Implications of noise and neural heterogeneity for vestibulo-ocular reflex fidelity.
The vestibulo-ocular reflex (VOR) is characterized by a short-latency, high-fidelity eye movement response to head rotations at frequencies up to 20 Hz. Electrophysiological studies of medial vestibular nucleus (MVN) neurons, however, show that their response to sinusoidal currents above 10 to 12 Hz is highly nonlinear and distorted by aliasing for all but very small current amplitudes. How can this system function in vivo when single cell response cannot explain its operation? Here we show that the necessary wide VOR frequency response may be achieved not by firing rate encoding of head velocity in single neurons, but in the integrated population response of asynchronously firing, intrinsically active neurons. Diffusive synaptic noise and the pacemaker-driven, intrinsic firing of MVN cells synergistically maintain asynchronous, spontaneous spiking in a population of model MVN neurons over a wide range of input signal amplitudes and frequencies. Response fidelity is further improved by a reciprocal inhibitory link between two MVN populations, mimicking the vestibular commissural system in vivo, but only if asynchrony is maintained by noise and pacemaker inputs. These results provide a previously missing explanation for the full range of VOR function and a novel account of the role of the intrinsic pacemaker conductances in MVN cells. The values of diffusive noise and pacemaker currents that give optimal response fidelity yield firing statistics similar to those in vivo, suggesting that the in vivo network is tuned to optimal performance. While theoretical studies have argued that noise and population heterogeneity can improve coding, to our knowledge this is the first evidence indicating that these parameters are indeed tuned to optimize coding fidelity in a neural control system in vivo.
Institute for Adaptive and Neural Computation, School of Informatics, University of Edinburgh, Edinburgh EH1 2QL, U.K. t.hospedales@ed.ac.uk
Timothy M
TM
Hospedales
Mark C W
MC
van Rossum
Bruce P
BP
Graham
Mayank B
MB
Dutia
D000200:Action Potentials / Q000502:physiology; D000818:Animals; D016477:Artifacts; D001683:Biological Clocks / Q000502:physiology; D001921:Brain / Q000502:physiology*; D003198:Computer Simulation; D005133:Eye Movements / Q000502:physiology*; D019416:Head Movements / Q000502:physiology; D006801:Humans; D008959:Models, Neurological; D009415:Nerve Net / Q000502:physiology; D009433:Neural Inhibition / Q000502:physiology; D016571:Neural Networks, Computer; D009434:Neural Pathways / Q000502:physiology; D009474:Neurons / Q000502:physiology*; D009801:Oculomotor Muscles / Q000294:innervation / Q000502:physiology; D004856:Postural Balance / Q000502:physiology*; D012027:Reflex, Vestibulo-Ocular / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology; D014726:Vestibular Nuclei / Q000502:physiology; D014722:Vestibule, Labyrinth / Q000502:physiology*