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Spatial and temporal plasticity of synaptic organization in anterior cingulate cortex following peripheral inflammatory pain: multi-electrode array recordings in rats.

ABSTRACT: To explore whether experiencing inflammatory pain has an impact upon intracortical synaptic organization, the planar multi-electrode array (MEA) technique and 2-dimensional current source density (2D-CSD) imaging were used in slice preparations of the anterior cingulate cortex (ACC) from rats. Synaptic activity across different layers of the ACC was evoked by deep layer stimulation through one electrode. The layer-localization of both local field potentials (LFPs) and the spread of current sink calculated by 2D-CSD analysis was characterized pharmacologically. Moreover, the induction of long-term potentiation (LTP) and changes in LTP magnitude were also evaluated. We found that under naïve conditions, the current sink was initially generated in layer VI, then spread to layer V and finally confined to layers II-III. This spatial pattern of current sink movement typically reflected changes in depolarized sites from deep layers (V-VI) to superficial layers (II-III) where intra- and extracortical inputs terminate. In the ACC slices from rats in an inflamed state (for 2 h) caused by intraplantar bee-venom injection, the spatial profile of intra-ACC synaptic organization was significantly changed, showing an enlarged current sink distribution and a leftward shift of the stimulus-response curves relative to the naïve and saline controls. The change was more distinct in the superficial layers (II-III) than in the deep site. In terms of temporal properties, the rate of LTP induction was significantly increased in layers II-III by inflammatory pain. However, the magnitude of LTP was not significantly enhanced by this treatment. Taken together, these results show that inflammatory pain results in distinct spatial and temporal plasticity of synaptic organization in the ACC, which may lead to altered synaptic transmission and modulation.

SUBMITTER: Lu YF

PROVIDER: S-EPMC5561851 | biostudies-other | 2014 Feb

REPOSITORIES: biostudies-other

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Project description:There is substantial evidence supporting the notion that the anterior cingulate cortex (ACC) is an important limbic structure involved in multiple brain functions such as sensory perception, motor conflict monitoring, memory, emotion and cognition. It has been shown that long term potentiation (LTP) is an important synaptic model of neural plasticity in the ACC, however, little is known about the spatiotemporal properties of ACC at network level. The present study was designed to see the LTP induction effects across different layers of the ACC by using different conditioning stimuli (CS) protocols.A unique multi-electrode array recording technique was used in the acutely-dissociated ACC slices of rats. Long and short train theta burst stimulation (TBS) paradigms were applied in layer V-VI as the CS and the LTP induction effects were compared across different layers of the ACC. Briefly, both long and short train TBS are composed of bursts (4 pulses at 100 Hz) with a 200 ms interval, however, the former (TBS1) was with 10 trains and the latter (TBS2) was with 5 trains. After test stimulation at layer V-VI in the ACC, network field potentials (FPs) could be simultaneously recorded across all layers of the ACC.The waveforms of FPs were different across different layers. Namely, positive-going waveforms were recorded in layer I and negative-going waveforms were recorded in layers V-VI, in contrast, complex waveforms were localized mainly in layers II-III. Following application of two CS protocols, the induction rate of LTP was significantly different between TBS1 and TBS2 regardless of the spatial properties. TBS1 had more than 60% success, while TBS2 was less than 25% in induction of LTP. Moreover, both the 2 CS protocols could induce LTP in layers II-III and layers V-VI without layer-related difference. However, no LTP was inducible in layer I.The present findings indicate that stimulation protocols may, at least in part, account for a large portion of variations among previous LTP studies, and hence highlight the importance of selecting the best LTP induction protocol when designing such experiments. Moreover, the present results demonstrate the prominent superiority of multi-electrode array recording in revealing the network properties of synaptic activities in the ACC, especially in comparing the spatiotemporal characteristics between different layers of this structure.

Project description:The well-established planar multi-electrode array recording technique was used to investigate neural circuits and temporal plasticity in the hindlimb representation of the rat primary somatosensory cortex (S1 area).Freshly dissociated acute brain slices of rats were subject to constant perfusion with oxygenated artificial cerebrospinal fluid (95% O(2) and 5% CO(2)), and were mounted on a Med64 probe (64 electrodes, 8x8 array) for simultaneous multi-site electrophysiological recordings. Current sources and sinks across all the 64 electrodes were transformed into two-dimensional current source density images by bilinear interpolation at each point of the 64 electrodes.The local intracortical connection, which is involved in mediation of downward information flow across layers II-VI, was identified by electrical stimulation (ES) at layers II-III. The thalamocortical connection, which is mainly involved in mediation of upward information flow across layers II-IV, was also characterized by ES at layer IV. The thalamocortical afferent projections were likely to make more synaptic contacts with S1 neurons than the intracortical connections did. Moreover, the S1 area was shown to be more easily activated and more intensively innervated by the thalamocortical afferent projections than by the intracortical connections. Finally, bursting conditioning stimulus (CS) applied within layer IV of the S1 area could successfully induce long-term potentiation (LTP) in 5 of the 6 slices (83.3%), while the same CS application at layers II-III induced no LTP in any of the 6 tested slices.The rat hindlimb representation of S1 area is likely to have at least 2 patterns of neural circuits on brain slices: one is the intracortical circuit (ICC) formed by interlaminar connections from layers II-III, and the other is the thalamocortical circuit (TCC) mediated by afferent connections from layer IV. Besides, ICC of the S1 area is spatially limited, with less plasticity, while TCC is spatially extensive and exhibits a better plasticity in response to somatosensory afferent stimulation. The present data provide a useful experimental model for further studying microcircuit properties in S1 cortex at the network level in vitro.

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Spatial and temporal plasticity of synaptic organization in anterior cingulate cortex following peripheral inflammatory pain: multi-electrode array recordings in rats.

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