Brain damage and behavioral recovery: Serial lesion phenomena

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Brain damage and behavioral recovery: Serial lesion phenomena
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  Brain Research 63 (1973) 1-18 1 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands Review rticle BRAIN DAMAGE AND BEHAVIORAL RECOVERY: SERIAL LESION PHENOMENA STANLEY FINGER, BONNIE WALBRAN AND DONALD G. STEIN Department of Psychology, Washington University, St. Louis, Mo. 63130, and *Department of Psychol- ogy, Clark University, ~orcester, Mass. 01610 U.S.A.) (Accepted 20th March, 1973) INTRODUCTION One of the most interesting and least understood phenomena in the field of neuropsychology is the observation that under certain conditions organisms appear capable of recovering from severe, traumatic injury to the central nervous system 13,63. For example, although the finding is by no means universal 25,52,71, it often has been reported that very young rats, cats and monkeys, as well as humans, show consider- able restitution or sparing of function following extensive damage to various areas of the brain13, 63. In one such study, Benjamin and Thompson 6 produced bilateral somatosensory cortical lesions in neonatal and adult cats and then tested the animals on a battery of tactile discriminations. The operated animals compared favorably to controls on all but the most difficult tasks when the lesions were placed in the first week of life. In contrast, virtually all animals operated upon in adulthood were unable to learn even the simplest discriminations in the series. That more cognitive tasks are simi- larly affected is also well documented. For example, Tucker and Kling 74 ablated frontal granular cortex in neonatal monkeys and reported that these animals could learn delayed response tasks with longer delays than could subjects that underwent surgery at about 3 years of age. Studies such as these frequently have fostered the conclusion that damage to the adult nervous system is more marked and less reversible than brain damage in- flicted early in life. Most investigators would agree that intensive care and training may lead to varying degrees of compensation in the former case, but acceptance of the principle that little if any reorganization or sparing of function occurs following acute damage to the mature mammalian nervous system, has led may researchers to assume that most structure-function relationships are fixed or committed early in life. It has been argued recently that considerable sparing of function may follow extensive damage to the adult nervous system if the target area is damaged serially with a specified number of days between operations -- a phenomenon herein referred  2 s. FINGER et al to as the serial lesion effect This laboratory observation may be related to the effect of momentum of lesion 31,32 which was described as early as 1836 in the clinical literature concerning language disturbances 3z. These studies appear to show that the nervous system of the adult animal has greater plasticity than generally is granted to it, and this would suggest a reexamination of some ideas relating to structure- function relationships in the brain. SERI L LESION EFFECTS Serial surgery and mortality The finding that removal of neural tissue in two or more stages is associated with a lower mortality rate than ablation of the same structures in a single sitting has been known for some time. Flourens x8 was able to keep decorticated pigeons alive for considerable periods by removing small amounts of tissue in each operation. More than 100 years later, Lashley 48 observed that lesions involving more than 50 of the cortex usually required two successive operations for survival (p. 16). Kleitman and CamiUe 42, investigating the relationship between cerebral cortex and sleep behavior in dogs, also relied on two-stage extirpations of cerebral cortex because of the high mortality rate associated with ablating the entire cortex in one operation. Mortality rates also may be lower with serial lesions in subcortical structures. Adametz I examined a large number of cats with extensive lesions of the mesial teg- mentum of the rostral midbrain and found that his animals survived this surgery without incident when the lesions were accomplished in several sittings with 1-3 weeks between operations. In contrast, but in accord with the historic findings of Lindsley et al 45 and French and Magoun 19, one-stage lesions in the same loci resulted in a deep coma from which only 1 of 15 animals recovered. Kesner et al a8 reported somewhat analogous pilot data for rats with one-stage and two-stage lesions of the midbrain reticular formation. Lower mortality rates have been observed after serial lesions of the posterior thalamus 60, and after damage to the midbrain medial lem- niscus in rats 20. Unlearned behaviors Motor coordination Some of the earliest systematic investigations on restitution of function were performed by Kennard 35-37 on the motor cortex. She ablated Brodmann areas 4 and 6 in infant and in more mature Macaca mulatta and found (a) that the animal s ability to recover motor functions was directly related to age at time of surgery, and (b) that recovery was maximal when ablations