An attempt was made by Miles and Lisberger (1981) to address this question, but the best they could do was to put a ‘black-box’ (see Fig. 1, flocculus) around the granular-Purkinje circuit and then, to say, that once a new gain has been calibrated for the vestibulo-ocular reflex that the granular-Purkinje circuit is no longer necessary for the execution of the vestibulo-ocular response. That the flocculus/vestibular nuclei receive proprioceptive information about the position of the head and eyes is well established (Cullen 2012), but it remains unclear how this information would be used to contribute to reset the gain. There has been a long tradition in oculomotor neurophysiology to disqualify the role of proprioception in eye movement control (e.g., Robinson 1981), even though there is overwhelming evidence that proprioception affects ocular behavior, particularly at the level of the cerebellum (Chen 2019; Noda et al. 1991; Roll and Roll 1987; Roll et al. 1991; Valey et al. 1994, 1995, 1997).
A common conscious experience following vestibular receptor damage is that when the head moves vertigo is elicited (Cullen 2012). Astronauts returning to earth experience this sensation as well, since they need to adjust to a new gravitational force (Demontis et al. 2017). To minimize vertigo, astronauts try to limit their head movements, a behavior that can last up to a week before the vestibulo-ocular reflex is fully calibrated (Carriot et al. 2021). It is now clear that to adjust the gain of the vestibulo-ocular reflex many senses participate in this process, including the visual sense, the vestibular sense, and the proprioceptive sense (Cullen 2012). For example, when adjusting to magnifying or minimizing prisms the eye movements that counter rotate once the head is in motion for the vestibulo-ocular reflex, the peak velocity of the eye movements must be increased or decreased accordingly (Lisberger and Fuchs 1978; Lisberger and Miles 1981) to eventually generate a reflex with latencies as short as 5 to 6 ms (Hunter and Cullen 2002). To bring about adaptation, the visual sense is not sufficient by itself, given the great delay of 30 ms or more between the retina and the cerebellum. To facilitate the adaptive process, both the vestibular and the proprioceptive senses, whose signals can reach the cerebellum at a minimal latency of 4 ms (Fuchs and Kornhuber 1969; Shinoda and Yoshima 1975), need to signal the start and stop position of the head and eyes which utilize the vestibular receptors attached to the head and the proprioceptors attached to the head and eyes.
Now back to the ‘black box’ of Miles and Lisberger (1981, see Fig. 1, flocculus), which is composed of granular and Purkinje neurons at the level of the cerebellar cortex. Much is known about the Purkinje neurons in terms of how the gains to the neurons are altered via inputs from the mossy and climbing fibres (Bell et al. 1997; De Zeeuw 2021; Ito and Miyashita 1975; Loyola et al. 2019; Robinson 1976; Shadmehr 2020; Tehovnik et al. 2021; Wang et al. 2023), but much less is known about how the granular cells, which are the most abundant neurons of the brain (Herculano-Houzel 2009; Huang 2008), process visual, vestibular, and proprioceptive information to calibrate the vestibulo-ocular reflex. Miles and Braitman (1980) recorded from 771 granular-layer cells of the flocculus of the cerebellum of the monkey. Just over half the neurons were modulated by saccadic eye movements and most of these were silent during fixation (which means eyes fixed in orbit with respect to the head). The remaining neurons were modulated by fixation of the eyes in orbit, and these neurons discharged to a particular direction of pursuit eye movement over a range of eye velocities. A third of the neurons responded over a range of head movement velocities as well. A minority of neurons responded to vergence/ accommodation, blinking, and visual input. The granular neurons have all the characteristics to calibrate the vestibulo-ocular reflex. What is not known is how proprioception (of the head and eyes) contributes to the adaptation process, since most models are based on putting the vestibular signal in register with the pursuit movement signal with no explicit representation of proprioception in the adaptive process.
Figure 1: The ‘black box’ of Miles and Lisberger (1981, Fig. 3).
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