Widespread vestibular activation of the rodent cortex (original) (raw)
Related papers
Differentiating ascending vestibular pathways to the cortex involved in spatial cognition
Journal of Vestibular Research
Vestibular information is an important factor in maintaining accurate spatial awareness. Yet, each of the cortical areas involved in processing vestibular information has unique functionality. Further, the anatomical pathways that provide vestibular input for cognitive processes are also distinct. This review outlines some of the current understanding of vestibular pathways contributing to the perception of self-motion in the cortex. The vestibulo-thalamic pathway is associated with self-motion cues for updating motor behaviors, spatial representations, and self versus object motion distinctions. The mammillo-tegmental pathway supplies vestibular input to create a cognitive representation of head direction. Self-motion and head direction information then converge to define self-location. By outlining the functional anatomy of the vestibular cortical pathways, a multi-sensory and multi-faceted view of vestibular related spatial awareness emerges.
Hippocampal spatial representations require vestibular input
Hippocampus, 2002
The hippocampal formation is essential for forming declarative representations of the relationships among multiple stimuli. The rodent hippocampal formation, including the entorhinal cortex and subicular complex, is critical for spatial memory. Two classes of hippocampal neurons fire in relation to spatial features. Place cells collectively map spatial locations, with each cell firing only when the animal occupies that cell's "place field," a particular subregion of the larger environment. Head direction (HD) cells encode directional heading, with each HD cell firing when the rat's head is oriented in that cell's particular "preferred firing direction." Both landmarks and internal cues (e.g., vestibular, motor efference copy) influence place and HD cell activity. However, as is the case for navigation, landmarks are believed to exert greater influence over place and HD cell activity. Here we show that temporary inactivation of the vestibular system led to the disruption of location-specific firing in hippocampal place cells and direction-specific discharge of postsubicular HD cells, without altering motor function. Place and HD cell activity recovered over a time course similar to that of the restoration of vestibular function. These results indicate that vestibular signals provide an important influence over the expression of hippocampal spatial representations, and may explain the navigational deficits of humans with vestibular dysfunction.
The vestibular contribution to the head direction signal and navigation
Frontiers in Integrative Neuroscience, 2014
Spatial learning and navigation depend on neural representations of location and direction within the environment. These representations, encoded by place cells and head direction (HD) cells, respectively, are dominantly controlled by visual cues, but require input from the vestibular system. Vestibular signals play an important role in forming spatial representations in both visual and non-visual environments, but the details of this vestibular contribution are not fully understood. Here, we review the role of the vestibular system in generating various spatial signals in rodents, focusing primarily on HD cells. We also examine the vestibular system's role in navigation and the possible pathways by which vestibular information is conveyed to higher navigation centers.
INTEGRATIVE NEUROSCIENCE Vestibular pathways involved in cognition
Recent discoveries have emphasized the role of the vestibular system in cognitive processes such as memory, spatial navigation and bodily self-consciousness. A precise understanding of the vestibular pathways involved is essential to understand the consequences of vestibular diseases for cognition, as well as develop therapeutic strategies to facilitate recovery. The knowledge of the "vestibular cortical projection areas" , defined as the cortical areas activated by vestibular stimulation, has dramatically increased over the last several years from both anatomical and functional points of view. Four major pathways have been hypothesized to transmit vestibular information to the vestibular cortex: (1) the vestibulo-thalamo-cortical pathway, which probably transmits spatial information about the environment via the parietal, entorhinal and perirhinal cortices to the hippocampus and is associated with spatial representation and self-versus object motion distinctions; (2) the pathway from the dorsal tegmental nucleus via the lateral mammillary nucleus, the anterodorsal nucleus of the thalamus to the entorhinal cortex, which transmits information for estimations of head direction; (3) the pathway via the nucleus reticularis pontis oralis, the supramammillary nucleus and the medial septum to the hippocampus, which transmits information supporting hippocampal theta rhythm and memory; and (4) a possible pathway via the cerebellum, and the ventral lateral nucleus of the thalamus (perhaps to the parietal cortex), which transmits information for spatial learning. Finally a new pathway is hypothesized via the basal ganglia, potentially involved in spatial learning and spatial memory. From these pathways, progressively emerges the anatomical network of vestibular cognition.
Rats with lesions of the vestibular system require a visual landmark for spatial navigation
Behavioural Brain Research, 2002
The role of the vestibular system in acquisition and performance of a spatial navigation task was examined in rats. Male Long-Evans rats received sham or bilateral sodium arsanilate-induced vestibular lesions. After postoperative recovery, under partial water-deprivation, rats were trained (16 trials/day) to find a water reward in one corner of a black square enclosure. A cue card fixed to one wall of the enclosure served as a stable landmark cue. The orientation of the rat at the start of each trial was pseudo-randomized such that the task could not be solved by an egocentric response strategy. Rats with vestibular lesions acquired the task in fewer trials than the sham treated control rats. Vestibular lesions did not influence the motivation or motor function necessary to perform the task. Performance of sham rats was maintained during probe trials in which the cue card was removed from the enclosure, while lesioned rats were markedly impaired. Rotation of the cue card ( 9 90°) caused an equivalent shift in corner choice behavior of the lesioned rats. However, sham rats often disregarded the rotated cue card and made place responses. These results suggest that the vestibular lesions disrupt idiothetic navigation or path integration and render navigational behavior critically dependent upon external landmarks. These results are consistent with the navigational abilities of humans with bilateral vestibular dysfunction.
