4.7 Article

Brainstem Circuits Triggering Saccades and Fixation

Journal

JOURNAL OF NEUROSCIENCE
Volume 42, Issue 5, Pages 789-803

Publisher

SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.1731-21.2021

Keywords

eye movement; inhibitory burst neuron; oculomotor; omnipause neuron; saccade trigger; superior colliculus

Categories

Funding

  1. Japan Science and Technology Agency FOREST (Fusion Oriented Research for Disruptive Science and Technology) Grant [JPMJFR2044]
  2. Japan Society for the Promotion of Science (JSPS) [JP19K06937]
  3. JSPS KAKENHI [JP18300133, JP18K06517]

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The study identified different neural inputs from the rostral and caudal superior colliculi to the nucleus raphe interpositus, showing that inhibitory burst neurons suppress activity of omnipause neurons immediately before and during saccades. This suggests a role for IBNs in triggering and controlling eye movements.
Omnipause neurons (OPNs) in the nucleus raphe interpositus have tonic activity while the eyes are stationary (fixation) but stop firing immediately before and during saccades. To locate the source of suppression, we analyzed synaptic inputs from the rostral and caudal superior colliculi (SCs) to OPNs by using intracellular recording and staining, and investigated pathways transmitting the inputs in anesthetized cats of both sexes. Electrophysiologically or morphologically identified OPNs received monosynaptic excitation from the rostral SCs with contralateral dominance, and received disynaptic inhibition from the caudal SCs with ipsilateral dominance. Cutting the tectoreticular tract transversely between the contralateral OPN and inhibitory burst neuron (IBN) regions eliminated inhibition from the caudal SCs, but not excitation from the rostral SCs in OPNs. In contrast, a midline section between IBN regions eliminated disynaptic inhibition in OPNs from the caudal SCs but did not affect the monosynaptic excitation from the rostral SCs. Stimulation of the contralateral IBN region evoked monosynaptic inhibition in OPNs, which was facilitated by preconditioning SC stimulation. Three-dimensional reconstruction of HRP-stained cells revealed that individual OPNs have axons that terminate in the opposite IBN area, while individual IBNs have axon collaterals to the opposite OPN area. These results show that there are differences in the neural circuit from the rostral and caudal SCs to the brainstem premotor circuitry and that IBNs suppress OPNs immediately before and during saccades. Thus, the IBNs, which are activated by caudal SC saccade neurons, shut down OPN firing and help to trigger saccades and suppress (latch) OPN activity during saccades.

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