High frequency stimulation of the ventrolateral and mediodorsal thalamic nuclei: differential effects on impulsive action

Year 2009, Volume: 26 Issue: 1, 27 - 34, 06.12.2010

Thibaut Sesia Koray Basar Rinske Vlamings Lee Wei Lim Yasin Temel

Abstract

Ventrolateral thalamic nucleus stimulation is a frequently applied clinical procedure to control disabling tremor. Its motor effects are largely established now, but the cognitive effects are largely unknown and are currently under investigation. Here, we performed a detailed investigation of the effects of electrical stimulation at high frequency (130 Hz) and various amplitude (0, 1, 3, 30, 150) of the VL thalamic nucleus in a rat model on specific cognitive functions, using a reaction time task, and compared to DBS of the mediodorsal thalamic nucleus (MD) to evaluate the specificity of the site of stimulation. The involvement of the MD thalamic nucleus in cognitive functions has already been established. In addition, we mapped the effect of VL and MD thalamic nuclei DBS on the neuronal activity of the mPFC using c-Fos immunohistochemistry to investigate the neural pathways underlying the behavioural effects. Results show that DBS of the VL and MD thalamic nuclei had no significant effects on reaction time and motor time. DBS of the VL thalamic nucleus induced no significant effect on premature responding, whereas DBS of the MD thalamic nucleus increased this. In addition, MD and VL thalamic nuclei DBS significantly increased the number of c-Fos-immunoreactive cells in the prelimbic cortex as compared to control animals. In the infralimbic cortex, the number of c-Fos-immunoreactive cells was significantly higher following MD thalamic nucleus DBS as compared to the other groups. These findings support that the VL thalamic nuclei is not involved in impulsive action. However, DBS of the MD thalamic nucleus induced specific changes in cognitive parameters, which further establishes its involvement in behavioral functions.. This behavioral effect is mediated by a circuit involving specific prefrontal cortical areas.

Keywords

Deep brain stimulation c-Fos, Mediodorsal thalamic nucleus, Premature responding, Reaction time task, Ventrolateral thalamic nucleusRat

