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DynaPage - 2001 Nature Publishing Group...

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184 nature neuroscience volume 4 no 2 february 2001 articles Persistent neural activity refers to a sustained change of sodium action potential firing rate extending beyond a brief sensory stim- ulus or motor command. This activity has been observed in diverse brain areas 1–8 , suggesting that it is a general form of neural dynam- ics. Because persistent activity carries a ‘trace’ of a past event, it is thought to be closely related to short-term or ‘working’ memo- ry 1,3,9 . In this study, we obtained intracellular recordings in awake goldfish from neurons that show sustained firing during eye fixa- tion, providing information about intrinsic neuronal excitability and movement-associated membrane potential changes that con- strains proposed mechanisms of persistent neural activity. The neurons recorded are located in area I, a bilateral pre- motor hindbrain nucleus 7 . During sequential saccades and fix- ations composing the back and forth scanning pattern of goldfish spontaneous eye movements 10 , these neurons discharge as shown in Fig. 1a (refs. 7, 11). Transient increases in firing rate are observed during ipsilaterally directed (on) saccades, and tran- sient decreases occur during contralaterally directed (off) sac- cades. When eye position is above a threshold value, there is a sustained tonic firing rate that long outlasts the transient changes in rate observed during saccades ( Fig. 1b ). This persistent neur- al activity varies linearly with eye position, with different ‘posi- tion’ neurons showing different slopes and thresholds in the firing rate/eye position relationship 11 . This transformation of a pulse-like saccadic command into a step of sustained discharge can be described in terms of a veloc- ity-to-position neural integrator (VPNI), a concept originally introduced 12 to explain the time integration of head-velocity sig- nals into eye-position signals during the vestibulo-ocular reflex (VOR) 13 . Lidocaine inactivation of area I disrupts fixations and low-frequency VOR, demonstrating that this nucleus (connec- tivity, Fig. 1c ) is an essential component of the VPNI for hori- zontal eye movements 7,11 . Hypothetical mechanisms for the persistent activity of VPNI position neurons must account for several characteristics 14 . First, there is a continuum of stable firing rates 5,6,11 , which is more dif- ficult to explain than bistability. Second, persistent activity remains without either visual 11 or proprioceptive feedback 15 , demonstrating a central origin. Third, a different linear rela- tionship between firing rate and eye position for each neuron implies that for each eye position, a constrained pattern of sta- ble activity exists. At one extreme, persistent activity may be a purely single-cell phenomenon. For example, burst input could trigger plateau potentials 16,17 , with multiple dendritic generation sites produc- ing multiple firing levels 18 . Alternatively, saccadic command neu- rons could release neuromodulators that modify the frequency of intrinsic pacemaker currents 19 or alter sodium action poten-
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