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Homeostatic structural plasticity can account for topology changes following deafferentation and focal stroke.

Butz M, Steenbuck ID, van Ooyen A - Front Neuroanat (2014)

Bottom Line: Homeostatic structural plasticity postulates that neurons aim to maintain a desired level of electrical activity by deleting synapses when neuronal activity is too high and by providing new synaptic contacts when activity is too low.Using our Model of Structural Plasticity, we explored how local changes in connectivity induced by a focal loss of input affected global network topology.Furthermore, deafferentated neurons increased their global but decreased their local efficiency and got longer tailed degree distributions, indicating the emergence of hub neurons.

View Article: PubMed Central - PubMed

Affiliation: Simulation Lab Neuroscience - Bernstein Facility for Simulation and Database Technology, Institute for Advanced Simulation, Jülich Aachen Research Alliance, Forschungszentrum Jülich Jülich, Germany.

ABSTRACT
After brain lesions caused by tumors or stroke, or after lasting loss of input (deafferentation), inter- and intra-regional brain networks respond with complex changes in topology. Not only areas directly affected by the lesion but also regions remote from the lesion may alter their connectivity-a phenomenon known as diaschisis. Changes in network topology after brain lesions can lead to cognitive decline and increasing functional disability. However, the principles governing changes in network topology are poorly understood. Here, we investigated whether homeostatic structural plasticity can account for changes in network topology after deafferentation and brain lesions. Homeostatic structural plasticity postulates that neurons aim to maintain a desired level of electrical activity by deleting synapses when neuronal activity is too high and by providing new synaptic contacts when activity is too low. Using our Model of Structural Plasticity, we explored how local changes in connectivity induced by a focal loss of input affected global network topology. In accordance with experimental and clinical data, we found that after partial deafferentation, the network as a whole became more random, although it maintained its small-world topology, while deafferentated neurons increased their betweenness centrality as they rewired and returned to the homeostatic range of activity. Furthermore, deafferentated neurons increased their global but decreased their local efficiency and got longer tailed degree distributions, indicating the emergence of hub neurons. Together, our results suggest that homeostatic structural plasticity may be an important driving force for lesion-induced network reorganization and that the increase in betweenness centrality of deafferentated areas may hold as a biomarker for brain repair.

No MeSH data available.


Related in: MedlinePlus

Degree distributions of intact zone (green) and LPZ neurons (red) before and after the lesion in the recurrent case. In the bar charts, the larger amount is always placed in the background and the minor amount in the foreground. Before the lesion, the in-degree (A) and out-degree distributions (B) are not tailed. After the lesion, the shapes of in-degree (C) and out-degree (D) distributions do not change markedly, but the centers of the in- and out-degree distributions of the LPZ neurons are shifted to the right. The diagram shows data from one simulation at T = 7950 and T = 20000 updates in connectivity, the latter corresponding to 24 weeks after lesion.
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Figure 10: Degree distributions of intact zone (green) and LPZ neurons (red) before and after the lesion in the recurrent case. In the bar charts, the larger amount is always placed in the background and the minor amount in the foreground. Before the lesion, the in-degree (A) and out-degree distributions (B) are not tailed. After the lesion, the shapes of in-degree (C) and out-degree (D) distributions do not change markedly, but the centers of the in- and out-degree distributions of the LPZ neurons are shifted to the right. The diagram shows data from one simulation at T = 7950 and T = 20000 updates in connectivity, the latter corresponding to 24 weeks after lesion.

Mentions: The different types of network rewiring have a direct impact not only on global network topology but also on the local degree distributions of neurons. Before the lesion, neurons of the intact zone and the LPZ have the same in- and out-degree distribution, in the physiological case (Figures 9A,B) as well as in the recurrent case (Figures 10A,B). The distributions in the physiological case are slightly more tailed than in the recurrent case. After the lesion in the physiological case, the center of the in-degree distribution of the LPZ neurons shifts to the right (Figure 9C), indicating the presence of neurons with high in-degrees. The centers of the out-degree distributions of LPZ and intact zone neurons do not change, but the distributions as a whole become more fat-tailed (Figure 9D). Thus, compensatory network rewiring generates more hub-like neurons in the LPZ, but the majority of neurons in the LPZ and the intact zone maintains its out-degree. In the recurrent case, LPZ neurons shift the centers of their in- and out-degree distributions completely to the right (Figure 10), but the distributions do not become more fat-tailed. The in- and out-degree distributions become markedly different from the ones before the lesion and from the degree distributions of the intact zone neurons. We may conclude that due to the massive recurrent connections, the LPZ neurons separate from the intact zone in terms of degree distribution.


