Neural circuits for triggering saccades in the brainstem.

Department of Systems Neurophysiology, Graduate School of Medicine, Tokyo Medical and Dental University, Yushima, Bunkyo-ku, Tokyo 113-8519, Japan.
Progress in brain research (Impact Factor: 4.19). 02/2008; 171:79-85. DOI: 10.1016/S0079-6123(08)00611-0
Source: PubMed

ABSTRACT Here we review the functional anatomy of brainstem circuits important for triggering saccades. Whereas the rostral part of the superior colliculus (SC) is considered to be involved in visual fixation, the caudal part of the SC plays an important role in generation of saccades. We determined the neural connections from the rostral and caudal parts of the SC to inhibitory burst neurons (IBNs) and omnipause neurons (OPNs) in the nucleus raphe interpositus. To reveal the neural mechanisms of triggering saccadic eye movements, we analysed the effects of stimulation of the SC on intracellular potentials recorded from IBNs and OPNs in anaesthetized cats. Our studies show that IBNs receive monosynaptic excitation from the contralateral caudal SC, and disynaptic inhibition from the ipsilateral caudal SC, via contralateral IBNs. Further, IBNs receive disynaptic inhibition from the rostral part of the SC, on either side, via OPNs. Intracellular recording revealed that OPNs receive excitation from the rostral parts of the bilateral SCs, and disynaptic inhibition from the caudal SC mainly via IBNs. The neural connections determined in this study are consistent with the notion that the "fixation zone" is localized in the rostral SC, and suggest that IBNs, which receive monosynaptic excitation from the caudal "saccade zone," may inhibit tonic activity of OPNs and thereby trigger saccades.

  • [Show abstract] [Hide abstract]
    ABSTRACT: The saccade trigger signal was proposed by D.A. Robinson, but neural substrates for triggering saccades by inhibiting omnipause neuron (OPN) activity still remain controversial. We investigated tectal inputs to OPNs by recording intracellular potentials from OPNs and inhibitory burst neurons (IBNs) and searched for interneurons to inhibit OPNs in the brainstem of anesthetized cats. IBNs received monosynaptic excitation from the contralateral caudal superior colliculus (SC) and disynaptic inhibition via contralateral IBNs from the ipsilateral caudal SC, whereas IBNs received disynaptic inhibition from the rostral SC. The latter disynaptic inhibition was mediated by OPNs, since OPNs received monosynaptic excitation from the rostral SC and projected to IBNs. In contrast, OPNs received disynaptic inhibition from the caudal SC. This disynaptic inhibition from the caudal SC was mediated to OPNs by IBNs. These findings suggested possible roles of IBNs for triggering and maintaining saccades by actively inhibiting the tonic activity of OPNs.
    Annals of the New York Academy of Sciences 09/2011; 1233:100-6. · 4.38 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Intelligent agents balance speed of responding with accuracy of deciding. Stochastic accumulator models commonly explain this speed-accuracy tradeoff by strategic adjustment of response threshold. Several laboratories identify specific neurons in prefrontal and parietal cortex with this accumulation process, yet no neurophysiological correlates of speed-accuracy tradeoff have been described. We trained macaque monkeys to trade speed for accuracy on cue during visual search and recorded the activity of neurons in the frontal eye field. Unpredicted by any model, we discovered that speed-accuracy tradeoff is accomplished through several distinct adjustments. Visually responsive neurons modulated baseline firing rate, sensory gain, and the duration of perceptual processing. Movement neurons triggered responses with activity modulated in a direction opposite of model predictions. Thus, current stochastic accumulator models provide an incomplete description of the neural processes accomplishing speed-accuracy tradeoffs. The diversity of neural mechanisms was reconciled with the accumulator framework through an integrated accumulator model constrained by requirements of the motor system.
    Neuron 11/2012; 76(3):616-28. · 15.77 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Omnipause neurons (OPNs) within the nucleus raphe interpositus (RIP) help gate the transition between fixation and saccadic eye movements by monosynaptically suppressing activity in premotor burst neurons during fixation, and releasing them during saccades. Premotor neuron activity is initiated by excitatory input from the superior colliculus (SC), but how the tectum's saccade-related activity turns off OPNs is not known. Since the central mesencephalic reticular formation (cMRF) is a major SC target, we explored whether this nucleus has the appropriate connections to support tectal gating of OPN activity. In dual-tracer experiments undertaken in macaque monkeys (Macaca fascicularis), cMRF neurons labeled retrogradely from injections into RIP had numerous anterogradely labeled terminals closely associated with them following SC injections. This suggested the presence of an SC-cMRF-RIP pathway. Furthermore, anterograde tracers injected into the cMRF of other macaques labeled axonal terminals in RIP, confirming this cMRF projection. To determine whether the cMRF projections gate OPN activity, postembedding electron microscopic immunochemistry was performed on anterogradely labeled cMRF terminals with antibody to GABA or glycine. Of the terminals analyzed, 51.4% were GABA positive, 35.5% were GABA negative, and most contacted glycinergic cells. In summary, a trans-cMRF pathway connecting the SC to the RIP is present. This pathway contains inhibitory elements that could help gate omnipause activity and allow other tectal drives to induce the bursts of firing in premotor neurons that are necessary for saccades. The non-GABAergic cMRF terminals may derive from fixation units in the cMRF.
    Journal of Neuroscience 10/2013; 33(41):16285-16296. · 6.91 Impact Factor