Plane-specific Purkinje cell responses to vertical head rotations in the cat cerebellar nodulus and uvula

Abstract

We recorded simple spike (SS) and complex spike (CS) firing of Purkinje cell in the cerebellar nodulus and uvula of awake, head-restrained cats during sinusoidal vertical rotation of the head in four stimulus planes (pitch, roll, and two vertical canal planes). Two SS response types (position- and velocity-types) with response phases close to those of head position and velocity, respectively, were recognized. Optimal response planes and directions for SS and CS of each cell were estimated from the response amplitudes in the four stimulus planes by fitting with a sinusoidal function. The principal findings are as follows: (1) two rostrocaudally oriented functional zones of Purkinje cells can be distinguished; (2) the medially located parasagittal band is active during rotation in the pitch plane; (3) the laterally located band is active during rotation in the roll plane. These two zones are the same as previously reported zones in the cerebellar flocculus active during head rotation in the canal planes in the point that both cerebellar sagittal zones are plane-specific functional zones, suggesting that the anatomical sagittal zones serve as functional plane-specific zones at least in the vestibulocerebellum.

Two functionally distinct Purkinje cell populations implement an internal model within a single olivo-cerebellar loop

“…Considering that tilt-selective cells encode velocity , 'velocity' cells likely correspond to tilt-selective cells, whereas 'position' cells likely correspond to translation-selective cells. This interpretation is corroborated by the SS modulation gain during tilt at 0.5Hz: 133 and 64 spk/s/G respectively for 'velocity' and 'position' cells respectively in (Kitama et al, 2014), that match our recordings (Fig. 3A).…”

“…Previous CS studies were limited to rotation stimuli (Barmack & Shojaku, 1995;Fushiki & Barmack, 1997;Kitama et al, 2014;Yakhnitsa & Barmack, 2006), or only characterized translation-selective cells (Yakusheva et al, 2010). A crucial, yet unanswered, question is whether CS firing is different in tiltselective and translation-selective cells: this would imply that there are two distinct cerebellar loops.…”

“…Olivo-cerebellar loops in the NU have been studied in rabbits (Barmack & Shojaku, 1995;Fushiki & Barmack, 1997), mice (Yakhnitsa & Barmack, 2006) and cats (Kitama et al, 2014) using exclusively rotation (but not translation) stimuli. Although it is impossible to test the current hypotheses in the absence of translation stimuli, findings from these studies are consistent with the present results.…”

“…Despite a good understanding on the properties of SS responses, little is currently known about CSs, which are fundamental for understanding the organisation of the corresponding cerebellar circuits. Previous CS studies were limited to rotation stimuli (Barmack & Shojaku, 1995; Fushiki & Barmack, 1997; Kitama et al, 2014; Yakhnitsa & Barmack, 2006), or only characterized translation-selective cells (Yakusheva et al, 2010). A crucial, yet unanswered, question is whether CS firing is different in tilt-selective and translation-selective cells: this would imply that there are two distinct cerebellar loops.…”

The neural basis of motion sickness

“…Three zones have been described in the nodulus (Wearne et al 1997;1998). One senses the orientation of the head and body to gravity (Angelaki et al 2010;Raphan and Cohen 2002;Tarnutzer et al 2011Tarnutzer et al , 2015 a second is primarily oriented to roll Hess 1994, 1995;Kim et al 2009;Walker et al 2008) with some pitch (Kitama et al 2014), and a third has strong inhibitory control of the velocity storage integrator in the vestibular nuclei (Solomon and Cohen 1992;Meng et al 2014).…”