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Restoration of function after cortical lesion: does it require an internal template?

Schulze H, Tziridis K - Neural Regen Res (2014)

View Article: PubMed Central - PubMed

Affiliation: Experimental Otolaryngology, Friedrich-Alexander University Erlangen-N├╝rnberg, Waldstrasse 1, 91054 Erlangen, Germany.

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As the basic body anatomy of all vertebrates has a bilateral symmetry, structures and functions of vertebrate brains are also organized according to this fundamental anatomical principle to meet all sensory, motor, and internal requirements of body control... On the other hand, many functions are bilaterally organized so the brain may still be able to solve certain tasks after unilateral lesion of a particular brain structure, for example in cases where symmetric sensory systems process redundant information, by using the respective undamaged contralateral structure (Schulze et al., 2014)... This was true for animals that received bilateral AC ablation prior to the first training session and also for those that had learned to solve the task during 15 days of training with single daily training session prior to the bilateral lesion surgery... As we could demonstrate in a follow-up study, unilateral lesion of the AC did not result in a complete loss of the ability to discriminate fast AM in our animal model (Schulze et al., 2014)... Finally, in a third study (Depner et al., 2014), we described the effect of a serial bilateral ablation of AC on the discrimination performance of fast AM in our animal model... We then continued to train the animals in the fast AM discrimination task for another 15 training session, followed by a second lesion surgery where the AC contralateral to the side lesioned initially was ablated... Surprisingly we found that these animals were still able to perform the task as well as sham lesioned controls, even after complete lesion of both AC... That is, in contrast to simultaneous bilateral AC lesion that totally extinguished the ability to solve the task in our animals, serial lesion of both AC in two consecutive surgeries with continuing training in between the two unilateral lesions fully conserved the ability to discriminate between the two stimuli... It refers to the “finding that serially placed lesions of the brain with some minimum time between lesions result in less severe residual deficits than do simultaneous lesions of equal extent and comparable loci” (Schmidt, 1976)... But in contrast to our report the serial lesion effect typically does not lead to fully conserved function of the lesioned loci, but rather enables the system to better recover from brain damage although the function still remains impaired to some extent so that restoration of function is incomplete (e.g., Barbas and Spear, 1976)... The same training is ineffective if ACs of both hemispheres are ablated simultaneously (Deutscher et al., 2006)... These results clearly demonstrate that after unilateral lesion of the first AC an intact contralateral AC is needed to successfully enable potential substitute structures to take over the lost function by functionally reorganizing themselves... This compensatory plasticity seems to be triggered by the first lesion, thereby opening a time window for possible new therapeutic interventions that aim to strengthen the proposed transfer process... If the training that we applied in our animal model in between the two sequential AC lesions could be a model for such a therapeutic intervention is currently unclear, as we do not know if the compensatory plasticity we described would not have taken place without that training, although it is likely that training indeed is needed (Scheff and Wright, 1977)... If the latter would be the case, new therapeutic strategies may be developed to maximize the benefit of the serial lesion effect in sensory or motor modalities where rehabilitation after brain lesion is still unsatisfactory.

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Schematic overview over effects of different avditory cortex (AC) lesion types on discrimination performance of fast amplitude modulations (AM) in Mongolian Gerbil.Whereas it is completely impossible for the animals to solve the task after bilateral AC lesion (A), the task is still possible after unilateral lesion of the AC of one hemisphere (B). Surprisingly, if AC of both hemispheres are not ablated simultaneously but sequentially, with 15 daily sessions of continuing discrimination training after the first unilateral lesion, the task is still possible after the second lesion of the contralateral AC (C).
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Figure 1: Schematic overview over effects of different avditory cortex (AC) lesion types on discrimination performance of fast amplitude modulations (AM) in Mongolian Gerbil.Whereas it is completely impossible for the animals to solve the task after bilateral AC lesion (A), the task is still possible after unilateral lesion of the AC of one hemisphere (B). Surprisingly, if AC of both hemispheres are not ablated simultaneously but sequentially, with 15 daily sessions of continuing discrimination training after the first unilateral lesion, the task is still possible after the second lesion of the contralateral AC (C).

Mentions: In the auditory discrimination task investigated here, the animals had to discriminate AM with periodicities of 160 vs. 320 Hz in a shuttle-box GO-NOGO paradigm. In contrast to slow AM with periodicities of 20 vs. 40 Hz, it was completely impossible for the animals to solve the task after bilateral lesion of AC (Deutscher et al., 2006). This was true for animals that received bilateral AC ablation prior to the first training session and also for those that had learned to solve the task during 15 days of training with single daily training session prior to the bilateral lesion surgery (Figure 1A). As we could demonstrate in a follow-up study, unilateral lesion of the AC did not result in a complete loss of the ability to discriminate fast AM in our animal model (Schulze et al., 2014). Obviously an intact AC in one hemisphere was sufficient to solve the task (Figure 1B), although we were able to report subtle differences between left and right AC lesion.


Restoration of function after cortical lesion: does it require an internal template?

