Monosynaptic and disynaptic connections in the utriculo-ocular reflex arc of the cat

Abstract

1. Connections from the utricular (UT) nerve to motoneurons and interneurons in the ipsilateral abducens (AB) nucleus were studied in anesthetized and decerebrated cats. Bipolar electrodes were fixed on the left UT nerve under visual observation. The other branches of the vestibular nerve and the facial nerve were transected in the left inner ear. 2. Stimulation of the UT nerve evoked a small positive-negative (P/N) deflection and a negative (N1) potential in the vestibular nuclei, with mean latencies of 0.56 and 0.84 ms, respectively. In the AB nucleus a small P/N deflection with a mean latency of 0.72 ms was recorded, which was considered as a incoming volley of the UT nerve. 3. Excitatory postsynaptic potentials (EPSPs) were recorded from AB motoneurons with short latencies after UT nerve stimulation. They were classified into two types, M and D. M-type EPSPs, which followed repetitive high-frequency stimuli and were recorded from the majority of AB motoneurons, had latencies ranging from 0.9 to 1.2 ms. Double shocks to the UT nerve evoked EPSPs that had the same latency. It was suggested that the AB motoneurons had monosynaptic connections with the UT nerve. D-type EPSPs, which were recorded from most of the AB motoneurons, had slightly longer latencies ranging from 1.2 to 1.8 ms. They showed temporal facilitation when double shocks were provided to the UT nerve. They did not follow repetitive high-frequency stimuli (< or = 2.5-ms interval). It was suggested that D-type EPSPs were di-synaptically evoked via secondary vestibular neurons. Interneurons in the AB nucleus had the same characteristics as AB motoneurons.(ABSTRACT TRUNCATED AT 250 WORDS)

Acoustic Clicks Activate both the Canal and Otolith Vestibulo-Ocular Reflex Pathways in Behaving Monkeys

“…In this study, the minimum latency of crossed, excitatory response was 1.02 ms, which was plausible for a response mediated by a disynaptic circuit given the small difference in the vestibular afferent minimum latency to electric pulses and clicks (0.33 vs. 0.4 ms). Third, as shown by several earlier studies (Uchino et al 1994(Uchino et al , 1996(Uchino et al , 1997Isu et al 2000), the latency analysis involves not only the minimum latency but also the range and distribution of the latency. According to Broussard et al (1995), the median latency of crossed, excitatory response was 1.5 ms.…”

“…To elucidate the neural pathways that mediate the two excitatory responses, we measured abducens neurons' latencies to ipsilateral and contralateral clicks and compared them to the published latencies of vestibular afferents and abducens neurons to clicks as well as to brief electrical pulses. As shown in Figure 5, it has been well established that the contralateral canal-abducens connection is excitatory and disynaptic (Scudder and Fuchs 1992) and the ipsilateral utricular-abducens connection is excitatory and monosynaptic (Uchino et al 1994(Uchino et al , 1996. The latency analysis, in combination with the well-established VOR circuits, provided important insights into understanding how clicks activate specific VOR pathways.…”

“…The otolith-ocular pathways, however, have been shown to have a very different circuitry. Specifically, the utricule projections make monosynaptic and disynaptic excitatory connections to the ipsilateral abducens neurons and trisynaptic inhibitory connections to the contralateral abducens neurons (Imagawa et al 1995;Schwindt et al 1973;Uchino et al 1994Uchino et al , 1996Uchino et al , 1997. The saccular projections make no connections to the horizontal extraocular motoneurons.…”

“…For the horizontal AVOR, extensive studies in monkeys and cats have established that the direct AVOR pathways are mainly organized in a disynaptic threeneuron-arc pattern, i.e., from the lateral canal afferents to the interneurons in the vestibular nuclei, then to the abducens motoneurons that innervate the lateral rectus muscle of the contralateral eye (Lorente De No, 1933;Scudder and Fuchs 1992). For the horizontal LVOR, Uchino et al (1994Uchino et al ( , 1996 showed that utricule afferents make monosynaptic excitatory connections to the abducens motoneurons that innervate the lateral rectus muscle of the ipsilateral eye in cats. Thus, by analyzing the sound-evoked responses in abducens neurons on both sides, we were able to determine how clicks activate the canal and otolith VOR pathways in behaving monkeys.…”

Differential Sensorimotor Processing of Vestibulo-Ocular Signals during Rotation and Translation

“…Finally, there is increasing evidence that the synaptic organization of the otolith-ocular and canal-ocular pathways is different. Whereas the shortest latency RVOR pathways are mediated dominantly by excitatory projections to the contralateral abducens, the shortest latency TrVOR pathways are instead excitatory to the ipsilateral abducens (Schwindt et al, 1973;Uchino et al, 1994Uchino et al, , 1996Uchino et al, , 1997Imagawa et al, 1995). These differences at both sensory and motor levels, as well as the existence of unique neuroanatomical connections, suggest that the sensorimotor processing of canal and otolith signals in the RVOR and TrVOR is at least partially distinct.…”