were accomplished seriatim with long intervals between operations. Kennard postulated that remaining areas of the cortex were responsible for mediating normal behaviors. As evidence, she noted that subsequent removal of prefrontal or postcentral areas greatly aug- mented the deficits of animals that had areas 4 and 6 ablated in infancy. These lesions failed to affect skilled motor performance in previously unoperated animals. Ades and Raab 3 reported similar findings in the mature monkey. They observed that if both motor and somesthetic areas of one hemisphere were removed, a later  BRAIN DAMAGE AND BEHAVIORAL RECOVERY 3 ablation of the motor region of the opposite hemisphere produced a severe hemipa- resis. They also found that severing the corpus callosum at the time of the first operation did not change the relative absence of lesion effects after motor cortex damage in the multiple-stage condition. By using multi-stage lesions, Travis and Woolsey 7a were able to demonstrate good recovery of motor functioning after total removal of the neocortex from both hemispheres in two monkeys (see also ref. 77). In this investigation, one of the mon- keys retained both righting and walking ability, and the other was able to right and walk with assistance immediately after surgery. Findings such as these stand in marked contrast to the descriptions by previous investigators a4,47 of the decorticate monkey. In 1966, Braun a analyzed the conditions under which placing reflexes could be observed after removal of the neocortex. Rats with extensive neocortical damage exhibited a gradual return of placing responses after one-stage surgery and extensive practice, or after sequential hemispheric lesions with practice interpolated between operations. Braun also reported that only operated animals with serial lesions were able to eat hard food pellets immediately after surgery. One-stage subjects had to be fed special foods for approximately 7 days postoperatively. Schultze ~5 observed normal eating and grooming behaviors, and only transient signs of motor akinesis, after successive lesions centered in the caudate nucleus. Animals subjected to simul- taneous bilateral lesions underwent serious deterioration after this surgery and, like Braun s s rats, were aphagic. In addition, the one-stage caudate animals did not preen for sustained periods of time. Further evidence for the mitigating effects of two-stage lesions on feeding behaviors comes from a study by Blatt and Lyon 7. They found that one-stage bilateral lesions in the midbrain tegmentum dorsolateral to nucleus ruber were followed by prolonged feeding losses. However, two-stage lesions of the same area with a 14 day interoperative period decreased these deleterious effects in their rats. The two-stage lesions in this experiment were made first by operating on one side of the brain and later by damaging homologous tissue across the midline. With one exception in which small bilateral lesions were enlarged in a second operation 17, investigators placing two-stage lesions in adult animals have chosen a sequential unilateral lesion procedure. Motivational and emotional responding In a recent series of experiments on emotionality in rats, Mclntyre a6 studied the effects of single-stage or two-stage damage to the basolateral nucleus of the amygdala on responsivity to aversive stimu- lation. Although the specific role of the amygdala in the control of emotional respond- ing has not been defined clearly, there is evidence that damage to this area may result in amygdaloid sluggishness and deficits in passive avoidance performance26,5~, 75. In one part of her study, Mclntyre 46 trained amygdalectomized rats to run down a straight alley to obtain water. The goal box containing the water spout was constructed from an elliptical laboratory shaker which could be activated at various speeds. Once the rat learned to run down the alley to drink without hesitating, the shaker was activated and measurements were made of (a) the rotation speed necessary to disrupt drinking, (b) the time required to stop drinking after rotation had started, (c) response latencies on subsequent trials, and (d) the degree to which an animal  4 s. FINGER el al would enter the goal area to obtain water while the platform was in motion. McIntyre found that subjects with two-stage lesions resembled controls on these tests and that rats with one-stage lesions of the basolateral amygdala were significantly less respon- sive than the other animals on most of the measures. Sleep and wakefulness The question of whether rats could maintain a waking state subsequent to one-stage or sequentially induced posterior hypothalamic lesions has been examined by LeVere 44. The results of this study showed that wakefulness was related to the completeness of destruction of the target area rather than to temporal course of the lesion. This negative finding appears difficult to interpret in the light of experiments by Adametz 1, Capps and StockwelP 2, Chow and Randall 14 and Kesner et al 3s showing seemingly normal wakefulness after large sequential lesions in the reticular formation. LeVere hypothesized that such differences could reflect the plasticity of the involved neural area as indicated by its participation in learned