperatively all animals were individually immobilized according to the procedure described by Gallup, Nash and Wagner [5]. Briefly, each animal was immobilized by imposing 15 set of manual restraint. The duration of self-paced immobility was recorded in seconds from the time restraint was removed until the bird rose to its feet. If the animal failed to show signs of IR within 5 induction attempts he was considered unsusceptible and the session ended. RESULTS

Anatomical

Figure 1 is a reconstruction of the maximal extent of the archistriatal lesions in two representative subjects. The archistriatal lesions were primarily in the archistriatum intermedium, presumably involving the occipito-mesencephalic tract. In one case, the lesion destroyed part of the anterior archistriatum and in another, part of the posterior archistriatum. There was also involvement of the tractus frontoarchistriaticus in one animal. Histological verification of the exact location of the archistriatal lesion was not obtainable from one bird, but the subject is included in the behavioral data analysis since his data closely approximated the mean of the group. All septal lesions destroyed the commissural septum and included the medial septal nucleus, either all or part of the lateral septal nucleus and the septo-mesencephalic tract. In some of the cases, the bed nucleus of the pallial commissure

and parts of the anterior commissure were damaged. In one instance, there was involvement of the medial portion of the lamina medullaris dorsalis. Sham operate animals in both groups sustained only electrode tract damage and neither the septum nor the archistriatum were infringed upon. Behavioral

As seen in Fig. 2, archistriatal lesions enhanced IR when compared to the septal and sham operated groups. The mean durations of IR were 1718.2, 143.4, 194.3 and 187.2 set for archistriatal, archistriatal-sham, septal and septal-sham groups, respectively. Analysis of variance revealed a significant difference between these groups (F = 10.76, df = 3/31, p
On the average, archistriatal chickens remained in a state of tonic immobility following manual restraint more than eight times longer than septal or sham operated control subjects. These data have, we believe, two important implications. The first is that functional support is provided for neuroanatomical models which view part of the archistriatum as conjuntive cortex. Kallen [7] , Karten [9] , and Nauta and Karten [ 171 proposed that both mammalian neocortex and avian archistriatum are derived from homologous neuroblast cells. To the extent that part of the archistriatum, especially the anterior two-thirds, may be considered conjunctive cortex, it might be expected that cortical damage and archistriatal damage would produce similar results. In fact, lesions to the cortex of rats increase IR [ 111. Thus, it would seem that cortical and archistriatal injury produce a similar effect on tonic immobility, thereby supporting the notion of morphological homology with an instance of functional similarity. Furthermore, Zeier and Karten [ 291 histologically demonstrated that the origin of the nonhypothalamic branch of the occipitomesencephalic tract is the anterior and intermediate divisions of the archistriatum. Both the route and the termination pattern of the nonhypothalamic occipitomesencephalic tract bear a striking resemblance to Bagley’s corticotegmental bundle [ 11, which is considered a variant of the pyramidal tract in primates [ 2 11. On this basis, Zeier and Karten identify the anterior archistriatum with somatosensorimotor functions, rather than limbic. The eight-fold increase in IR by archistriatal chickens would appear to corroborate Zeier and Karten, but extend the notion of motor involvement to participation of this region in response mechanisms. It is significant that in the rat Leonard and Scott [ 121 reported that lesions in the posterior part of the cortical nucleus (medially placed) produced degeneration in the ventromedial and anterior hypothalamus. This suggests that in the rat the medial and posterior regions of the amygdala, which project to the hypothalamus, are limbit in nature, while the more lateral nuclei, which do not appear to have direct hypothalamic connections, may be sensorimotor. The second implication of these data concerns the phylogenetic view of the brain-behavior correlations. Task differences make direct comparisons difficult, although not impossible. Lesions to the mammalian (rat) amygdaloid nu-

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FIG. 1. Reconstructions of two representative chicken brains with archistriatal lesions (birds A2 and A3). Numbers to the right of the lateral millimeter axis designate site of maximal damage in the anterior-posterior plane according to Van Tienhoven and Juhasz [23], while numbers to the left indicate the extent of the anterior-posterior damage. DA: Tractus archistriatalis dorsalis; DM: Nucleus dorsomedialis; HA: Hyperstriatum accessorium; LFB: Lateral forebrain bundle; LH: Tractus front0 occipitalis; LMD: Lamina medullaris dorsalis; NEOST: Neostriatum; OM: Tractus occipitomesencephalicus PALP: Paleostriatum primitivum; ROT: Nucleus rotundus; TEC: Optic tectum.

MASER, KLARA, AND GALLUP

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1800 1600 1400 1200 1000 800 600 400 200

A

AS

TREATMENT FIG.

S

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CONDITIONS

2. Duration in seconds of the tonic immobility response for archistriatal (A), septal (S), archistriatal sham (AS) and septal sham (SS) operated groups.

cleus generally appear to result in perseveration of dominant response tendencies, both during nonreinforced trials [ 201 and in the face of incentive change [ 18,251. Furthermore, Turner [ 221 describes unilateral damage to the medial amygdala of the rat to produce a contralateral orientation and localization deficit of somatosensory fields. It is important to note that the deficit could not be accounted for by motor impairment or raised sensory thresholds. Lesions to part of the avian archistriatum produce behavioral dysfunctions similar to that of the rat [ 26,271 and the present data could be interpreted as a further demonstration of a response perseveration resulting from amygdaloid damage, in this case the perserveration of a speciestypical behavior. This suggests that the components of the response mechanism underlying the expression of operant movements and the tonic immobility response have the same neural origin. However, the quality of performance may be a complex function of variables unique to each species [ 261. A recent report by Blanchard and Blanchard assessed the effect of corticomedial amygdaloid lesions on freezing be-

havior as a defensive reaction in the rat. Corticomedial damage reduced freezing and avoidance of both a predator (anesthetized cat) and a stimulus associated with shock. Thus it would appear that the present data and those of Blanchard and Blanchard are contradictory. However, there exist two alternative explanations of the apparent discrepancy. First, freezing does not require manual restraint and differs appreciably from behaviors characteristic of tonic immobility (e.g. eye closure, leg tremors, etc.). Moreover, from an ethological viewpoint, freezing might be seen as the first response in the predatordefense sequence of freezing, flight, fight, tonic immobility [ 191. In view of these findings, it would be valuable to test amygdaloid rats for both tonic immobility and freezing. Alternatively it should be noted that Blanchard and Blanchard lesioned the corticomedial amygdaoid nucleus, the region which gives rise to the hypothalamic projections, and which might be limbic rather than somatosensorimotor. In concert with the notion that the avian anterior archistriatum may represent conjuctive cortex, a lack of functional homology could be expected.

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