Neural mechanism of oculomotor horizontal velocity-to-position temporal integration

Storage of briefly presented information in “working” memory correlates with persistent firing in the brain. Persistent activity in response to transient stimulation is a form of neural temporal integration. Here, the mechanism of temporal integration was explored in the oculomotor velocity-to-position neural integrator (VPNI), where persistent activity is used to maintain eye position and fixation. Extracellular and intracellular electrophysiology, single-cell dye-labeling, and pharmacological inactivation were performed in awake behaving goldfish while monitoring eye motion with the scleral search-coil method.; Neurons identified within a compact subnucleus in the medulla designated as Area I are part of the VPNI for horizontal eye movements. Neurons fired tonically during fixations, with tonic rate higher for lateral eye positions and no discharge below a threshold position value. Dye-labeled somata were localized in a 350 micron extent of the inferior reticular formation. Axons either projected ipsilaterally to abducens motoneurons, or crossed the midline and projected toward the contralateral Area I and abducens. Bilateral inactivation of Area I induced inability to maintain eccentric gaze.; During intracellular recording, step changes in eye position and firing rate were accompanied by steps in underlying membrane potential. Steps remained when neurons were hyperpolarized below action potential threshold. Perturbation with brief intracellular current pulses only induced transient changes in firing rate and potential. Membrane potential fluctuations were greater during more depolarized steps. These results suggest that steps are generated by synaptic input changes rather than intrinsic properties like membrane multistability.; Spiking of unilateral pairs was positively correlated with 0–10 ms lag. Bilateral pairs were negatively correlated with 0–10 ms lag. These results are consistent with excitatory connections between unilateral pairs and inhibitory connections between bilateral pairs.; The precise role of synaptic interaction was tested by pharmacological inactivation of part of the VPNI. Inactivation of ipsilateral Area I neurons disrupted persistent firing of non-inactivated cells, with effects most pronounced at high rates. Inactivation of contralateral Area I neurons also disrupted persistent firing, with effects most pronounced at low rates.; These results suggest that both recurrent ipsilateral excitatory and contralateral inhibitory connections contribute to integration, apparently by mediating positive feedback.