behaviors (ref. 44, p. 343). ensory areas The fact that serial lesions may minimize performance deficits on sensory dis- criminative tasks is also well established. More than 25 years ago, Ades 2 investigated retention of visual discriminations after aspirative ablations of the parastriate and peristriate cortices (Brodmann areas 18 and 19) in monkeys. Although all of his sub- jects were to receive bilateral lesions in one sitting, the physical condition of one animal necessitated the termination of surgery after damage to the left hemisphere only. This monkey showed perfect retention when tested during the 18 day interlesion interval, and it continued to perform perfectly after surgery was completed. Other animals, all of whom sustained one-stage bilateral lesions, lost the habits but were able to relearn them at preoperative rates. Visual sparing after serial surgery was confirmed by Ades and Raab 4 in 1949. Two years later, Stewart and Ades 70 demonstrated excellent retention of an auditory avoidance response after serial lesions of the superior temporal gyri. Recently, Finger et al 17 extended these findings to the somatic afferent system. They assigned rats at random to one of four surgical conditions: one-stage bilateral lesions of somatosensory cortex areas 1 and 2; two-stage lesions of the same areas; and one-stage and two-stage sham operations. Their animals were tested in a T-maze for the ability to acquire a series of 5 tactile discriminations graded along a ridge- smooth continuum. They demonstrated that animals with one-stage lesions performed more poorly than rats with sequential unilateral lesions, and that the rats with simul- taneous lesions also performed worse than sham operated controls. The animals with serial lesions did not differ from the two-stage sham operates in this study. In a related experiment reported in the same paper, one group of rats experienced small bilateral lesions of the somatosensory cortex that were enlarged to full size after a 35 day interlesion interval. These animals performed more poorly than controls when scores across the 5 discriminations were pooled, but they again learned faster than cage-mates with identical tissue removed in one operation. Less research has been conducted on sequential lesions centered in subcortical  BRAIN DAMAGE AND BEHAVIORAL RECOVERY 5 sensory projections. However one recent experiment 60 has shown that large serial lesions centered in the ventrobasal homologue may decrease high mortality figures but may not minimize deficits in acquiring tactile discriminations in the rat. Learning after limbic system and association cortex lesions Discriminative sparing has been found following serial lesions of cortical areas other than primary sensory projection zones. For example, Rosen et al. 62 trained rhesus monkeys on a spatial delayed alternation task. Upon attaining criterion, the animals received either single-stage or multiple-stage ablations of prefrontal association cortex sulcus principalis). Their results showed that monkeys experien- cing 4 operations, each separated by a 3 week interval, made fewer errors than did one-stage animals on the delayed alternation problem. They also were able to acquire delayed response and position reversal tasks with fewer errors than other operated animals. These data are particularly striking in the context of the histological finding that multiple surgical entries into the same region resulted in adhesions and more extensive damage in the serial animals than in the single-stage preparations. In a related experiment dealing with the limbic system 69, rats with one-stage or two-stage lesions of the hippocampus, amygdala, or frontal cortex, and animals with sham operations, were tested on a light-dark discrimination and for habit reversals. In addition, animals with hippocampal or amygdaloid damage were given a passive avoidance test, while frontal subjects were tested on delayed alternation and simul- taneous discriminations. Each of these tasks was chosen for its known effectiveness in eliciting deficits after these lesions a9,4°,54. The serial animals exhibited little or no impairment on these measures, although rats with simultaneous lesions in the same loci demonstrated marked and long-standing deficits on the problems. Table I presents some of the data collected on animals with lesions of the frontal cortex in this study. More recently, Greene et al. 2s interrupted pathways to and from the hippo- campus by cutting the fornix in one or two stages and studied the effects of this surgery on spatial alternation behavior. Their results were similar to those of Stein et al. 69 TABLE I NUMBER OF TRI LS TO CRITERION IN T SKS PERFORMED BY R TS WITH LESIONS OF THE FRONT L CORTEX Groups with one-stage lesions are labeled l-S; groups with two-stage lesions arc labeled 2-S; un- operated controls are labeled UC; DSA, delayed spatial alternation; LDD, light-dark discrimination; SD, simultaneous discrimination. From Stein et al.S°.) Delayed spatial Light-dark Light-dark Simultaneous alternation discrimination discrimination reversal discrimination mean) mean) mean) mean) Group 1-S 300.0 278.5 313 120.0 Group 2-S 150.0 124.0 121 79.4 Group UC 104.6 148.0 132 73.0
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