Spatiotemporal characteristics of pain-associated neuronal activities in primary somatosensory cortex induced by peripheral persistent nociception

Chang, Ying-Jen; Yan, Lai-Hong; Zhang, Fu-Kang; Gong, Kerui; Liu, Ming-Gang; Xiao, Yutao; Xie, Fang; Han, Fangfang

doi:10.1016/j.neulet.2008.08.090

Cited by 17 publications

(12 citation statements)

References 26 publications

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“…However, it should be noted that the local circuit is likely to be re-organized or changed by peripheral persistent nociception under pathological conditions. In our previous immunohistochemical study, we observed a robust increase in activation of c-Fos-expressing cells within layers II-III of the hindlimb representation of the rat S1 area following contralateral injection of bee venom into the hindpaw pad, a model of persistent inflammatory pain [34] . Future experiments are directed towards explicating the effect of peripheral persistent nociception on the spatial map of local circuitry in the S1 cortex.…”

Section: Spatial Map Of Neural Circuit In the Hindlimb Represen-mentioning

confidence: 84%

Neural circuits and temporal plasticity in hindlimb representation of rat primary somatosensory cortex: revisited by multi-electrode array on brain slices

Wang

Chang

et al. 2010

Neurosci. Bull.

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Objective 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).Methods 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, 8×8 array) for simultaneous multi-site electrophysiological recordings. Current sources and sinks across all the 64 electrodes were transformed into twodimensional current source density images by bilinear interpolation at each point of the 64 electrodes. Results 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. Conclusion 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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Section: Spatial Map Of Neural Circuit In the Hindlimb Represen-mentioning

confidence: 84%

Neural circuits and temporal plasticity in hindlimb representation of rat primary somatosensory cortex: revisited by multi-electrode array on brain slices

Wang

Chang

et al. 2010

Neurosci. Bull.

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“…In all three animals, there are labeled cells in the same structures as in CAT2. The lower Fos-immunoreactivity in CAT3 may reflect the limited time course of c-Fos gene expression (Hughes and Dragunow, 1995), rather than a lower effectiveness of the high velocity of rotation; a recent study found a reduction in Fos-immunoreactivity in somatosensory cortex beyond two hours, despite the persistently painful stimulation of bee venom (Chang et al, 2008). …”

Section: Resultsmentioning

confidence: 99%

Otolith stimulation induces c-Fos expression in vestibular and precerebellar nuclei in cats and squirrel monkeys

2010

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Vestibular information is critical for the control of balance, posture, and eye movements. Signals from the receptors, the semicircular canals and otoliths, are carried by the eighth nerve and distributed to the four nuclei of the vestibular nuclear complex, the VNC. However, anatomical and physiological data suggest that many additional brainstem nuclei are engaged in the processing of vestibular signals and generation of motor responses. In order to assess the role of these structures in vestibular functions, we have used expression of the immediate early gene cFos as a marker for neurons activated by stimulation of the otoliths or the semicircular canals. Excitation of the otolith organs resulted in widespread c-Fos expression in the VNC, but also in other nuclei, including the external cuneate nucleus, the postpyramidal nucleus of the raphé, the nucleus prepositus hypoglossi, the subtrigeminal nucleus, the pontine nuclei, the dorsal tegmental nucleus, the locus coeruleus and the reticular formation. Rotations that excited the semicircular canals were much less effective in inducing c-Fos expression. The large number of brainstem nuclei that showed c-Fos expression may reflect the multiple functions of the vestibular system. Some of these neurons may be involved in sensory processing of the vestibular signals, while others provide input to the vestibulo-ocular, vestibulocollic and vestibulospinal reflexes, or mediate changes in autonomic function. The data show that otolith stimulation engages brainstem structures both within and outside of the VNC, many of which project to the cerebellum.

