Volitional Control of Individual Neurons in the Human Brain

Can the human brain, a complex interconnected structure of over 80 billion neurons learn to control itself at the most elemental scale – a single neuron. We directly linked the firing rate of a single (direct) neuron to the position of a box on a screen, which participants tried to control. Remarkably, all subjects upregulated the firing rate of the direct neuron in memory structures of their brain. Learning was accompanied by improved performance over trials, simultaneous decorrelation of the direct neuron to local neurons, and direct neuron to beta frequency oscillation phase-locking. Such previously unexplored neuroprosthetic skill learning within memory related brain structures, and associated beta frequency phase-locking implicates the ventral striatum. Our demonstration that humans can volitionally control neuronal activity in mnemonic structures, may provide new ways of probing the function and plasticity of human memory without exogenous stimulation.

[1]  E. Fetz.  Operant Conditioning of Cortical Unit Activity , 1969, Science.

[2]  T. Powell,et al.  The cortico-striate projection in the monkey. , 1970, Brain : a journal of neurology.

[3]  E. Fetz,et al.  Operantly conditioned patterns on precentral unit activity and correlated responses in adjacent cells and contralateral muscles. , 1973, Journal of neurophysiology.

[4]  J. Lubar,et al.  Behavioral management of epileptic seizures following EEG biofeedback training of the sensorimotor rhythm , 1976, Biofeedback and self-regulation.

[5]  Douglas L. Jones,et al.  From motivation to action: Functional interface between the limbic system and the motor system , 1980, Progress in Neurobiology.

[6]  J. Lubar,et al.  EEG operant conditioning in intractable epileptics. , 1981, Archives of neurology.

[7]  W. Nauta,et al.  The visual cortico-striato-nigral pathway in the rat , 1986, Neuroscience.

[8]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[9]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[10]  A. D. Smith,et al.  The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones , 1990, Trends in Neurosciences.

[11]  S. Haber,et al.  Organization of the output of the ventral striatopallidal system in the rat: Ventral pallidal efferents , 1993, Neuroscience.

[12]  S. Haber,et al.  Primate cingulostriatal projection: Limbic striatal versus sensorimotor striatal input , 1994, The Journal of comparative neurology.

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

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

[15]  A. Graybiel.  The basal ganglia and cognitive pattern generators. , 1997, Schizophrenia bulletin.

[16]  J. Glowinski,et al.  Hippocampo‐prefrontal cortex pathway: Anatomical and electrophysiological characteristics , 2000, Hippocampus.

[17]  A. Graybiel,et al.  Synchronous, Focally Modulated β-Band Oscillations Characterize Local Field Potential Activity in the Striatum of Awake Behaving Monkeys , 2003, The Journal of Neuroscience.

[18]  H. Groenewegen.  The Basal Ganglia and Motor Control , 2003, Neural plasticity.

[19]  H. Eichenbaum,et al.  Oscillatory Entrainment of Striatal Neurons in Freely Moving Rats , 2004, Neuron.

[20]  T. Robbins,et al.  Putting a spin on the dorsal–ventral divide of the striatum , 2004, Trends in Neurosciences.

[21]  P. Fries,et al.  Gamma-Band Synchronization in the Macaque Hippocampus and Memory Formation , 2009, The Journal of Neuroscience.

[22]  U. Rutishauser,et al.  Human memory strength is predicted by theta-frequency phase-locking of single neurons , 2010, Nature.

[23]  JONATHAN E. Walker,et al.  Using QEEG-Guided Neurofeedback for Epilepsy Versus Standardized Protocols: Enhanced Effectiveness? , 2010, Applied psychophysiology and biofeedback.

[24]  W. Schultz,et al.  Operant Conditioning of Primate Prefrontal Neurons , 2010, Journal of neurophysiology.

[25]  Christof Koch,et al.  On-line, voluntary control of human temporal lobe neurons , 2010, Nature.

[26]  E. Fetz,et al.  Volitional control of single cortical neurons in a brain–machine interface , 2011, Journal of neural engineering.

[27]  R. Desimone,et al.  Laminar differences in gamma and alpha coherence in the ventral stream , 2011, Proceedings of the National Academy of Sciences.

[28]  R. Quiroga.  Concept cells: the building blocks of declarative memory functions , 2012, Nature Reviews Neuroscience.

[29]  Daniel K. Leventhal,et al.  Basal Ganglia Beta Oscillations Accompany Cue Utilization , 2012, Neuron.

