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Working Memory, Spikes, and Neuromodulation

Principal investigator(s): Boris Gutkin, Mario Dipoppa (UCL)

Dopaminergic Modulation of Working Memory Circuit. Upper: General Model Network Diagram Lower: Transfer Function of the BG Units - DA induces bistability. Gruber et al 2006. We have studied the mechanisms of working memory formation. This is the kind of memory where information is held actively on-line for use in generating cognition-guided action and behavior. Neurons in several cortical areas, and particularly in the dorsolateral prefrontal cortex of primates show sustained activity that is a neural representation of the working memory trace. We are exploring the dynamical mechanisms underlying this activity, focusing on the structure of spiking in such circuits and the influence of neuromodulation.
The underlying theoretical models for this activity are the so-called 'bump' attractors or sustained foci of activity that are spatially and temporally stable. We have considered the relationship between the structure of spike-timing within a bump attractor and its stability. We have shown an "inhibitory" effect of synchronizing excitation, that is sustained activity stops when the active neurons are synchronized. This is independent of the neuronal model used and also independent of recurrent inhibition. We have suggested that this could be an efficient way to update the representations in working memory.
We are studying the influence of noise on the stability and the onset of sustained activity in spiking neural circuits. We have shown that random excitatory synaptic inputs can disrupt sustained activity in a simple, purely excitatory circuit. We are presently analyzing the mechanism for this and studying the consequences for neural phenomena as up-down states.
We have studied bump formation and stability in networks with patchy long-range lateral connections: excitatory "lattices". We have also found that patchy connections can play a role in sustaining multiple bumps by proving that these stabilize the coexistence of multiple bumps, hence traces of multiple memories.
We have studied the influence of basal ganglia on the stability of bump attractors. We have specifically examined the role of dopamine in modulating the relative interactions between the prefrontal cortex and the basal ganglia, suggesting that dopaminergic modulation enables contextual control of memory store access.
We have recently studied the influence of coherent oscillations and background noise correlations on the stbility of persistent activity. Our models show that both change the memory state from an attractor to a slow transient, with the characteristic life times dependent on the statistics of the background activity and the parameters of the oscillations. We showed that different oscillatiory frequency bands, at equal coherence, have a differential effect on the ability of transient stimuli to activate the memory state and an apriori memory state to be deactivated. Using this fact we show how flexible shifts in oscillatory frequency content can ensure the various dynamical and gating regimes to implement whole delay response tasks. Surprisingly we found that theta-band oscillations ensure robust memory maintenance in the face of irrelevant distractors and alpha-band clears the memory and ensures only transient responses to transient stimuli.

Publications

Dipoppa, M. and Gutkin, B.S., Flexible frequency control of cortical oscillations enables computations required for working memory, PNAS, in press, (2013).

Dipoppa, M. and Gutkin, B.S., Correlations in background activity control persistent state stability and allow execution of working memory tasks., Frontiers in Computational Neuroscience, 7:00139, (2013).

DiPoppa, M., Krupa, M., Torcini, A., and Gutkin, B., Splay States in Finite Pulse-Coupled Networks of Excitable Neurons, SIAM Journal of Applied Dynamical Systems, 11, 864894 (2012).

Gutkin, B.S., Tuckwell, H., and Jost, J., The Phenomenon of Inverse Stochastic Resonance, Naturwissenschaft, DOI 10.1007/s00114-009-0570-5, (2009).

Gutkin, B.S., Tuckwell, H., and Jost, J., Transient termination of synaptically sustained firing by noise, Euro Physics Letters, 81, 20005 (2008).

Mongillo, G., Barak, O., and Tsodyks, M., Synaptic theory of working memory, Science, 319, 1543-1546 (2008).

Gruber, A.J., Dayan, P., Gutkin, B.S., and Solla, S.A., Dopamine modulation in the basal ganglia locks the gate to working memory, Journal of Computational Neuroscience, 20 (2), 153-166 (2006).

Gutkin, B.S., Jost, J., and Hely, T., Noise Delays Onset of Sustained Firing in a Positively Coupled Neural Circuit, Neurocomputing, 58-60, 753-760 (2004).

Laing, C.R., Troy, W.C., Gutkin, B.S., and Ermentrout, G.B., Multiple Bumps in a Neuronal Model of Working Memory, SIAM Journal of Applied Mathematics, 63 (1), 62-97 (2002).

Gutkin, B.S., Laing, C.R., Colby, C., Chow, C.C., and Ermentrout, G.B., Turning On and Off with Excitation, J. Computational Neuroscience, 11:2, 121-134 (2001).

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