Responses of Single Neurons in the Parietoinsular Vestibular Cortex of Primates^a

Abstract

1. Neurons activated by stimulation of the horizontal and/or vertical vestibular semicircular canals were recorded in the parietoinsular vestibular cortex in four awake Java monkeys (Macaca fascicularis) and three squirrel monkeys (Saimiri sciureus). Steady tilt in darkness or during illumination of a vertically striped cylinder or of the normal laboratory surroundings did not lead to a significant change in PIVC neuron activity. Thus vestibular input to this cortical region seems to be restricted to signals originating in the semicircular canal receptors. 2. Vestibular stimulation in the three main experimental planes (roll, yaw, and pitch) and in planes in between provided clear evidence that optimum activation can be found in planes that do not coincide with the planes of the semicircular canals but are distributed over all possible spatial planes through the head. 3. Definite evidence of clustering in subdivisions of PIVC of neurons responding to the same optimum rotation plane was obtained in squirrel monkeys and is also suggested to exist in PIVC of Java monkeys. 4. Nearly all neurons responding to vestibular stimulation were also activated by visual large-field movement (optokinetic stimulation). Responses to optokinetic stimuli were always at optimum when the direction of the movement pattern corresponded to the optimum vestibular plane. Two classes of visual-vestibular interaction were found: Synergistic neurons were those PIVC cells with the strongest response to visual movement stimulation in the opposite direction to that leading to a maximum response to vestibular stimulation. Antagonistic neurons had a response maximum when the visual stimulus was moved in the direction of optimum vestibular stimulation. 5. Most PIVC neurons responded to stimulation of the deep mechanoreceptors in the neck region. This input from the neck receptors was tested quantitatively only in the horizontal plane (trunk rotation with the head fixed in space or head rotation with the trunk fixed in space). It interacted with vestibular signals at the PIVC neurons either in an antagonistic or a synergistic manner, the latter meaning activation during rotation of the head in the same direction as that leading to activation induced by semicircular canal stimulation. 6. In addition to the direction-specific vestibular, visual, and neck receptor inputs, a rather complex somatosensory input to PIVC neurons exists, including responses to stimulation of mechanoreceptors of the skin, the muscles, and the joint receptors of legs and arms. Total body vibration also led to activation of some of the neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Visual-vestibular processing in the human Sylvian fissure

“…Single-cell recordings in primates (Chen et al 2010) and functional imaging studies in humans (Brandt et al 1998;Deutschländer et al 2002;Kleinschmidt et al 2002) repeatedly reported little activation or even deactivation in PIVC during stimulation with visual object motion cues [but note that PIVC neurons appear to become activated when a moving object is actively tracked (see Shinder and Newlands 2014) or during full field visual motion (Akbarian et al 1988)]. Some imaging studies in humans found activation in the posterior Sylvian fissure during self-motion sensations induced by visual motion cues (see Cardin and Smith 2010;Huang et al 2015;Uesaki and Ashida 2015).…”

“…This information is of critical relevance for guiding locomotion and for process- There is accumulating evidence that the potential hub of the cortical vestibular network is located in a region including the posterior part of the Sylvian fissure (also called lateral sulcus), perisylvian cortex, and the posterior insula. At this site, functional imaging studies in humans found activation during vestibular stimulation (Bense et al 2001;Dieterich et al 2003;Eickhoff et al 2006;Fasold et al 2002;Lobel et al 1998) and labeled it the parieto-insular vestibular cortex (PIVC), following terminology in the primate brain (Akbarian et al 1988;Chen et al 2010;Grüsser et al 1990; Shinder and Newlands 2014).…”

“…This information is of critical relevance for guiding locomotion and for process- There is accumulating evidence that the potential hub of the cortical vestibular network is located in a region including the posterior part of the Sylvian fissure (also called lateral sulcus), perisylvian cortex, and the posterior insula. At this site, functional imaging studies in humans found activation during vestibular stimulation (Bense et al 2001;Dieterich et al 2003;Eickhoff et al 2006;Fasold et al 2002;Lobel et al 1998) and labeled it the parieto-insular vestibular cortex (PIVC), following terminology in the primate brain (Akbarian et al 1988;Chen et al 2010;Grüsser et al 1990; Shinder and Newlands 2014).However, the vestibular network in the posterior Sylvian fissure is likely more complex and might include at least one additional area, named posterior insular cortex (PIC), that responds to vestibular stimuli as well as to visual object motion and potentially serves as a site of multisensory integration .The anatomical and functional relationship between PIC and PIVC is still unclear, because both areas have not yet been investigated in the same participant. Therefore, in this study we aimed to define and compare the regions known as PIVC and PIC directly in the same participants.…”

Multimodal Coding of Three-Dimensional Rotation and Translation in Area MSTd: Comparison of Visual and Vestibular Selectivity

“…Area MSTd lies within extrastriate visual cortex and is not typically considered to be a part of "vestibular cortex," which is thought to include the parieto-insular vestibular cortex, area 2v, and area 3a (Schwarz and Fredrickson, 1971;Akbarian et al, 1988;Fukushima, 1997). Yet, we have shown that MSTd responses during physical movement in the absence of optic flow arise from sensory signals originating in the vestibular labyrinths.…”

Identifying human parieto‐insular vestibular cortex using fMRI and cytoarchitectonic mapping

“…1). However, the cortical area, which is interconnected most densely with all other "vestibular" areas and with the vestibular brainstem, is the parieto-insular vestibular cortex (PIVC) in the depth of the Sylvian fissure [Akbarian et al, 1988;Grusser et al, 1990a,b;Guldin and Grusser, 1998]. This area is located in the posterior parietal operculum/retroinsular region, extending into the posterior parts of the insular lobe.…”