Homeostatic structural plasticity can account for topology changes following deafferentation and focal stroke.

Butz M, Steenbuck ID, van Ooyen A - Front Neuroanat (2014)

Degree distributions of intact zone (green) and LPZ neurons (red) before and after the lesion in the recurrent case. In the bar charts, the larger amount is always placed in the background and the minor amount in the foreground. Before the lesion, the in-degree (A) and out-degree distributions (B) are not tailed. After the lesion, the shapes of in-degree (C) and out-degree (D) distributions do not change markedly, but the centers of the in- and out-degree distributions of the LPZ neurons are shifted to the right. The diagram shows data from one simulation at T = 7950 and T = 20000 updates in connectivity, the latter corresponding to 24 weeks after lesion.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4199279&req=5

Figure 10: Degree distributions of intact zone (green) and LPZ neurons (red) before and after the lesion in the recurrent case. In the bar charts, the larger amount is always placed in the background and the minor amount in the foreground. Before the lesion, the in-degree (A) and out-degree distributions (B) are not tailed. After the lesion, the shapes of in-degree (C) and out-degree (D) distributions do not change markedly, but the centers of the in- and out-degree distributions of the LPZ neurons are shifted to the right. The diagram shows data from one simulation at T = 7950 and T = 20000 updates in connectivity, the latter corresponding to 24 weeks after lesion.
Mentions: The different types of network rewiring have a direct impact not only on global network topology but also on the local degree distributions of neurons. Before the lesion, neurons of the intact zone and the LPZ have the same in- and out-degree distribution, in the physiological case (Figures 9A,B) as well as in the recurrent case (Figures 10A,B). The distributions in the physiological case are slightly more tailed than in the recurrent case. After the lesion in the physiological case, the center of the in-degree distribution of the LPZ neurons shifts to the right (Figure 9C), indicating the presence of neurons with high in-degrees. The centers of the out-degree distributions of LPZ and intact zone neurons do not change, but the distributions as a whole become more fat-tailed (Figure 9D). Thus, compensatory network rewiring generates more hub-like neurons in the LPZ, but the majority of neurons in the LPZ and the intact zone maintains its out-degree. In the recurrent case, LPZ neurons shift the centers of their in- and out-degree distributions completely to the right (Figure 10), but the distributions do not become more fat-tailed. The in- and out-degree distributions become markedly different from the ones before the lesion and from the degree distributions of the intact zone neurons. We may conclude that due to the massive recurrent connections, the LPZ neurons separate from the intact zone in terms of degree distribution.

Bottom Line: Homeostatic structural plasticity postulates that neurons aim to maintain a desired level of electrical activity by deleting synapses when neuronal activity is too high and by providing new synaptic contacts when activity is too low.Using our Model of Structural Plasticity, we explored how local changes in connectivity induced by a focal loss of input affected global network topology.Furthermore, deafferentated neurons increased their global but decreased their local efficiency and got longer tailed degree distributions, indicating the emergence of hub neurons.

View Article: PubMed Central - PubMed

Affiliation: Simulation Lab Neuroscience - Bernstein Facility for Simulation and Database Technology, Institute for Advanced Simulation, Jülich Aachen Research Alliance, Forschungszentrum Jülich Jülich, Germany.

ABSTRACT
After brain lesions caused by tumors or stroke, or after lasting loss of input (deafferentation), inter- and intra-regional brain networks respond with complex changes in topology. Not only areas directly affected by the lesion but also regions remote from the lesion may alter their connectivity-a phenomenon known as diaschisis. Changes in network topology after brain lesions can lead to cognitive decline and increasing functional disability. However, the principles governing changes in network topology are poorly understood. Here, we investigated whether homeostatic structural plasticity can account for changes in network topology after deafferentation and brain lesions. Homeostatic structural plasticity postulates that neurons aim to maintain a desired level of electrical activity by deleting synapses when neuronal activity is too high and by providing new synaptic contacts when activity is too low. Using our Model of Structural Plasticity, we explored how local changes in connectivity induced by a focal loss of input affected global network topology. In accordance with experimental and clinical data, we found that after partial deafferentation, the network as a whole became more random, although it maintained its small-world topology, while deafferentated neurons increased their betweenness centrality as they rewired and returned to the homeostatic range of activity. Furthermore, deafferentated neurons increased their global but decreased their local efficiency and got longer tailed degree distributions, indicating the emergence of hub neurons. Together, our results suggest that homeostatic structural plasticity may be an important driving force for lesion-induced network reorganization and that the increase in betweenness centrality of deafferentated areas may hold as a biomarker for brain repair.

No MeSH data available.


Related in: MedlinePlus