Dopamine modulation in the basal ganglia locks the gate to working memory

The prefrontal cortex and basal ganglia are deeply implicated in working memory. Both structures are subject to dopaminergic neuromodulation in a way that exerts a critical influence on the proper operation of working memory. We present a novel network model to elucidate the role of phasic dopamine in the interaction of these two structures in initiating and maintaining mnemonic activity. We argue that neuromodulation plays a critical role in protecting memories against both internal and external sources of noise. Increases in cortical gain engendered by prefrontal dopamine release help make memories robust against external distraction, but do not offer protection against internal noise accompanying recurrent cortical activity. Rather, the output of the basal ganglia provides the gating function of stabilization against noise and distraction by enhancing select memories through targeted disinhibition of cortex. Dopamine in the basal ganglia effectively locks this gate by influencing the stability of up and down states in the striatum. Dopamine’s involvement in affective processing endows this gating with specificity to motivational salience. We model a spatial working memory task and show that these combined effects of dopamine lead to superior performance.

[1]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[2]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[3]  J D Cohen,et al.  A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. , 1990, Science.

[4]  A. Grace Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: A hypothesis for the etiology of schizophrenia , 1991, Neuroscience.

[5]  C. Marsden,et al.  Fronto-striatal cognitive deficits at different stages of Parkinson's disease. , 1992, Brain : a journal of neurology.

[6]  W. Schultz,et al.  Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  P. Goldman-Rakic,et al.  The role of D1-dopamine receptor in working memory: local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task. , 1994, Journal of neurophysiology.

[8]  J. Fuster Memory in the cerebral cortex , 1994 .

[9]  S. Haber,et al.  The organization of midbrain projections to the striatum in the primate: Sensorimotor-related striatum versus ventral striatum , 1994, Neuroscience.

[10]  J. Joseph,et al.  Activity in the caudate nucleus of monkey during spatial sequencing. , 1995, Journal of neurophysiology.

[11]  A. Graybiel Building action repertoires: memory and learning functions of the basal ganglia , 1995, Current Opinion in Neurobiology.

[12]  P. Goldman-Rakic,et al.  Modulation of memory fields by dopamine Dl receptors in prefrontal cortex , 1995, Nature.

[13]  O. Hikosaka,et al.  Eye movements in monkeys with local dopamine depletion in the caudate nucleus. II. Deficits in voluntary saccades , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  P. Goldman-Rakic Cellular basis of working memory , 1995, Neuron.

[15]  O. Hikosaka,et al.  Eye movements in monkeys with local dopamine depletion in the caudate nucleus. I. Deficits in spontaneous saccades , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  T. Sejnowski,et al.  Ionic mechanisms underlying synchronized oscillations and propagating waves in a model of ferret thalamic slices. , 1996, Journal of neurophysiology.

[17]  G. Rebec,et al.  Dopaminergic modulation of glutamate-induced excitations of neurons in the neostriatum and nucleus accumbens of awake, unrestrained rats. , 1996, Journal of neurophysiology.

[18]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[19]  Charles J. Wilson,et al.  The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[21]  K. Zhang,et al.  Representation of spatial orientation by the intrinsic dynamics of the head-direction cell ensemble: a theory , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  H S Seung,et al.  How the brain keeps the eyes still. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Bargas,et al.  D1 Receptor Activation Enhances Evoked Discharge in Neostriatal Medium Spiny Neurons by Modulating an L-Type Ca2+ Conductance , 1997, The Journal of Neuroscience.

[24]  H. Groenewegen,et al.  The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia , 1997, Journal of psychopharmacology.

[25]  JaneR . Taylor,et al.  Supranormal Stimulation of D1 Dopamine Receptors in the Rodent Prefrontal Cortex Impairs Spatial Working Memory Performance , 1997, The Journal of Neuroscience.

[26]  J. Houk,et al.  Network models of the basal ganglia , 1997, Current Opinion in Neurobiology.

[27]  F. Gonon Prolonged and Extrasynaptic Excitatory Action of Dopamine Mediated by D1 Receptors in the Rat Striatum In Vivo , 1997, The Journal of Neuroscience.

[28]  O. Hikosaka,et al.  Differential Roles of the Frontal Cortex, Basal Ganglia, and Cerebellum in Visuomotor Sequence Learning , 1998, Neurobiology of Learning and Memory.

[29]  P. Goldman-Rakic,et al.  Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. , 1998, Journal of neurophysiology.

[30]  S. Pollmann,et al.  D1- Versus D2-Receptor Modulation of Visuospatial Working Memory in Humans , 1998, The Journal of Neuroscience.

[31]  P. Goldman-Rakic,et al.  The cerebral cortex: a case for a common site of action of antipsychotics. , 1998, Trends in pharmacological sciences.

[32]  Jonathan D. Cohen,et al.  Dopamine and the mechanisms of cognition: Part II. D-amphetamine effects in human subjects performing a selective attention task , 1998, Biological Psychiatry.

[33]  J. Houk,et al.  Model of cortical-basal ganglionic processing: encoding the serial order of sensory events. , 1998, Journal of neurophysiology.

[34]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[35]  J. Cohen,et al.  Dopamine, cognitive control, and schizophrenia: the gating model. , 1999, Progress in brain research.

