Intracortical Circuits in Rat Anterior Cingulate Cortex Are Activated by Nociceptive Inputs Mediated by Medial Thalamus

Jenq-Wei Yang, Hsi-Chien Shih, Bai-Chuang Shyu
2006 Journal of Neurophysiology  
Intracortical circuits in rat anterior cingulate cortex are activated by nociceptive inputs mediated by medial thalamus. . We investigated the afferents and intracortical synaptic organization of the anterior cingulate cortex (ACC) during noxious electrical stimulation. Extracellular field potentials were recorded simultaneously from 16 electrodes spanning all layers of the ACC in male Sprague-Dawley rats anesthetized by halothane inhalation. Laminar-specific transmembrane currents were
more » ... ed with the current source density analysis method. Two major groups of evoked sink currents were identified: an early group (latency ϭ 54.04 Ϯ 2.12 ms; 0.63 Ϯ 0.07 mV/mm 2 ) in layers V-VI and a more intense late group (latency ϭ 80.07 Ϯ 4.85 ms; 2.16 Ϯ 0.22 mV/mm 2 ) in layer II/III and layer V. Multiunit activities were evoked mainly in layer V and deep layer II/III with latencies similar to that of the early and late sink groups. The evoked EPSP latencies of pyramidal neurons in layers II/III and V related closely with the sink currents. The sink currents were inhibited by intracortical injection of CNQX (1 mM, 1 l), a glutaminergic receptor antagonist, and enhanced by intraperitoneal (5 mg/kg) and intracortical (10 g/l, 1 l) injection of morphine, a -opioid receptor agonist. Paired-pulse depression was observed with interpulse intervals of 50 to 1,000 ms. High-frequency stimulation (100 Hz, 11 pulses) enhanced evoked responses in the ACC and evoked medial thalamic (MT) unit activities. MT lesions blocked evoked responses in the ACC. Our results demonstrated that two distinct synaptic circuits in the ACC were activated by noxious stimuli and that the MT is the major thalamic relay that transmits nociceptive information to the ACC. Adreani CM, Hill JM, and Kaufman MP. Responses of group III and IV muscle afferents to dynamic exercise. Bantick SJ, Wise RG, Ploghaus A, Clare S, Smith SM, and Tracey I. Imaging how attention modulates pain in humans using functional MRI. Brain 125: 310 -319, 2002. Berendse HW and Groenewegen HJ. Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42: 73-102, 1991. Berkley KJ, Benoist JM, Gautron M, and Guilbaud G. Responses of neurons in the caudal intralaminar thalamic complex of the rat to stimulation of the uterus, vagina, cervix, colon and skin. Brain Res 695: 92-95, 1995. Branchereau P, Van Bockstaele EJ, Chan J, and Pickel VM. Pyramidal neurons in rat prefrontal cortex show a complex synaptic response to single electrical stimulation of the locus coeruleus region: evidence for antidromic activation and GABAergic inhibition using in vivo intracellular recording and electron microscopy. Synapse 22: 313-331, 1996. Brooks JC, Nurmikko TJ, Bimson WE, Singh KD, and Roberts N. fMRI of thermal pain: effects of stimulus laterality and attention. Neuroimage 15: 293-301, 2002. Calejesan AA, Kim SJ, and Zhuo M. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur J Pain 4: 83-96, 2000. Casey KL. Forebrain mechanisms of nociception and pain: analysis through imaging. Proc Natl Acad Sci USA 96: 7668 -7674, 1999. Casey KL, Morrow TJ, Lorenz J, and Minoshima S. Temporal and spatial dynamics of human forebrain activity during heat pain: analysis by positron emission tomography. J Neurophysiol 85: 951-959, 2001. Casey KL, Svensson P, Morrow TJ, Raz J, Jone C, and Minoshima S. Selective opiate modulation of nociceptive processing in the human brain. J Neurophysiol 84: 525-533, 2000. Castro-Alamancos MA and Connors BW. Cellular mechanisms of the augmenting response: short-term plasticity in a thalamocortical pathway. J Neurosci 16: 7742-7756, 1996. Cauller LJ and Connors BW. Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex. J Neurosci 14: 751-762, 1994. Chang C and Shyu BC. A fMRI study of brain activations during nonnoxious and noxious electrical stimulation of the sciatic nerve of rats. Brain Res 897: 71-81, 2001. Chiou LC and Huang LY. Mechanism underlying increased neuronal activity in the rat ventrolateral periaqueductal grey by a mu-opioid. J Physiol 518: 551-559, 1999. Coghill RC, Sang CN, Maisog JM, and Iadarola MJ. Pain intensity processing within the human brain: a bilateral, distributed mechanism. Davis KD, Taylor SJ, Crawley AP, Wood ML, and Mikulis DJ. Functional MRI of pain-and attention-related activations in the human cingulate cortex. J Neurophysiol 77: 3370 -3380, 1997. Derbyshire SW, Vogt BA, and Jones AK. Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex. Exp Brain Res 118: 52-60, 1998. Devinsky O, Morrell MJ, and Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain 118: 279 -306, 1995. Dostrovsky JO and Guilbaud G. Nociceptive responses in medial thalamus of the normal and arthritic rat. Pain 40: 93-104, 1990. Freeman JA and Nicholson C. Experimental optimization of current sourcedensity technique for anuran cerebellum. J Neurophysiol 38: 369 -382, 1975. Gabbott PL, Warner TA, Jays PR, and Bacon SJ. Areal and synaptic interconnectivity of prelimbic (area 32), infralimbic (area 25) and insular cortices in the rat. Brain Res 993: 59 -71, 2003. Gabbott PL, Warner TA, Jays PR, Salway P, and Busby SJ. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers.
doi:10.1152/jn.00623.2006 pmid:16956990 fatcat:4s6olmdmlzfmximwzvybbmu7pi