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An experimental evaluation of differential natural reactivity as a basis for the oscillation effect
Abstract
Previous research indicated that an oscillation effect resulted during sequential alternation of unilateral amygdaloid stimulation with consistent low-latency values for one side and consistent high values for the contralateral one. One possible basis for this effect is that one of the two sides naturally has a greater reactivity to the stimulating current. This hypothesis was evaluated in this study. One group of rats had the usual alternation of stimulation from one side to the other over 10 phases of six convulsions each. A second group received five consecutive phases of stimulation of the primary site and then five consecutive phases for the secondary side. If the hypothesis were true, the latency values for one side would be consistently lower (or higher) than those for the phases on the other side; this result did not occur, although significant oscillation patterns were prominent with the alternation group. These results tend to suggest that differential natural reactivity of the two sides is not the basis for the oscillation effect.
There are three types of interference effects during kindling: that produced by alternate stimulation of homologous brain sites, by successive stimulation of one site, and by stimulation of one site by different frequencies. These three types of interference appear to be similar. Facilitation and interference effects during kindling seem to be generated by the operation of two factors: a “neurological trace” process, possibly involving synaptic changes, and an “aftereffect.” The latter process may be the main basis for these interference effects.
Data from a number of sequential alternation experiments were factor analyzed to determine the number of common factors present. Three dependent variables (latency of convulsion, number of trials to six convulsions, duration of convulsions) were evaluated by three procedures: principal components solution with 1s in main diagonals, principal axes solution with largest r in the diagonals, principal axes solution with R2 in the diagonals. The results were similar; the presence of two factors was suggested in the latency and criterion measures (primary site stimulation and secondary site stimulation) and one in the duration data. A principal components factor analysis over the three dependent variables showed the presence of three factors, those observed in each of the separate analyses.
Animals subjected periodically to low-intensity electrical stimulation unilaterally to the amygdala or some other brain sites gradually develop automatic behaviors which culminate eventually in convulsions. Characteristic brain wave patterns accompany these behavioral changes. A 60-Hz sine wave with a 24-h interval provides the most optimum condition of stimulation. This kindling effect shows some characteristics similar to learning events, viz, relatively permanent changes, positive and negative transfer effects, involvement of limbic system. The results suggest that two factors are involved in the kindling process: a long-term effect of positive nature (probably due to modified neural circuitry) and a short-term “aftereffect” of negative nature.
Previous research indicated that an oscillation effect resulted during sequential alternation of unilateral electrical stimulation of the amygdala over 10 phases of six clonic convulsions per phase, with consistent low latency values for one side and consistent high values for the contralateral one (i.e., a fluctuation of low and high values on consecutive phases). In the present experiment 10 rats were stimulated for up to 50 phases. Four of the 10 showed remarkable patterns of oscillation in latency data: One oscillated on every one of 50 phases, two showed oscillation patterns on 48 of 50 phases, and the fourth oscillated on every one of 32 phases.
In two experiments, rats were subjected to a sequence of electrical stimulations alternating from one amygdala to the contralateral one. Each phase of stimulation was for six convulsions prior to alternation to the other side. An oscillation effect resulted, involving low trials to six clonic convulsions and low latency to convulse for stimulation of one side, but high values of these measures for the contralateral site. The oscillation persisted, especially for the latency measure, even when one phase of bilateral stimulation preceded unilateral stimulation, when a 17- to 23-day rest period was inserted following a sequence of alternations and when two phases of bilateral stimulation occurred following postrest unilateral stimulations. The oscillation effect was less prominent in the number of trials to six convulsions data and almost nonexistent in duration of convulsion. Of 16 rats used in 15 to 19 alternating phases, 7 oscillated throughout all of these phases in latency data, but none showed oscillation over all phases in the other dependent variables.
Five experiments were conducted in which donor rats were kindled to the clonic-convulsion stage, sacrificed, and their brains removed. The brain was homogenized, and the supernatant fraction was injected intraperitoneally into recipient experimental rats, who then were subjected to the kindling procedure. Control donors which received no stimulation were included. When the injection involved two or more brain amounts, a retarding effect tended to occur with the experimentals. If only one brain amount was used for the injection, no change resulted in the kindling rate of these recipients. This interanimal negative-transfer effect appears to be similar to the intraanimal negative-transfer effect reported by Mclntyre and Goddard.
