Functional Implications of Ubiquitous Semicircular Canal Non-Orthogonality in Mammals

The ‘canonical model’ of semicircular canal orientation in mammals assumes that 1) the three ipsilateral canals of an inner ear exist in orthogonal planes (i.e., orthogonality), 2) corresponding left and right canal pairs have equivalent angles (i.e., angle symmetry), and 3) contralateral synergistic canals occupy parallel planes (i.e., coplanarity). However, descriptions of vestibular anatomy that quantify semicircular canal orientation in single species often diverge substantially from this model. Data for primates further suggest that semicircular canal orthogonality varies predictably with the angular head velocities encountered in locomotion. These observations raise the possibility that orthogonality, symmetry, and coplanarity are misleading descriptors of semicircular canal orientation in mammals, and that deviations from these norms could have significant functional consequences. Here we critically assess the canonical model of semicircular canal orientation using high-resolution X-ray computed tomography scans of 39 mammal species. We find that substantial deviations from orthogonality, angle symmetry, and coplanarity are the rule for the mammals in our comparative sample. Furthermore, the degree to which the semicircular canals of a given species deviate from orthogonality is negatively correlated with estimated vestibular sensitivity. We conclude that the available comparative morphometric data do not support the canonical model and that its overemphasis as a heuristic generalization obscures a large amount of functionally relevant variation in semicircular canal orientation between species.Funding for this research was provided by grants NSFIIS-0208675 (http://www.nsf.gov/cise/iis/hcc_pgm.jsp), and EAR-0948842 (http://www.nsf.gov/awards/award_visualiz​ation.jsp?org=EAR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Geological SciencesAnthropologyEmail: [email protected]

The human semicircular canal model of galvanic vestibular stimulation

A vector summation model of the action of galvanic stimuli on the semicircular canals has been shown to explain empirical balance and perceptual responses to binaural-bipolar stimuli. However, published data suggest binaural-monopolar stimuli evoke responses that are in the reverse direction of the model prediction. Here, we confirm this by measuring balance responses to binaural-monopolar stimulation as movements of the upper trunk. One explanation for the discrepancy is that the galvanic stimulus might evoke an oppositely directed balance response from the otolith organs that sums with and overrides the semicircular canal response. We tested this hypothesis by measuring sway responses across the full range of head pitch. The results showed some modulation of sway with pitch such that the maximal response occurred with the head in the primary position. However, the effect fell a long way short of that required to reverse the canal sway response. This indicates that the model is incomplete. Here, we examine alterations to the model that could explain both the bipolar and monopolar-evoked behavioural responses. An explanation was sought by remodelling the canal response with more recent data on the orientation of the individual canals. This improved matters but did not reverse the model prediction. However, the model response could be reversed by either rotating the entire labyrinth in the skull or by altering the gains of the individual canals. The most parsimonious solution was to use the more recent canal orientation data coupled with a small increase in posterior canal gain

Projections from visual areas of the cerebral cortex to pretectal nuclear complex, terminal accessory optic nuclei, and superior colliculus in macaque monkey

The purpose of this study was to analyze the projections from visually related areas of the cerebral cortex of rhesus monkey to subcortical nuclei involved in eye-movement control; i.e., the pretectal nuclear complex, the terminal nuclei of the accessory optic system (AOS), and the superior colliculus (SC). The anterograde tracer H-3-leucine was pressure injected bilaterally into the cortex of six monkeys (for a total of 12 cases) involving the primary visual cortex (area 17); the medial prestriate cortex (medial 18/19); dorsomedial area 19; the caudal portion of the cortex of the superior temporal sulcus, upper bank (cytoarchitectural area OAa) and lower bank (area PGa); the lower bank of the caudal lateral intraparietal sulcus (area POa); and the inferior parietal lobule (area 7). The results revealed that the pretectal nucleus of the optic tract received inputs from medial prestriate cortex, dorsomedial part of area 19, OAa, and PGa. The posterior pretectal nucleus received sparse projections from area 7 and the cortex lining the intraparietal sulcus (dorsomedial part of area 19 and POa). The pretectal olivary nucleus was targeted by neurons in cortex of dorsomedial area 19, and the anterior pretectal nucleus was targeted by neurons in both dorsomedial 19 and area 7. The nuclei of the AOS (dorsal terminal; lateral terminal; and interstitial nuclei of the superior fasciculus, posterior and medial fibers) received projections exclusively from areas OAa and PGa. Furthermore, in one case with PGa injection, the medial terminal nucleus, dorsal portion, was also labeled. The visual cortical areas studied projected differentially upon the SC laminae. The primary visual area 17 projected only to the superficial laminae, i.e., stratum zonale (SZ), stratum griseum superficiale (SGS), and stratum opticum (SO). On the other hand, the medial portion of the prestriate cortex and caudal OAa and PGa targeted the superficial and intermediate laminae, i.e., SZ, SGS, SO, and stratum griseum intermediale (SGI), whereas caudal area POa projected primarily to the intermediate layer SGI. Rostral area 7 (mainly 7b) neurons terminated in the stratum album intermediale (SAI); no SC terminals were found in a case in which caudal area 7 (mainly 7a) was injected