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“…Recently, we found that BV-induced persistent pain produced long-lasting activation of mitogen-activated protein kinase subfamily members in both S1 area and HF [ 37 , 85 ]. Up-regulation of c-Fos protein was also predominantly localized within layer II-III of the S1 region in response to intraplantar BV injection [ 86 ]. Taken together, the spatial plasticity of synaptic connection and organization might be caused by persistent nociceptive drive produced by long-lasting activation and sensitization of primary nociceptors and spinal dorsal horn nociceptive neurons [ 72 , 73 ].…”

Section: Discussionmentioning

confidence: 99%

Nociception-Induced Spatial and Temporal Plasticity of Synaptic Connection and Function in the Hippocampal Formation of Rats: a Multi-Electrode Array Recording

et al. 2009

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BackgroundPain is known to be processed by a complex neural network (neuromatrix) in the brain. It is hypothesized that under pathological state, persistent or chronic pain can affect various higher brain functions through ascending pathways, leading to co-morbidities or mental disability of pain. However, so far the influences of pathological pain on the higher brain functions are less clear and this may hinder the advances in pain therapy. In the current study, we studied spatiotemporal plasticity of synaptic connection and function in the hippocampal formation (HF) in response to persistent nociception.ResultsOn the hippocampal slices of rats which had suffered from persistent nociception for 2 h by receiving subcutaneous bee venom (BV) or formalin injection into one hand paw, multisite recordings were performed by an 8 × 8 multi-electrode array probe. The waveform of the field excitatory postsynaptic potential (fEPSP), induced by perforant path electrical stimulation and pharmacologically identified as being activity-dependent and mediated by ionotropic glutamate receptors, was consistently positive-going in the dentate gyrus (DG), while that in the CA1 was negative-going in shape in naïve and saline control groups. For the spatial characteristics of synaptic plasticity, BV- or formalin-induced persistent pain significantly increased the number of detectable fEPSP in both DG and CA1 area, implicating enlargement of the synaptic connection size by the injury or acute inflammation. Moreover, the input-output function of synaptic efficacy was shown to be distinctly enhanced by the injury with the stimulus-response curve being moved leftward compared to the control. For the temporal plasticity, long-term potentiation produced by theta burst stimulation (TBS) conditioning was also remarkably enhanced by pain. Moreover, it is strikingly noted that the shape of fEPSP waveform was drastically deformed or split by a TBS conditioning under the condition of persistent nociception, while that in naïve or saline control state was not affected. All these changes in synaptic connection and function, confirmed by the 2-dimentional current source density imaging, were found to be highly correlated with peripheral persistent nociception since pre-blockade of nociceptive impulses could eliminate all of them. Finally, the initial pharmacological investigation showed that AMPA/KA glutamate receptors might play more important roles in mediation of pain-associated spatiotemporal plasticity than NMDA receptors.ConclusionPeripheral persistent nociception produces great impact upon the higher brain structures that lead to not only temporal plasticity, but also spatial plasticity of synaptic connection and function in the HF. The spatial plasticity of synaptic activities is more complex than the temporal plasticity, comprising of enlargement of synaptic connection size at network level, deformed fEPSP at local circuit level and, increased synaptic efficacy at cellular level. In addition, the multi-synaptic model established in the pres...

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Spatiotemporal characteristics of pain-associated neuronal activities in primary somatosensory cortex induced by peripheral persistent nociception

Cited by 17 publications

References 26 publications

Neural circuits and temporal plasticity in hindlimb representation of rat primary somatosensory cortex: revisited by multi-electrode array on brain slices

Neural circuits and temporal plasticity in hindlimb representation of rat primary somatosensory cortex: revisited by multi-electrode array on brain slices

Otolith stimulation induces c-Fos expression in vestibular and precerebellar nuclei in cats and squirrel monkeys

Nociception-Induced Spatial and Temporal Plasticity of Synaptic Connection and Function in the Hippocampal Formation of Rats: a Multi-Electrode Array Recording

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