Electrical high frequency stimulation in the dorsal striatum: Effects on response learning and on GABA levels in rats

Electrical high frequency stimulation (HFS) has been used to treat various neurological and psychiatric diseases. The striatal area contributes to response learning and procedural memory. Therefore, we investigated the effect of striatal HFS application on procedural/declarative-like memory in rats. All rats were trained in a flooded Double-H maze for three days (4 trials/day) to swim to an escape platform hidden at a constant location. The starting place was the same for all trials. After each training session, HFS of the left dorsal striatum was performed over 4h in alternating 20 min periods (during rest time, 10a.m. to 3p.m.). Nineteen hours after the last HFS and right after a probe trial assessing the rats' strategy (procedural vs. declarative-like memory-based choice), animals were sacrificed and the dorsal striatum was quickly removed. Neurotransmitter levels were measured by HPLC. Stimulated rats did not differ from sham-operated and control rats in acquisition performance, but exhibited altered behavior during the probe trial (procedural memory responses being less frequent than in controls). In stimulated rats, GABA levels were significantly increased in the dorsal striatum on both sides. We suggest that HFS of the dorsal striatum does not alter learning behavior in rats but influences the strategy by which the rats solve the task. Given that the HFS-induced increase of GABA levels was found 19 h after stimulation, it can be assumed that HFS has consequences lasting for several hours and which are functionally significant at a behavioral level, at least under our stimulation (frequency, timing, location, side and strength of stimulation) and testing conditions.

[1]  A. Lozano,et al.  Advances in neurostimulation for movement disorders , 2000, Neurological research.

[2]  Jean-Christophe Cassel,et al.  The double-H maze test, a novel, simple, water-escape memory task: Acquisition, recall of recent and remote memory, and effects of systemic muscarinic or NMDA receptor blockade during training , 2011, Behavioural Brain Research.

[3]  J. D. McGaugh,et al.  Inactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning , 1996, Neurobiology of Learning and Memory.

[4]  J. Glowinski,et al.  Release of dopamine in both caudate nuclei and both substantia nigrae in response to unilateral stimulation of cerebellar nuclei in the cat , 1978, Brain Research.

[5]  J. D. McGaugh,et al.  Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. , 1992, Behavioral neuroscience.

[6]  R. Prado-Alcalá,et al.  Effects of Regional GABAergic Blockade of the Striatum on Memory Consolidation , 1996, Neurobiology of Learning and Memory.

[7]  G. Krauss,et al.  Visual function loss from vigabatrin , 2000, Neurology.

[8]  M. Packard,et al.  Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  Jeffrey M Albert,et al.  Prospective randomized double-blind trial of bilateral thalamic deep brain stimulation in adults with Tourette syndrome. , 2007, Journal of neurosurgery.

[10]  A L Benabid,et al.  Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. , 2000, Neurology.

[11]  J. Zentner,et al.  GABAA autoreceptors enhance GABA release from human neocortex: towards a mechanism for high-frequency stimulation (HFS) in brain? , 2009, Naunyn-Schmiedeberg's Archives of Pharmacology.

[12]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[13]  O. Hikosaka,et al.  Differential roles of monkey striatum in learning of sequential hand movement , 1997, Experimental Brain Research.

[14]  M. Chesselet,et al.  Local and distal effects induced by unilateral striatal application of opiates in the absence or in the presence of naloxone on the release of dopamine in both caudate nuclei and substantiae nigrae of the cat , 1983, Brain Research.

[15]  R. Romo,et al.  Distinct commissural pathways are involved in the enhanced release of dopamine induced in the contralateral caudate nucleus and substantia nigra by unilateral application of GABA in the cat thalamic motor nuclei , 1984, Brain Research.

[16]  David W. Roberts,et al.  High-frequency stimulation of the subthalamic nucleus increases glutamate in the subthalamic nucleus of rats as demonstrated by in vivo enzyme-linked glutamate sensor , 2007, Brain Research.

[17]  M. Delong,et al.  Deep Brain Stimulation for Neurologic and Neuropsychiatric Disorders , 2006, Neuron.

[18]  R. Snider,et al.  Cerebellar pathways to ventral midbrain and nigra , 1976, Experimental Neurology.

[19]  Andreas Moser,et al.  Neuronal electrical high frequency stimulation modulates presynaptic GABAergic physiology , 2004, Neuroscience Letters.

[20]  Anatol C. Kreitzer,et al.  Striatal Plasticity and Basal Ganglia Circuit Function , 2008, Neuron.

[21]  H. Künzle Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study inMacaca fascicularis , 1975, Brain Research.

[22]  C. Lücking,et al.  Selective GABA release as a mechanistic basis of high-frequency stimulation used for the treatment of neuropsychiatric diseases , 2011, Naunyn-Schmiedeberg's Archives of Pharmacology.

[23]  C. McIntyre,et al.  Sources and effects of electrode impedance during deep brain stimulation , 2006, Clinical Neurophysiology.

[24]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[25]  A. Moser,et al.  Electrical high frequency stimulation of the caudate nucleus induces local GABA outflow in freely moving rats , 2007, Journal of Neuroscience Methods.

[26]  E. Tolman,et al.  Studies in spatial learning; response learning vs. place learning by the non-correction method. , 1947, Journal of experimental psychology.

[27]  H. Steinbusch,et al.  Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus , 2007, Proceedings of the National Academy of Sciences.

[28]  R. Wennberg,et al.  Cortical activation with deep brain stimulation of the anterior thalamus for epilepsy , 2006, Clinical Neurophysiology.

[29]  Lorys Castelli,et al.  Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: comparison of pre- and postoperative neuropsychological evaluation , 2001, Journal of the Neurological Sciences.

[30]  W M COWAN,et al.  A bilateral cortico-striate projection , 1965, Journal of neurology, neurosurgery, and psychiatry.

[31]  H. Blodgett,et al.  Place versus response learning in the simple T-maze. , 1947, Journal of experimental psychology.

[32]  M. Packard Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[33]  A. Moser,et al.  Modulation of a neuronal network by electrical high frequency stimulation in striatal slices of the rat in vitro , 2006, Neurochemistry International.