Elsevier

Brain Research Bulletin

Volume 81, Issue 6, 5 April 2010, Pages 574-578
Brain Research Bulletin

Research report
Plasticity changes of neuronal activities in central lateral nucleus by stimulation of the anterior cingulate cortex in rat

https://doi.org/10.1016/j.brainresbull.2009.12.009Get rights and content

Abstract

The medial thalamus (MT) and anterior cingulate cortex (ACC) are essential components in mediating the affective emotional-aspect of pain. Whether ACC modulates the neuron activity in MT has not been elucidated and clarifying this point will further reveal the neurobiological mechanism underlying pain related emotions. In the present study, we used in vivo single unit recording and retrograde tracing technique to demonstrate that the majority of examined neurons in the central lateral nucleus (CL), an important nucleus of MT, responded to noxious stimulation. Tetanic stimulation in the ACC increased spike activities of nociceptive-responding neurons in the CL; retrograde tracing by fluorogold in the CL showed the positive neurons are distributed bilaterally in the ACC. Taken together, we demonstrated descending modulation to nociceptive responses of CL neurons by direct projections from the ACC, which may underlie the neuronal mechanism of negative pain emotions.

Introduction

Pain experience includes two major components: sensory-discrimination and affective emotion, which are represented and processed in the lateral and medial systems respectively [22]. The former proceeds via the lateral thalamus to the somatosensory cortex, which is thought to transmit information about the detection of noxious stimuli [4]. The latter proceeds via the medial/intralaminar thalamic nucleus to the limbic cortex, which is thought to process information leading to pain's perception as unpleasant [22], [24].

The anterior cingulate cortex (ACC), an important structure of the limbic system, is consistently activated by painful stimuli. Results from a variety of studies, including electrophysiology, positron emission tomography (PET), and animal behavior have indicated that the ACC is involved not only in the processing of both the sensory and emotional components of pain, but also in the modulation of descending facilitation on spinal nociceptive transmission [16], [12], [13], [28], [30], [5]. The central lateral nucleus (CL) is an important structure of the medial/intralaminar thalamus, which is involved in the processing of somatic and visceral nociceptive information [18], [3]. The pathway of information from CL to ACC constitutes an important part of the medial pain system in the mediation of affective response [22], [24], [13], [25].

Accumulating evidence indicates that changes in cortex can trigger plasticity responses in the thalamus and that the regulation of neuronal activities in the thalamus is partially mediated by feedback inputs from the cortex [9], [15]. It has also been shown that the ACC presents plastic changes under chronic pain conditions [27], and that changes in molecular expression in the ACC affect the emotional behavior of pain [5]. However, whether the ACC exerts descending modulation on the neuronal activities in the medial thalamic nucleus remains largely unknown. To address this issue, we employed in vivo single unit recording and retrograde tracing technique in rats to investigate the descending modulation of the ACC on the neurons of CL in the present study.

Section snippets

Animal preparation

Male Sprague–Dawley rats (250–300 g body weight) were used in this study and supplied by the Experimental Animal Center of Fudan University. Urethane carbamate (1.5 g/kg, i.p.) was used for anesthesia. After tracheal intubation, the rat was mounted in a sterotaxic apparatus (SN-2; Narishige, Japan). After parting the skin and exposing the skull, two small holes were drilled on the skull to allow electrode penetration. One small hole was drilled for inserting electrodes to the CL (−2.8 to 3.3 mm

Spontaneous activities and responses of CL neurons to mechanical stimulation

A total of 106 neurons within or adjacent to the CL were isolated from 50 rats and studied. A histology examination revealed that 97 neurons were in the CL while the other 9 neurons were in the medial dorsal (MD) nucleus which is located medial to the CL (Fig. 1B). Most neurons showed spontaneous activities with an average firing rate of 4.87 ± 0.49 Hz. We observed the receptive fields (Rf) of 30 neurons in the CL. Six (20%) of them presented contralateral Rf to the recording, whereas the other 24

Discussion

In the present study, we first observed the response of neurons in the CL to various stimuli. Then we investigated changes in the activity of the CL neurons resulting from high-frequency tetanic stimulation of the ACC. Finally, we traced the fibers that project from the ACC to the CL by fluorogold. Our study provides the first evidence showing that high-frequency electrical stimulation of the ACC produces increased neuronal activities in most CL nociceptive neurons, which receive direct

Acknowledgements

We thank Dr. Long-Jun Wu and Miss Sara Gallant for the revising of this paper. This work was supported by grant from the National Natural Science Fund of China (NSFC) grants 30600171, 30830044 and 30670694, and the National Basic Research Program of China grants 2006CB500800 and 2006CB500807.

References (30)

  • X.C. Zhang et al.

    Different roles of two nitric oxide activated pathways in spinal long-term potentiation of C-fiber-evoked field potentials

    Neuropharmacology

    (2006)
  • C. Baleydier et al.

    The duality of the cingulate gyrus in monkey. Neuroanatomical study and functional hypothesis

    Brain

    (1980)
  • M.C. Bushnell

    Pain perception: is there a role for primary somatosensory cortex?

    Proc. Natl. Acad. Sci. U.S.A.

    (1999)
  • H. Cao

    Activation of extracellular signal-regulated kinase in the anterior cingulate cortex contributes to the induction and expression of affective pain

    J. Neurosci.

    (2009)
  • F. Cervero et al.

    Effects of noxious stimulation of the skin on transmission through the spinocervical tract

    J. Physiol.

    (1976)
  • Cited by (0)

    View full text