Schulze H, Tziridis K - Neural Regen Res (2014)

Schematic overview over effects of different avditory cortex (AC) lesion types on discrimination performance of fast amplitude modulations (AM) in Mongolian Gerbil.Whereas it is completely impossible for the animals to solve the task after bilateral AC lesion (A), the task is still possible after unilateral lesion of the AC of one hemisphere (B). Surprisingly, if AC of both hemispheres are not ablated simultaneously but sequentially, with 15 daily sessions of continuing discrimination training after the first unilateral lesion, the task is still possible after the second lesion of the contralateral AC (C).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4316459&req=5

Figure 1: Schematic overview over effects of different avditory cortex (AC) lesion types on discrimination performance of fast amplitude modulations (AM) in Mongolian Gerbil.Whereas it is completely impossible for the animals to solve the task after bilateral AC lesion (A), the task is still possible after unilateral lesion of the AC of one hemisphere (B). Surprisingly, if AC of both hemispheres are not ablated simultaneously but sequentially, with 15 daily sessions of continuing discrimination training after the first unilateral lesion, the task is still possible after the second lesion of the contralateral AC (C).
Mentions: In the auditory discrimination task investigated here, the animals had to discriminate AM with periodicities of 160 vs. 320 Hz in a shuttle-box GO-NOGO paradigm. In contrast to slow AM with periodicities of 20 vs. 40 Hz, it was completely impossible for the animals to solve the task after bilateral lesion of AC (Deutscher et al., 2006). This was true for animals that received bilateral AC ablation prior to the first training session and also for those that had learned to solve the task during 15 days of training with single daily training session prior to the bilateral lesion surgery (Figure 1A). As we could demonstrate in a follow-up study, unilateral lesion of the AC did not result in a complete loss of the ability to discriminate fast AM in our animal model (Schulze et al., 2014). Obviously an intact AC in one hemisphere was sufficient to solve the task (Figure 1B), although we were able to report subtle differences between left and right AC lesion.

View Article: PubMed Central - PubMed

Affiliation: Experimental Otolaryngology, Friedrich-Alexander University Erlangen-N├╝rnberg, Waldstrasse 1, 91054 Erlangen, Germany.

AUTOMATICALLY GENERATED EXCERPT
Please rate it.

As the basic body anatomy of all vertebrates has a bilateral symmetry, structures and functions of vertebrate brains are also organized according to this fundamental anatomical principle to meet all sensory, motor, and internal requirements of body control... On the other hand, many functions are bilaterally organized so the brain may still be able to solve certain tasks after unilateral lesion of a particular brain structure, for example in cases where symmetric sensory systems process redundant information, by using the respective undamaged contralateral structure (Schulze et al., 2014)... This was true for animals that received bilateral AC ablation prior to the first training session and also for those that had learned to solve the task during 15 days of training with single daily training session prior to the bilateral lesion surgery... As we could demonstrate in a follow-up study, unilateral lesion of the AC did not result in a complete loss of the ability to discriminate fast AM in our animal model (Schulze et al., 2014)... Finally, in a third study (Depner et al., 2014), we described the effect of a serial bilateral ablation of AC on the discrimination performance of fast AM in our animal model... We then continued to train the animals in the fast AM discrimination task for another 15 training session, followed by a second lesion surgery where the AC contralateral to the side lesioned initially was ablated... Surprisingly we found that these animals were still able to perform the task as well as sham lesioned controls, even after complete lesion of both AC... That is, in contrast to simultaneous bilateral AC lesion that totally extinguished the ability to solve the task in our animals, serial lesion of both AC in two consecutive surgeries with continuing training in between the two unilateral lesions fully conserved the ability to discriminate between the two stimuli... It refers to the “finding that serially placed lesions of the brain with some minimum time between lesions result in less severe residual deficits than do simultaneous lesions of equal extent and comparable loci” (Schmidt, 1976)... But in contrast to our report the serial lesion effect typically does not lead to fully conserved function of the lesioned loci, but rather enables the system to better recover from brain damage although the function still remains impaired to some extent so that restoration of function is incomplete (e.g., Barbas and Spear, 1976)... The same training is ineffective if ACs of both hemispheres are ablated simultaneously (Deutscher et al., 2006)... These results clearly demonstrate that after unilateral lesion of the first AC an intact contralateral AC is needed to successfully enable potential substitute structures to take over the lost function by functionally reorganizing themselves... This compensatory plasticity seems to be triggered by the first lesion, thereby opening a time window for possible new therapeutic interventions that aim to strengthen the proposed transfer process... If the training that we applied in our animal model in between the two sequential AC lesions could be a model for such a therapeutic intervention is currently unclear, as we do not know if the compensatory plasticity we described would not have taken place without that training, although it is likely that training indeed is needed (Scheff and Wright, 1977)... If the latter would be the case, new therapeutic strategies may be developed to maximize the benefit of the serial lesion effect in sensory or motor modalities where rehabilitation after brain lesion is still unsatisfactory.

No MeSH data available.