References

• Alexander, G.E., Crutcher, M.D., 1990. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13, 266-71.
• Alexander, G.E., Crutcher, M.D., DeLong, M.R., 1990. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculo- motor, “prefrontal” and “limbic” functions. Prog Brain Res. 85, 119-46.
• Anderson, T.R., Hu, B., Iremonger, K., Kiss, Z.H., 2006. Selective attenuation of afferent synaptic transmission as a mechanism of thalamic deep brain stimulation-induced tremor arrest. J Neurosci. 26, 841-50.
• Babel, T.B., Warnke, P.C., Ostertag, C.B., 2001. Immediate and long term outcome after infrathalamic and thalamic lesioning for intractable Tourette’s syndrome. J Neurol Neurosurg Psychiatry. 70, 666-71.
• Baunez, C., Robbins, T., 1997. Bilateral lesions of the subthalamic nucleus induce multiple deficits in an attentional task in rats. The European journal of neuroscience. 9, 2086-2099.
• Benabid, A., Pollak, P., Louveau, A., Henry, S., de Rougemont, J., 1987. Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson disease. Appl Neurophysiol. 50, 344-346.
• Benazzouz, A., Gao, D.M., Ni, Z.G., Piallat, B., Bouali-Benazzouz, R., Benabid, A.L., 2000. Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat. Neuroscience. 99, 289-95.
• Benazzouz, A., Tai, C.H., Meissner, W., Bioulac, B., Bezard, E., Gross, C., 2004. High-frequency stimulation of both zona incerta and subthalamic nucleus induces a similar normalization of basal ganglia metabolic activity in experimental parkinsonism. Faseb J. 18, 528-30.
• Blokland, A., 1998. Reaction Time Responding in Rats. Neuroscience & Biobehavioral Reviews. 22, 847-864.
• Chudasama, Y., Muir, J.L., 2001. Visual attention in the rat: a role for the prelimbic cortex and thalamic nuclei? Behav Neurosci. 115, 417-28.
• Chudasama, Y., Passetti, F., Rhodes, S.E., Lopian, D., Desai, A., Robbins, T.W., 2003. Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity. Behav Brain Res. 146, 105-19.
• Dalley, J.W., Fryer, T.D., Brichard, L., Robinson, E.S., Theobald, D.E., Laane, K., Pena, Y., Murphy, E.R., Shah, Y., Probst, K., Abakumova, I., Aigbirhio, F.I., Richards, H.K., Hong, Y., Baron, J.C., Everitt, B.J., Robbins, T.W., 2007. Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science. 315, 1267-70.
• DeLong, M.R., 1990. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13, 281-5.
• Desbonnet, L., Temel, Y., Visser-Vandewalle, V., Blokland, A., Hornikx, V., Steinbusch, H.W., 2004. Premature responding following bilateral stimulation of the rat subthalamic nucleus is amplitude and frequency dependent. Brain Res. 1008, 198-204.
• Evenden, J., 1999a. Impulsivity: a discussion of clinical and experimental findings. J Psychopharmacol. 13, 180 - 192.
• Evenden, J.L., 1999b. Varieties of impulsivity. Psychopharmacology (Berl). 146, 348 - 361.
• Filali, M., Hutchison, W.D., Palter, V.N., Lozano, A.M., Dostrovsky, J.O., 2004. Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus. Exp Brain Res. 156, 274-81.
• Gabbott, P.L., Warner, T.A., Jays, P.R., Salway, P., Busby, S.J., 2005. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol. 492, 145-77.
• Groenewegen, H.J., 1988. Organization of the afferent connections of the mediodorsal thalamic nucleus in the rat, related to the mediodorsal-prefrontal topography. Neuroscience. 24, 379-431.
• Groenewegen, H.J., Berendse, H.W., 1990. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol. 294, 607-22.
• Groenewegen, H.J., Galis-de Graaf, Y., Smeets, W.J., 1999. Integration and segregation of limbic cortico-striatal loops at the thal- amic level: an experimental tracing study in rats. J Chem Neuroanat. 16, 167-85.
• Groenewegen, H.J., Witter, M.P., 2004. Thalamus. The Rat Nevous System, Third Edition. New York, Elsevier. Chapter 17, 407-453.
• Heidbreder, C.A., Groenewegen, H.J., 2003. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neuroscience & Biobehavioral Reviews. 27, 555-579.
• Hubble, J.P., Busenbark, K.L., Wilkinson, S., Penn, R.D., Lyons, K., Koller, W.C., 1996. Deep brain stimulation for essential tremor. Neurology. 46, 1150-3.
• Kobayashi, K., Katayama, Y., Kasai, M., Oshima, H., Fukaya, C., Yamamoto, T., 2003. Localization of thalamic cells with tremor- frequency activity in Parkinson’s disease and essential tremor. Acta Neurochir Suppl. 87, 137-9.
• Kuroda, M., Yokofujita, J., Murakami, K., 1998. An ultrastructural study of the neural circuit between the prefrontal cortex and the mediodorsal nucleus of the thalamus. Prog Neurobiol. 54, 417-58.
• Lamprea, M.R., Cardenas, F.P., Vianna, D.M., Castilho, V.M., Cruz-Morales, S.E., Brandao, M.L., 2002. The distribution of fos immuno- reactivity in rat brain following freezing and escape responses elicited by electrical stimulation of the inferior colliculus. Brain Res. 950, 186-94.
