Central Thalamic Deep-Brain Stimulation Alters Striatal-Thalamic Connectivity in Cognitive Neural Behavior

Central thalamic deep brain stimulation (CT-DBS) has been proposed as an experimental therapeutic approach to produce consistent sustained regulation of forebrain arousal for several neurological diseases. We investigated local field potentials (LFPs) induced by CT-DBS from the thalamic central lateral nuclei (CL) and the striatum as potential biomarkers for the enhancement of lever-pressing skill learning. LFPs were simultaneously recorded from multiple sites in the CL, ventral striatum (Vstr), and dorsal striatum (Dstr). LFP oscillation power and functional connectivity were assessed and compared between the CT-DBS and sham control groups. The theta and alpha LFP oscillations were significantly increased in the CL and striatum in the CT-DBS group. Furthermore, interhemispheric coherences between bilateral CL and striatum were increased in the theta band. Additionally, enhancement of c-Fos activity, dopamine D2 receptor (Drd2), and α4-nicotinic acetylcholine receptor (α4-nAChR) occurred after CT-DBS treatment in the striatum and hippocampus. CT-DBS strengthened thalamic-striatal functional connectivity, which demonstrates that the inter-regional connectivity enhancement might contribute to synaptic plasticity in the striatum. Altered dopaminergic and cholinergic receptors resulted in modulation of striatal synaptic plasticity's ability to regulate downstream signaling cascades for higher brain functions of lever-pressing skill learning.

[1]  A. Scholey,et al.  Functional Activation during the Rapid Visual Information Processing Task in a Middle Aged Cohort: An fMRI Study , 2015, PloS one.

[2]  S. Nagel,et al.  Preserving cortico-striatal function: deep brain stimulation in Huntington’s disease , 2015, Front. Syst. Neurosci..

[3]  K. Khodakhah,et al.  Short latency cerebellar modulation of the basal ganglia , 2014, Nature Neuroscience.

[4]  John T. Green,et al.  Voluntary exercise improves performance of a discrimination task through effects on the striatal dopamine system , 2014, Learning & memory.

[5]  Supratim Ray,et al.  Effect of amplitude correlations on coherence in the local field potential , 2014, Journal of neurophysiology.

[6]  A. Graybiel,et al.  Differential Entrainment and Learning-Related Dynamics of Spike and Local Field Potential Activity in the Sensorimotor and Associative Striatum , 2014, The Journal of Neuroscience.

[7]  Itzhak Fried,et al.  Deep brain stimulation for enhancement of learning and memory , 2014, NeuroImage.

[8]  N. Axmacher,et al.  Electrical engram: how deep brain stimulation affects memory , 2013, Trends in Cognitive Sciences.

[9]  Michael S Okun,et al.  Deep brain stimulation (DBS) at the interface of neurology and psychiatry. , 2013, The Journal of clinical investigation.

[10]  Bettina H. Bewernick,et al.  Neuromodulation for Treatment Resistant Depression: State of the Art and Recommendations for Clinical and Scientific Conduct , 2013, Brain Topography.

[11]  Raymond P. Kesner,et al.  A process analysis of the CA3 subregion of the hippocampus , 2013, Front. Cell. Neurosci..

[12]  B. Staresina,et al.  Memory Modulation by Weak Synchronous Deep Brain Stimulation: A Pilot Study , 2013, Brain Stimulation.

[13]  R. Cassel,et al.  Dorsolateral striatum and dorsal hippocampus: A serial contribution to acquisition of cue-reward associations in rats , 2013, Behavioural Brain Research.

[14]  D. Denys,et al.  [Deep brain stimulation for psychiatric disorders]. , 2013, Nederlands tijdschrift voor geneeskunde.

[15]  X.L. Chen,et al.  Deep Brain Stimulation , 2013, Interventional Neurology.

[16]  A. Gharabaghi,et al.  Increased coherence among striatal regions in the theta range during attentive wakefulness , 2012, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas.

[17]  I. Fried,et al.  Memory enhancement and deep-brain stimulation of the entorhinal area. , 2012, The New England journal of medicine.

[18]  P. Frankland,et al.  Stimulation of Entorhinal Cortex Promotes Adult Neurogenesis and Facilitates Spatial Memory , 2011, The Journal of Neuroscience.

[19]  J. Jankovic,et al.  Diagnosis and treatment of complications related to deep brain stimulation hardware , 2011, Movement disorders : official journal of the Movement Disorder Society.

[20]  B. Moghaddam,et al.  Reduced Neuronal Inhibition and Coordination of Adolescent Prefrontal Cortex during Motivated Behavior , 2011, The Journal of Neuroscience.

[21]  T. Womelsdorf,et al.  Human Neuroscience , 2022 .

[22]  G. Alarcón,et al.  Single pulse electrical stimulation of the hippocampus is sufficient to impair human episodic memory , 2010, Neuroscience.

[23]  Eliana Della Flora,et al.  Deep brain stimulation for essential tremor: A systematic review , 2010, Movement disorders : official journal of the Movement Disorder Society.

[24]  M. Wilson,et al.  Disruption of ripple‐associated hippocampal activity during rest impairs spatial learning in the rat , 2009, Hippocampus.

[25]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[26]  J. Born,et al.  Slow oscillation electrical brain stimulation during waking promotes EEG theta activity and memory encoding , 2009, Proceedings of the National Academy of Sciences.

[27]  T. Robbins,et al.  The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. , 2009, Annual review of neuroscience.

[28]  A. Grace,et al.  Nucleus Accumbens Deep Brain Stimulation Produces Region-Specific Alterations in Local Field Potential Oscillations and Evoked Responses In Vivo , 2009, The Journal of Neuroscience.

