Engagement of Rat Striatal Neurons by Cortical Epileptiform Activity Investigated With Paired Recordings

Enrico Bracci, Diego Centonze, Giorgio Bernardi, Paolo Calabresi
2004 Journal of Neurophysiology  
Calabresi. Engagement of rat striatal neurons by cortical epileptiform activity investigated with paired recordings. . The striatum is thought to play an important role in the spreading of epilepsy from cortical areas to deeper brain structures, but this issue has not been addressed with intracellular techniques. Paired recordings were used to assess the impact of cortical epileptiform activity on striatal neurons in brain slices. Bath-application of 4-amynopyridine (100 M) and bicuculline (20
more » ... ) induced synchronized bursts in all pairs of cortical neurons (Յ5 mm apart) in coronal, sagittal, and oblique slices (which preserve connections from the medial agranular cortex to the striatum). Under these conditions, striatal medium spiny neurons (MSs) displayed a strong increased spontaneous glutamatergic activity. This activity was not correlated to the cortical bursts and was asynchronous in pairs of MSs. Sporadic, large-amplitude synchronous depolarizations also occurred in MSs. These events were simultaneously detected in glial cells, suggesting that they were accompanied by considerable increases in extracellular potassium. In oblique slices, cortically driven bursts were also observed in MSs. These events were synchronized to cortical epileptiform bursts, depended on non-N-methyl-D-aspartate (NMDA) glutamate receptors, and persisted in the cortex, but not in the striatum, after disconnection of the two structures. During these bursts, MS membrane potential shifted to a depolarized value (59 Ϯ 4 mV) on which an irregular waveform, occasionally eliciting spikes, was superimposed. Thus synchronous activation of a limited set of corticostriatal afferents can powerfully control MSs. Cholinergic interneurons located Ͻ120 m from simultaneously recorded MSs, did not display cortically driven bursts, suggesting that these cells are much less easily engaged by cortical epileptiform activity. Amzica F and Steriade M. Spontaneous and artificial activation of neocortical seizures. J Neurophysiol 82: 3123-3138, 1999. Amzica F and Steriade M. Neuronal and glial membrane potentials during sleep and paroxysmal oscillations in the neocortex. J Neurosci 20: 6648 -6665, 2000. Anderson TR and Andrew RD. Spreading depression, imaging and blockade in the rat neocortical brain slice. J Neurophysiol 88: 2713-2725, 2002. Apicella P. Tonically active neurons in the primate striatum and their role in the processing of information about motivationally relevant events. Eur J Neurosci 16: 2017-2026, 2002. Avoli M, D'Antuono M, Louvel J, Kohling R, Biagini G, Pumain R, D'Arcangelo G, and Tancredi V. Network and pharmacological mechanisms leading to epileptiform synchronization the limbic system in vitro. Prog Neurobiol 68: 167-207, 2002. Beierlein M, Gibson JR, and Connors BW. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000, 2003. Bennett BD and Bolam JP. Synaptic input and output of parvalbuminimmunoreactive neurons in the neostriatum of the rat. Neuroscience 62: 707-719, 1994. Bennett BD, Callaway JC, and Wilson CJ. Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20: 8493-8503, 2000. Bennett BD and Wilson CJ. Synaptology and physiology of striatal neurons. In: Brain Dynamics and the Striatal Complex, edited by Miller R and Wickens JR. Harwood Academic, 2000. Bevan MD, Magill PJ, Terman D, Bolam JP, and Wilson CJ. Move to the rhythm, oscillations in the subthalamic nucleus-external globus pallidus network. Trends Neurosci 25: 525-531, 2002. Boda B and Szente MB. Stimulation of the substantia nigra pars reticulata suppresses neocortical seizures. Brain Res 574: 237-243, 1992. Bolam JP, Hanley JJ, Booth PA, and Bevan MD. Synaptic organisation of the basal ganglia. J Anat 196: 527-542, 2000. Bonhaus DW, Walters JR, and McNamara JO. Activation of substantia nigra neurons, role in the propagation of seizures in kindled rats. J Neurosci 6: 3024 -3030, 1986. Bracci E, Centonze D, Bernardi G, and Calabresi P. Dopamine excites fast-spiking interneurons in the striatum. Bracci E, Centonze D, Bernardi G, and Calabresi P. Voltage-dependent membrane potential oscillations of rat striatal fast-spiking interneurons. J Physiol 549: 121-130, 2003. Bracci E, Vreugdenhil M, Hack SP, and Jefferys JG. On the synchronizing mechanisms of tetanically induced hippocampal oscillations. J Neurosci 19: 8104 -8113, 1999. Bragin A, Engel J Jr, Wilson CL, Fried I, and Buzsaki G. High-frequency oscillations in human brain. Hippocampus 9: 137-142, 1999. Bruckner C, Stenkamp K, Meierkord H, and Heinemann U. Epileptiform discharges induced by combined application of bicuculline and 4-aminopyridine are resistant to standard anticonvulsants in slices of rats. Neurosci Lett 268: 163-165, 1999. Calabresi P, Centonze D, and Bernardi G. Electrophysiology of dopamine in normal and denervated striatal neurons. Trends Neurosci 23: S57-S63, 2000a. Calabresi P, Centonze D, Gubellini P, Pisani A, and Bernardi G. Acetylcholine-mediated modulation of striatal function. Trends Neurosci 23: 120 -126, 2000b. Calabresi P, Gubellini P, Centonze D, Picconi B, Bernardi G, Chergui K, Svenningsson P, Fienberg AA, and Greengard P. Dopamine and cAMPregulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci 20: 8443-8451, 2000c. Calabresi P, Pisani A, Mercuri NB, and Bernardi G. The corticostriatal projection, from synaptic plasticity to dysfunctions of the basal ganglia. Facilitated glutamatergic transmission in the striatum of D2 dopamine receptor-deficient mice. J Neurophysiol 85: 659 -670, 2001. Cepeda C, Hurst RS, Calvert CR, Hernandez-Echeagaray E, Nguyen OK, Jocoy E, Christian LJ, Ariano MA, and Levine MS. Transient and progressive electrophysiological alterations in the corticostriatal pathway in a mouse model of Huntington's disease. J Neurosci 23: 961-969, 2003. Connors BW and Gutnick MJ. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13: 99 -104, 1990. Croning MD, Zetterstrom TS, Grahame-Smith DG, and Newberry NR. Action of adenosine receptor antagonists on hypoxia-induced effects in the rat hippocampus in vitro. Br J Pharmacol 116: 2113-2119, 1995. Crossman AR. Functional anatomy of movement disorders. J Anat 196: 519 -525, 2000. Depaulis A, Vergnes M, and Marescaux C. Endogenous control of epilepsy, the nigral inhibitory system. Prog Neurobiol 42: 33-52, 1994. Flores-Hernandez J, Galarraga E, Pineda JC, and Bargas J. Patterns of excitatory and inhibitory synaptic transmission in the rat neostriatum as revealed by 4-AP. J Neurophysiol 72: 2246 -2256, 1994. Gale K. Subcortical structures and pathways involved in convulsive seizure generation. J Clin Neurophysiol 9: 264 -277, 1992. Gerfen CR. The neostriatal mosaic, multiple levels of compartmental organization. Trends Neurosci 15: 133-139, 1992. Goldman-Rakic PS. The corticostriatal fiber system in the rhesus monkey, organization and development. Prog Brain Res 58: 405-418, 1983. Gray CM, Konig P, Engel AK, and Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334 -337, 1989. Graybiel AM. Building action repertoires, memory and learning functions of the basal ganglia. Curr Opin Neurobiol 5: 733-741, 1995.
doi:10.1152/jn.00585.2004 pmid:15240765 fatcat:ewwrbwhumrcolbcmq62zgctdj4