[36]  B. Postle,et al.  Dissociation of human caudate nucleus activity in spatial and nonspatial working memory: an event-related fMRI study. , 1999, Brain research. Cognitive brain research.

[37]  J. Tepper,et al.  Inhibitory control of neostriatal projection neurons by GABAergic interneurons , 1999, Nature Neuroscience.

[38]  A. Romanides,et al.  Glutamatergic and dopaminergic afferents to the prefrontal cortex regulate spatial working memory in rats , 1999, Neuroscience.

[39]  T. Sejnowski,et al.  Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. , 2000, Journal of neurophysiology.

[40]  M. Goldberg,et al.  Response of neurons in the lateral intraparietal area to a distractor flashed during the delay period of a memory-guided saccade. , 2000, Journal of neurophysiology.

[41]  P. Goldman-Rakic,et al.  Synaptic mechanisms and network dynamics underlying spatial working memory in a cortical network model. , 2000, Cerebral cortex.

[42]  R. Malenka,et al.  Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. , 2000, Annual review of neuroscience.

[43]  G. Glover,et al.  Basal ganglia involvement in memory‐guided movement sequencing , 2000, Neuroreport.

[44]  Örjan Ekeberg,et al.  Cortex-basal ganglia interaction and attractor states , 2001, Neurocomputing.

[45]  Michael J. Frank,et al.  Interactions between frontal cortex and basal ganglia in working memory: A computational model , 2001, Cognitive, affective & behavioral neuroscience.

[46]  Peter Redgrave,et al.  A computational model of action selection in the basal ganglia. I. A new functional anatomy , 2001, Biological Cybernetics.

[47]  Carson C. Chow,et al.  Stationary Bumps in Networks of Spiking Neurons , 2001, Neural Computation.

[48]  D. Hansel,et al.  Existence and stability of persistent states in large neuronal networks. , 2001, Physical review letters.

[49]  P. Duffy,et al.  Involvement of pallidothalamic circuitry in working memory , 2001, Neuroscience.

[50]  Y. Goto,et al.  Synchronous Activity in the Hippocampus and Nucleus Accumbens In Vivo , 2001, The Journal of Neuroscience.

[51]  Jonathan D. Cohen,et al.  Computational perspectives on dopamine function in prefrontal cortex , 2002, Current Opinion in Neurobiology.

[52]  P. Strick,et al.  Basal-ganglia 'projections' to the prefrontal cortex of the primate. , 2002, Cerebral cortex.

[53]  Y. Burnod,et al.  A Model of Prefrontal Cortex Dopaminergic Modulation during the Delayed Alternation Task , 2002, Journal of Cognitive Neuroscience.

[54]  E. Miyoshi,et al.  Impaired learning in a spatial working memory version and in a cued version of the water maze in rats with MPTP-induced mesencephalic dopaminergic lesions , 2002, Brain Research Bulletin.

[55]  K. Hikosaka,et al.  Coding and Monitoring of Motivational Context in the Primate Prefrontal Cortex , 2002, The Journal of Neuroscience.

[56]  Charles J. Wilson,et al.  Activity Patterns in a Model for the Subthalamopallidal Network of the Basal Ganglia , 2002, The Journal of Neuroscience.

[57]  D. Plenz When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function , 2003, Trends in Neurosciences.

[58]  C. Caltagirone,et al.  Dopaminergic Modulation of Visual-Spatial Working Memory in Parkinson’s Disease , 2003, Dementia and Geriatric Cognitive Disorders.

[59]  J. Houk,et al.  Modulation of striatal single units by expected reward: a spiny neuron model displaying dopamine-induced bistability. , 2003, Journal of neurophysiology.

[60]  J. Bargas,et al.  Spontaneous Voltage Oscillations in Striatal Projection Neurons in a Rat Corticostriatal Slice , 2003, The Journal of physiology.

[61]  S. Haber The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

[62]  Charles J. Wilson,et al.  GABAergic microcircuits in the neostriatum , 2004, Trends in Neurosciences.

[63]  R. Wightman,et al.  Dopamine Operates as a Subsecond Modulator of Food Seeking , 2004, The Journal of Neuroscience.

[64]  Xiao-Jing Wang,et al.  Effects of Neuromodulation in a Cortical Network Model of Object Working Memory Dominated by Recurrent Inhibition , 2004, Journal of Computational Neuroscience.

[65]  O. Hikosaka,et al.  Reward-predicting activity of dopamine and caudate neurons--a possible mechanism of motivational control of saccadic eye movement. , 2004, Journal of neurophysiology.

[66]  Boris S. Gutkin,et al.  Turning On and Off with Excitation: The Role of Spike-Timing Asynchrony and Synchrony in Sustained Neural Activity , 2001, Journal of Computational Neuroscience.

[67]  T. Robbins,et al.  Striatal contributions to working memory: a functional magnetic resonance imaging study in humans , 2004, The European journal of neuroscience.

[68]  Xiao-Jing Wang,et al.  A Model of Visuospatial Working Memory in Prefrontal Cortex: Recurrent Network and Cellular Bistability , 1998, Journal of Computational Neuroscience.

[69]  C. Marsden,et al.  l-Dopa withdrawal in Parkinson's disease selectively impairs cognitive performance in tests sensitive to frontal lobe dysfunction , 2005, Psychopharmacology.