Optogenetic fMRI interrogation of brain-wide central vestibular pathways
Proceedings of the National Academy of Sciences
Blood oxygen level-dependent functional MRI (fMRI) constitutes a powerful neuroimaging technology to map brain-wide functions in response to specific sensory or cognitive tasks. However, fMRI mapping of the vestibular system, which is pivotal for our sense of balance, poses significant challenges. Physical constraints limit a subject’s ability to perform motion- and balance-related tasks inside the scanner, and current stimulation techniques within the scanner are nonspecific to delineate complex vestibular nucleus (VN) pathways. Using fMRI, we examined brain-wide neural activity patterns elicited by optogenetically stimulating excitatory neurons of a major vestibular nucleus, the ipsilateral medial VN (MVN). We demonstrated robust optogenetically evoked fMRI activations bilaterally at sensorimotor cortices and their associated thalamic nuclei (auditory, visual, somatosensory, and motor), high-order cortices (cingulate, retrosplenial, temporal association, and parietal), and hippoca...
Visual-vestibular and visuovisual cortical interaction: New insights from fMRI and PET
Annals of the New York Academy of Sciences
PET and fMRI studies have revealed that excitation of the vestibular system by caloric or galvanic stimulation not only activates the parietoinsular vestibular cortex but also bilaterally deactivates the occipital visual cortex. Likewise, visual motion stimulation not only activates the visual cortex but also deactivates the parietoinsular vestibular cortex. These findings are functionally consistent with the hypothesis of an inhibitory reciprocal visual-vestibular interaction for spatial orientation and motion perception. Transcallosal visuovisual interaction between the two hemispheres was found by using half-field visual motion stimulation: activation of motion-sensitive areas hMT/V5 and deactivations of the primary visual cortex contralateral to the stimulated hemisphere. The functional significance of these inter- and intra-sensory interactions could be that they (A) allow a shift of the sensorial weight between two incongruent sensory inputs and (B) ensure a correspondence of ...
Cortical projection of peripheral vestibular signaling
Journal of …, 2003
The cerebral projection of vestibular signaling was studied by using PET with a special differential experimental protocol. Caloric vestibular stimulation (CVS)-induced regional cerebral blood flow (rCBF) changes were investigated in two populations. Butanol perfusion scans were carried out on six healthy volunteers and on six patients following the removal of tumors from the right cerebello pontine angle. The complete loss of the vestibular function postoperatively allowed a comparison of the rCBF changes in the populations with or without this input and offered a promising functional approach whereby to delineate the cortical region most responsive to pure vestibular input. The activations by left-sided and right-sided CVS were determined for both the healthy volunteers and the patient population. Statistical analysis of the data obtained following leftsided CVS did not reveal any cerebral region for which there was a significant difference in CVS-induced response by these two populations. In the case of right-sided CVS, however, the statistical comparison of the CVS-related responses demonstrated a single contralateral area characterized by a significantly different degree of response. This cortical area corresponds to part of the cortical region described recently which can be activated by both CVS and neck vibration. It appears to be anatomically identical to the aggregate of the somatosensory area SII and the retroinsular cortex described in primates, a region identified by other investigators as an analog of the parietoinsular vestibular cortex.
NeuroImage, 2002
Anatomic and electrophysiological studies in monkeys have yielded a detailed map of cortex areas receiving vestibular afferents. In contrast, comparatively little is known about the cortical representation of the human vestibular system. In this study we applied caloric stimulation and fMRI to further characterize human cortical vestibular areas and to test for hemispheric dominance of vestibular information processing. For caloric vestibular stimulation we used cold nitrogen to avoid susceptibility artifacts induced by water calorics. Right and left side vestibular stimulation was repetitively performed inducing a nystagmus for at least 90 s after the end of the stimulation in all subjects. Only the first 60 s of this nystagmus period was included for statistical analysis and compared with the baseline condition. Activation maps revealed a cortical network with right hemispheric dominance, which in all subjects comprised the temporoparietal junction extending into the posterior insula and, furthermore, the anterior insula, pre-and postcentral gyrus, areas in the parietal lobe, the ventrolateral portion of the occipital lobe, and the inferior frontal gyrus extending into the inferior part of the precentral sulcus. In conclusion, caloric stimulation in fMRI reveals a widespread cortical network involved in vestibular signal processing corresponding to the findings from animal experiments and previous functional imaging studies in humans. Furthermore, this study demonstrates a strong right hemispheric dominance of vestibular cortex areas regardless of the stimulated side, consistent with the current view of a rightward asymmetrical cortical network for spatial orientation.