[29]  E. G. Jones,et al.  Synchrony in the Interconnected Circuitry of the Thalamus and Cerebral Cortex , 2009, Annals of the New York Academy of Sciences.

[30]  Adriano B. L. Tort,et al.  Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task , 2008, Proceedings of the National Academy of Sciences.

[31]  P. Calabresi,et al.  ACh/Dopamine Crosstalk in Motor Control and Reward: A Crucial Role for α6-Containing Nicotinic Receptors? , 2008, Neuron.

[32]  B. Balleine,et al.  Reward‐guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico‐basal ganglia networks , 2008, The European journal of neuroscience.

[33]  M. Sarter,et al.  Cholinergic Mediation of Attention , 2008, Annals of the New York Academy of Sciences.

[34]  F. Plum,et al.  Behavioural improvements with thalamic stimulation after severe traumatic brain injury , 2008, Nature.

[35]  D. Denys,et al.  [Deep brain stimulation for psychiatric disorders]. , 2018, Nederlands tijdschrift voor geneeskunde.

[36]  G. Knyazev.  Motivation, emotion, and their inhibitory control mirrored in brain oscillations , 2007, Neuroscience & Biobehavioral Reviews.

[37]  M. Ragozzino,et al.  The effect of rat anterior cingulate inactivation on cognitive flexibility. , 2007, Behavioral neuroscience.

[38]  R. O’Reilly,et al.  Separate neural substrates for skill learning and performance in the ventral and dorsal striatum , 2007, Nature Neuroscience.

[39]  N. Schiff,et al.  Cognitive enhancement with central thalamic electrical stimulation , 2006, Proceedings of the National Academy of Sciences.

[40]  P. Calabresi,et al.  A convergent model for cognitive dysfunctions in Parkinson's disease: the critical dopamine–acetylcholine synaptic balance , 2006, The Lancet Neurology.

[41]  H. Yin,et al.  The role of the basal ganglia in habit formation , 2006, Nature Reviews Neuroscience.

[42]  S. Cragg.  Meaningful silences: how dopamine listens to the ACh pause , 2006, Trends in Neurosciences.

[43]  Hippocampal CA1 kindling but not long-term potentiation disrupts spatial memory performance. , 2006, Learning & memory.

[44]  P. Fries.  A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[45]  R. Cardinal,et al.  Nucleus accumbens core lesions retard instrumental learning and performance with delayed reinforcement in the rat , 2005, BMC Neuroscience.

[46]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[47]  P. Goldman-Rakic,et al.  Selective D2 Receptor Actions on the Functional Circuitry of Working Memory , 2004, Science.

[48]  B. Balleine,et al.  The Effect of Lesions of the Basolateral Amygdala on Instrumental Conditioning , 2003, The Journal of Neuroscience.

[49]  Michael E. Hasselmo,et al.  Neuromodulation, theta rhythm and rat spatial navigation , 2002, Neural Networks.

[50]  G. Buzsáki.  Theta Oscillations in the Hippocampus , 2002, Neuron.

[51]  E. Maguire.  The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. , 2001, Scandinavian journal of psychology.

[52]  G. Deuschl,et al.  The pathophysiology of tremor , 2001, Muscle & nerve.

[53]  B. Khakh,et al.  Point mutant mice with hypersensitive α4 nicotinic receptors show dopaminergic deficits and increased anxiety , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[54]  E. Basar,et al.  Gamma, alpha, delta, and theta oscillations govern cognitive processes. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[55]  I. Scheffer,et al.  Phenotypic Characterization of an α4 Neuronal Nicotinic Acetylcholine Receptor Subunit Knock-Out Mouse , 2000, The Journal of Neuroscience.

[56]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[57]  J L Vitek,et al.  Physiology of hypokinetic and hyperkinetic movement disorders: model for dyskinesia. , 2000, Annals of neurology.

[58]  Elena Erro,et al.  Thalamic interaction between the input and the output systems of the basal ganglia , 1999, Journal of Chemical Neuroanatomy.

[59]  T. Inouye,et al.  Medial prefrontal cortex generates frontal midline theta rhythm. , 1999, Neuroreport.

[60]  E. Levin,et al.  Nicotinic acetylcholine involvement in cognitive function in animals , 1998, Psychopharmacology.

[61]  E. Vaadia,et al.  Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates , 1998, Trends in Neurosciences.

[62]  M Doppelmayr,et al.  Brain oscillations and human memory: EEG correlates in the upper alpha and theta band , 1997, Neuroscience Letters.

[63]  T. Foster,et al.  Insensitivity of the Hippocampus to Environmental Stimulation during Postnatal Development , 1997, The Journal of Neuroscience.

[64]  M. Deschenes,et al.  Striatal and cortical projections of single neurons from the central lateral thalamic nucleus in the rat , 1996, Neuroscience.

[65]  A. Saiardi,et al.  Parkinsonian-like locomotor impairment in mice lacking dopamine D2 receptors , 1995, Nature.

[66]  B. Skinner.  'Superstition' in the pigeon. 1948. , 1992, Journal of experimental psychology. General.

[67]  R. Depue,et al.  Facilitation of Working Memory in Humans by a D2 Dopamine Receptor Agonist , 1992, Journal of Cognitive Neuroscience.

[68]  E. Halgren,et al.  Human medial temporal-lobe stimulation disrupts both formation and retrieval of recent memories , 1985, Brain and Cognition.

[69]  R. Sutherland,et al.  A comparison of the contributions of the frontal and parietal association cortex to spatial localization in rats. , 1983, Behavioral neuroscience.

[70]  H. Johnson,et al.  A comparison of 'traditional' and multimedia information systems development practices , 2003, Inf. Softw. Technol..

[71]  B. Skinner.  Superstition in the pigeon. , 1948, Journal of experimental psychology.