• Loher, T.J., Gutbrod, K., Fravi, N.L., Pohle, T., Burgunder, J.M., Krauss, J.K., 2003. Thalamic stimulation for tremor. Subtle changes in episodic memory are related to stimulation per se and not to a microthalamotomy effect. J Neurol. 250, 707-13.
• Lozano, A.M., 2000. Vim thalamic stimulation for tremor. Arch Med Res. 31, 266-9.
• Lyons, K.E., Pahwa, R., 2004. Deep brain stimulation and essential tremor. J Clin Neurophysiol. 21, 2-5.
• McCracken, C.B., Grace, A.A., 2007. High-Frequency Deep Brain Stimulation of the Nucleus Accumbens Region Suppresses Neuronal Activity and Selectively Modulates Afferent Drive in Rat Orbitofrontal Cortex In Vivo. J. Neurosci. 27, 12601- 12610.
• McIntyre, C.C., Grill, W.M., Sherman, D.L., Thakor, N.V., 2004a. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol. 91, 1457-69.
• McIntyre, C.C., Savasta, M., Kerkerian-Le Goff, L., Vitek, J.L., 2004b. Uncovering the mechanism(s) of action of deep brain stimula- tion: activation, inhibition, or both. Clin Neurophysiol. 115, 1239-48.
• McIntyre, C.C., Butson, C.R., Maks, C.B., Noecker, A.M., 2006. Optimizing deep brain stimulation parameter selection with detailed models of the electrode-tissue interface. Conf Proc IEEE Eng Med Biol Soc. 1, 893-5.
• Meissner, W., Leblois, A., Hansel, D., Bioulac, B., Gross, C.E., Benazzouz, A., Boraud, T., 2005. Subthalamic high frequency stimula- tion resets subthalamic firing and reduces abnormal oscillations. Brain. 128, 2372-82.
• Pahwa, R., Lyons, K.E., Wilkinson, S.B., Simpson, R.K., Jr., Ondo, W.G., Tarsy, D., Norregaard, T., Hubble, J.P., Smith, D.A., Hauser, R.A., Jankovic, J., 2006. Long-term evaluation of deep brain stimulation of the thalamus. J Neurosurg. 104, 506-12.
• Ray, J.P., Price, J.L., 1992. The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography. J Comp Neurol. 323, 167-97.
• Rubia, K., Smith, A.B., Brammer, M.J., Toone, B., Taylor, E., 2005. Abnormal brain activation during inhibition and error detection in medication-naive adolescents with ADHD. Am J Psychiatry. 162, 1067-75.
• Schuurman, P.R., Bosch, D.A., Bossuyt, P.M., Bonsel, G.J., van Someren, E.J., de Bie, R.M., Merkus, M.P., Speelman, J.D., 2000. A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. N Engl J Med. 342, 461-8.
• Smith, A.B., Taylor, E., Brammer, M., Toone, B., Rubia, K., 2006. Task-specific hypoactivation in prefrontal and temporoparietal brain regions during motor inhibition and task switching in medication-naive children and adolescents with attention deficit hyperactivity disorder. Am J Psychiatry. 163, 1044-51.
• Tai, C.H., Boraud, T., Bezard, E., Bioulac, B., Gross, C., Benazzouz, A., 2003. Electrophysiological and metabolic evidence that high- frequency stimulation of the subthalamic nucleus bridles neuronal activity in the subthalamic nucleus and the sub- stantia nigra reticulata. Faseb J. 17, 1820-30.
• Temel, Y., Blokland, A., Steinbusch, H.W., Visser-Vandewalle, V., 2005a. The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog Neurobiol. 76, 393-413.
• Temel, Y., Visser-Vandewalle, V., Aendekerk, B., Rutten, B., Tan, S., Scholtissen, B., Schmitz, C., Blokland, A., Steinbusch, H.W., 2005b. Acute and separate modulation of motor and cognitive performance in parkinsonian rats by bilateral stimulation of the subthalamic nucleus. Exp Neurol. 193, 43-52.
• Temel, Y., Boothman, L.J., Blokland, A., Magill, P.J., Steinbusch, H.W., Visser-Vandewalle, V., Sharp, T., 2007. Inhibition of 5-HT neu- ron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc Natl Acad Sci U S A. 104, 17087-92.
• Troster, A.I., Wilkinson, S.B., Fields, J.A., Miyawaki, K., Koller, W.C., 1998. Chronic electrical stimulation of the left ventrointermedi- ate (Vim) thalamic nucleus for the treatment of pharmacotherapy-resistant Parkinson’s disease: a differential impact on access to semantic and episodic memory? Brain Cogn. 38, 125-49.
• Uylings, H.B., van Eden, C.G., 1990. Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, in- cluding humans. Prog Brain Res. 85, 31-62.
• Vertes, R.P., 2004. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse. 51, 32-58.
• Vertes, R.P., 2006. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cogni- tive processing in the rat. Neuroscience. 142, 1-20.
• Wichmann, T., Delong, M.R., 2006. Deep brain stimulation for neurologic and neuropsychiatric disorders. Neuron. 52, 197-204.
• Winstanley, C.A., Eagle, D.M., Robbins, T.W., 2006. Behavioral models of impulsivity in relation to ADHD: Translation between clinical and preclinical studies. Clinical Psychology Review. 26, 379-395.