[30]  Aaron C. Koralek,et al.  Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills , 2012, Nature.

[31]  K. Müller,et al.  Psychological predictors of SMR-BCI performance , 2012, Biological Psychology.

[32]  Michael J. Jutras,et al.  Oscillatory activity in the monkey hippocampus during visual exploration and memory formation , 2013, Proceedings of the National Academy of Sciences.

[33]  H. Steinbusch,et al.  Deep brain stimulation of the forniceal area enhances memory functions in experimental dementia: The role of stimulation parameters , 2013, Brain Stimulation.

[34]  Ashesh D. Mehta,et al.  Dominant frequencies of resting human brain activity as measured by the electrocorticogram , 2013, NeuroImage.

[35]  Aaron C. Koralek,et al.  Temporally Precise Cell-Specific Coherence Develops in Corticostriatal Networks during Learning , 2013, Neuron.

[36]  K. Zilles,et al.  Deep brain stimulation of the nucleus basalis of Meynert in Alzheimer’s dementia , 2014, Molecular Psychiatry.

[37]  Y. Frégnac,et al.  Bidirectional control of a one-dimensional robotic actuator by operant conditioning of a single unit in rat motor cortex , 2014, Front. Neurosci..

[38]  Aaron C. Koralek,et al.  Volitional modulation of optically recorded calcium signals during neuroprosthetic learning , 2014, Nature Neuroscience.

[39]  T. Ros,et al.  Tuning pathological brain oscillations with neurofeedback: a systems neuroscience framework , 2014, Front. Hum. Neurosci..

[40]  R. Andersen,et al.  Decoding motor imagery from the posterior parietal cortex of a tetraplegic human , 2015, Science.

[41]  P. Fries.  Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

[42]  Dominique Hasboun,et al.  Voluntary control of intracortical oscillations for reconfiguration of network activity , 2016, Scientific Reports.

[43]  Jadin C. Jackson,et al.  Reward Expectancy Strengthens CA1 Theta and Beta Band Synchronization and Hippocampal-Ventral Striatal Coupling , 2016, The Journal of Neuroscience.

[44]  Jeannie-Marie S. Leoutsakos,et al.  A Phase II Study of Fornix Deep Brain Stimulation in Mild Alzheimer’s Disease , 2016, Journal of Alzheimer's disease : JAD.

[45]  S. Charpier,et al.  Self-induced intracerebral gamma oscillations in the human cortex. , 2016, Brain : a journal of neurology.

[46]  R. Dolan,et al.  Perimovement decrease of alpha/beta oscillations in the human nucleus accumbens , 2016, Journal of neurophysiology.

[47]  Timothy K. Leonard,et al.  Hippocampal gamma‐band Synchrony and pupillary responses index memory during visual search , 2017, Hippocampus.

[48]  Jarrod A. Lewis-Peacock,et al.  Closed-loop brain training: the science of neurofeedback , 2017, Nature Reviews Neuroscience.

[49]  Ryan W. Eaton,et al.  Operant conditioning of neural activity in freely behaving monkeys with intracranial reinforcement. , 2017, Journal of neurophysiology.

[50]  David Robbe,et al.  Integrative Systems Local or Not Local : Investigating the Nature of Striatal Theta Oscillations in Behaving Rats , 2018 .

[51]  Hugo Merchant,et al.  Primate beta oscillations and rhythmic behaviors , 2018, Journal of Neural Transmission.

[52]  Bradley C. Lega,et al.  Closed-loop stimulation of temporal cortex rescues functional networks and improves memory , 2018, Nature Communications.

[53]  D. Huber,et al.  Rapid Integration of Artificial Sensory Feedback during Operant Conditioning of Motor Cortex Neurons , 2017, Neuron.

[54]  David M. Groppe,et al.  Differential generation of saccade, fixation and image onset event-related potentials in the human mesial temporal lobe , 2018, bioRxiv.

[55]  Aaron C. Koralek,et al.  Volitional Modulation of Primary Visual Cortex Activity Requires the Basal Ganglia , 2018, Neuron.

[56]  Darrin J. Lee,et al.  Current Status of Deep Brain Stimulation for Alzheimer's Disease: From Chance Observation to Clinical Trials. , 2019, Cold Spring Harbor Symposia on Quantitative Biology.

[57]  Jose M Carmena,et al.  Neural reinforcement: re-entering and refining neural dynamics leading to desirable outcomes , 2019, Current Opinion in Neurobiology.