Cortical and subcortical afferents to the nucleus reticularis tegmenti pontis and basal pontine nuclei in the macaque monkey

Anatomical findings are presented that identify cortical and subcortical sources of afferents to the nucleus reticularis tegmenti pontis (NRTP) and basal pontine nuclei. Projections from the middle temporal visual area (MT), medial superior temporal visual area (MST), lateral intraparietal area (LIP), and areas 7a. and 7b to the basal pontine nuclei were studied using H-3-leucine autoradiography. The results complemented a parallel study of retrograde neuronal labeling attributable to injecting WGA-HRP into NRTP and neighboring pontine nuclei. Small 3H-leucine injections confined to MT, MST, LIP, area 7a, or area 7b, produced multiple patches of pontine terminal label distributed as follows: (1) An injection within MT produced terminal label limited to the dorsolateral and lateral pontine nuclei, (2) Injections restricted to MST or LIP showed patches of terminal label in the dorsal, dorsolateral, lateral, and peduncular pontine nuclei. (3) Area 7a targets the dorsal, dorsolateral, lateral, peduncular, and ventral pontine nuclei, whereas area 7b projects, additionally, to the dorsomedial and paramedian pontine nuclei. Notably, no projections were seen to NRTP from any of these cortical areas. In contrast, injections made by other investigators into cortical areas anterior to the central sulcus revealed cerebrocortical afferents to NRTP, in addition to nuclei of the basal pontine gray. With our pontine WGA-HRP injections, retrograde neuronal labeling was observed over a large extent of the frontal cortex continuing onto the medial surface which included the lining of the cingulate sulcus and cingulate gyrus. Significant subcortical sources for afferents to the NRTP and basal pontine nuclei were the zona incerta, ventral mesencephalic tegmentum, dorsomedial hypothalamic area, rostral interstitial nucleus of the medial longitudinal fasciculus, red nucleus, and subthalamic nucleus. The combined anterograde and retrograde labeling data indicated that visuo-motor cortico-pontine pathways arising from parietal cortices target only the basal pontine gray, whereas the NRTP, together with select pontine nuclei, is a recipient of afferents from frontal cortical areas. The present findings implicate the existence of parallel direct and indirect cortico-pontine pathways from frontal motor-related cortices to NRTP and neighboring pontine nuclei

Planar Relationships of the Semicircular Canals in Two Strains of Mice

The mouse is increasingly important as a subject of vestibular research. Although many studies have focused on the vestibular responses of mice to angular rotation, the geometry of their semicircular canals has not been described. High-voltage X-ray computed tomography was used to measure the anatomy of the semicircular canals of two strains of mice, C57Bl/6J and CBA/CaJ. The horizontal plane of a stereotaxic coordinate system was defined by the midpoints of the external auditory meati and the point where the incisors emerge from the maxilla. The centroids of the lumens of the bony canals were calculated, and planes that describe the canals were fit using a least-squares regression analysis to the resulting points. Vectors normal to each regressed plane were used to represent the corresponding canal's axis of rotation, and angles of these vectors relative to skull landmarks as well as to each other were calculated. The horizontal canal of the mouse was found to be angled anteriorly upward 17.8° for CBA/CaJ and 32.6° for C57Bl/6J from the reference horizontal plane. Angles between ipsilateral canals deviated up to 12.3° from orthogonal, and angles between contralateral synergistic canals (left anterior–right posterior, right anterior–left posterior, and horizontal–horizontal) deviated from parallel by up to 14.8°. The orientations of the canals within the head as well as the orientations of the canals relative to each other were significantly different between the two strains, suggesting that care must be taken in the design and interpretation of developmental and physiologic studies involving different mouse strains