Previous experiments using a sequence of alternating unilateral stimulations of the amygdalae indicated an “oscillation effect”, i.e., consistent low-latency values for convulsions elicited from one amygdala and consistent high-latency values for convulsions elicited by stimulation of the contralateral amygdala. The present study was concerned mainly with statistical evaluations of the reliability of oscillation events. Tests of the randomness of the observed primary and secondary oscillation patterns indicated that oscillation patterns were significant systematic ones in latency, criterion, and duration data, with the greatest frequency of oscillation occurring in the latency measure. Although there was no significant difference in the frequency of primary or secondary oscillation using chi-square methods, an analysis of variance trend analysis indicated that the primary oscillation pattern (low values on primary side) was the predominant one when considered over the total sample, 139 rats. Also, it was shown that the behavioral pattern (oscillation, nonoscillation) appears not to be related to the number of trials to reach the criterion of six convulsions. The exact basis for oscillatory behavior is unknown. However, for a number of reasons, it appears to be based probably on transfer and interference effects between the primary and secondary brain sites.
Previous research indicated that sequential alternation of stimulation of certain homologous brain areas via chronically implanted electrodes resulted in oscillation of high and low latencies for convulsions. This phenomenon suggested the establishement of interhemispheric facilitatory-inhibitory effects as a result of repeated stimulation of the two brain sites. In the present study, the latency oscillation pattern was observed in split-brain rats as well as in bilaterally stimulated controls, but not in rats stimulated on one side only. Significant differences were observed between split-brain and control rats in terms of initial kindling rates, duration of convulsions and type of oscillation. Results are discussed in the context of possible interhemispheric mechanisms involved in long term kindling.
Bipolar electrodes were implanted into the amygdala of each hemisphere of adult male rats. A short burst of low-intensity stimulation was applied to one of these electrodes once each day. Initially there was little response. With repetition, epileptiform responses progressively developed until each daily stimulus triggered a behavioral convulsion (kindling effect). Following six convulsions, the procedure was applied to the contralateral hemisphere. Convulsions were observed to kindle more rapidly, especially if a rest interval of 2 weeks followed the last primary site convulsion. When stimulation was reapplied to the primary site, convulsions were not triggered. This was associated with failure to evoke local after-discharge and/or failure of the after-discharge to propagate. Several trials were necessary to re-establish convulsion, unless a 2 week rest preceded testing, in which case convulsions were triggered on the first trial. Following a series of convulsions triggered from either hemisphere, the contralaterally triggered convulsions, when they appeared, showed consistently longer onset lattencies. These latency shifts were attentuated when rest intervals preceded the testing. Latency shifts and seizures failures were not observed if the preceeding series of convulsions was reduced from six to one. Lesions at the tip of either electrode had little effect on the results obtained in the contralateral hemisphere. Together, the results imply that: kindling establishes a lasting trace which is both transynaptic and widespread, kindling from a second location establishes a second trace utilizing parts of the existing trace, a series of convulsions leaves a less durable after-effect with a decay time of about 2 weeks and which interferes with various aspects of seizure activity, and the trace which activates the convulsions is less susceptible to interference from the after-effect.
Brief bursts of nonpolarizing electrical brain stimulation were presented once each day at constant intensity. At first the stimulation had little effect on behavior and did not cause electrographic afterdischarge. With repetition the response to stimulation progressively changed to include localized seizure discharge, behavioral automatisms and, eventually, bilateral clonic convulsions. Thereafter, the animal responded to each daily burst of stimulation with a complete convulsion. The effect was obtained from bipolar stimulation of loci associated with the limbic system, but not from stimulation of many other regions of the brain. Parametric studies and control observations revealed that the effect was due to electrical activation and not to tissue damage, poison, edema, or gliosis. The changes in brain function were shown to be both permanent and trans-synaptic in nature. Massed-trial stimulation, with short inter-burst intervals, rarely led to convulsions. The number of stimulation trials necessary to elicit the first convulsion decreased as the interval between trials approached 24 hours. Further increase in the inter-trial interval had little effect on the number of trials to first convulsion. High-intensity stimulation studies revealed that the development of convulsions was not based simply on threshold reduction, but involved complex reorganization of function. Experiments with two electrodes in separate parts of the limbic system revealed that previously established convulsions could facilitate the establishment of a second convulsive focus, but that the establishment of this second convulsive focus partially suppressed the otherwise permanent convulsive properties of the original focus.
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