Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling.
Cholinergic neuromodulation plays key roles in the regulation of neuronal excitability, network activity, arousal, and behavior. On longer time scales, cholinergic systems play essential roles in cortical development, maturation, and plasticity. Presumably, these processes are associated with substa...
| Main Authors: | , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2012-01-01
|
| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC3402441?pdf=render |
| _version_ | 1819077149353574400 |
|---|---|
| author | Maya Kaufman Michael A Corner Noam E Ziv |
| author_facet | Maya Kaufman Michael A Corner Noam E Ziv |
| author_sort | Maya Kaufman |
| collection | DOAJ |
| description | Cholinergic neuromodulation plays key roles in the regulation of neuronal excitability, network activity, arousal, and behavior. On longer time scales, cholinergic systems play essential roles in cortical development, maturation, and plasticity. Presumably, these processes are associated with substantial synaptic remodeling, yet to date, long-term relationships between cholinergic tone and synaptic remodeling remain largely unknown. Here we used automated microscopy combined with multielectrode array recordings to study long-term relationships between cholinergic tone, excitatory synapse remodeling, and network activity characteristics in networks of cortical neurons grown on multielectrode array substrates. Experimental elevations of cholinergic tone led to the abrupt suppression of episodic synchronous bursting activity (but not of general activity), followed by a gradual growth of excitatory synapses over hours. Subsequent blockage of cholinergic receptors led to an immediate restoration of synchronous bursting and the gradual reversal of synaptic growth. Neither synaptic growth nor downsizing was governed by multiplicative scaling rules. Instead, these occurred in a subset of synapses, irrespective of initial synaptic size. Synaptic growth seemed to depend on intrinsic network activity, but not on the degree to which bursting was suppressed. Intriguingly, sustained elevations of cholinergic tone were associated with a gradual recovery of synchronous bursting but not with a reversal of synaptic growth. These findings show that cholinergic tone can strongly affect synaptic remodeling and synchronous bursting activity, but do not support a strict coupling between the two. Finally, the reemergence of synchronous bursting in the presence of elevated cholinergic tone indicates that the capacity of cholinergic neuromodulation to indefinitely suppress synchronous bursting might be inherently limited. |
| first_indexed | 2024-12-21T18:52:36Z |
| format | Article |
| id | doaj.art-1784e3272af74f60a5c7033974766b09 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-21T18:52:36Z |
| publishDate | 2012-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-1784e3272af74f60a5c7033974766b092022-12-21T18:53:42ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0177e4098010.1371/journal.pone.0040980Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling.Maya KaufmanMichael A CornerNoam E ZivCholinergic neuromodulation plays key roles in the regulation of neuronal excitability, network activity, arousal, and behavior. On longer time scales, cholinergic systems play essential roles in cortical development, maturation, and plasticity. Presumably, these processes are associated with substantial synaptic remodeling, yet to date, long-term relationships between cholinergic tone and synaptic remodeling remain largely unknown. Here we used automated microscopy combined with multielectrode array recordings to study long-term relationships between cholinergic tone, excitatory synapse remodeling, and network activity characteristics in networks of cortical neurons grown on multielectrode array substrates. Experimental elevations of cholinergic tone led to the abrupt suppression of episodic synchronous bursting activity (but not of general activity), followed by a gradual growth of excitatory synapses over hours. Subsequent blockage of cholinergic receptors led to an immediate restoration of synchronous bursting and the gradual reversal of synaptic growth. Neither synaptic growth nor downsizing was governed by multiplicative scaling rules. Instead, these occurred in a subset of synapses, irrespective of initial synaptic size. Synaptic growth seemed to depend on intrinsic network activity, but not on the degree to which bursting was suppressed. Intriguingly, sustained elevations of cholinergic tone were associated with a gradual recovery of synchronous bursting but not with a reversal of synaptic growth. These findings show that cholinergic tone can strongly affect synaptic remodeling and synchronous bursting activity, but do not support a strict coupling between the two. Finally, the reemergence of synchronous bursting in the presence of elevated cholinergic tone indicates that the capacity of cholinergic neuromodulation to indefinitely suppress synchronous bursting might be inherently limited.http://europepmc.org/articles/PMC3402441?pdf=render |
| spellingShingle | Maya Kaufman Michael A Corner Noam E Ziv Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling. PLoS ONE |
| title | Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling. |
| title_full | Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling. |
| title_fullStr | Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling. |
| title_full_unstemmed | Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling. |
| title_short | Long-term relationships between cholinergic tone, synchronous bursting and synaptic remodeling. |
| title_sort | long term relationships between cholinergic tone synchronous bursting and synaptic remodeling |
| url | http://europepmc.org/articles/PMC3402441?pdf=render |
| work_keys_str_mv | AT mayakaufman longtermrelationshipsbetweencholinergictonesynchronousburstingandsynapticremodeling AT michaelacorner longtermrelationshipsbetweencholinergictonesynchronousburstingandsynapticremodeling AT noameziv longtermrelationshipsbetweencholinergictonesynchronousburstingandsynapticremodeling |