Robust vestibular self-motion signals in macaque posterior cingulate region.
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ABSTRACT:
SUBMITTER: Liu B
PROVIDER: S-EPMC8032402 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:We examined the responses of neurons in posterior parietal area 7a to passive rotational and translational self-motion stimuli, while systematically varying the speed of visually simulated (optic flow cues) or actual (vestibular cues) self-motion. Contrary to a general belief that responses in area 7a are predominantly visual, we found evidence for a vestibular dominance in self-motion processing. Only a small fraction of neurons showed multisensory convergence of visual/vestibular and linear/angular self-motion cues. These findings suggest possibly independent neuronal population codes for visual versus vestibular and linear versus angular self-motion. Neural responses scaled with self-motion magnitude (i.e., speed) but temporal dynamics were diverse across the population. Analyses of laminar recordings showed a strong distance-dependent decrease for correlations in stimulus-induced (signal correlation) and stimulus-independent (noise correlation) components of spike-count variability, supporting the notion that neurons are spatially clustered with respect to their sensory representation of motion. Single-unit and multiunit response patterns were also correlated, but no other systematic dependencies on cortical layers or columns were observed. These findings describe a likely independent multimodal neural code for linear and angular self-motion in a posterior parietal area of the macaque brain that is connected to the hippocampal formation.
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Project description:Recent studies have described vestibular responses in the dorsal medial superior temporal area (MSTd), a region of extrastriate visual cortex thought to be involved in self-motion perception. The pathways by which vestibular signals are conveyed to area MSTd are currently unclear, and one possibility is that vestibular signals are already present in areas that are known to provide visual inputs to MSTd. Thus, we examined whether selective vestibular responses are exhibited by single neurons in the middle temporal area (MT), a visual motion-sensitive region that projects heavily to area MSTd. We compared responses in MT and MSTd to three-dimensional rotational and translational stimuli that were either presented using a motion platform (vestibular condition) or simulated using optic flow (visual condition). When monkeys fixated a visual target generated by a projector, half of MT cells (and most MSTd neurons) showed significant tuning during the vestibular rotation condition. However, when the fixation target was generated by a laser in a dark room, most MT neurons lost their vestibular tuning whereas most MSTd neurons retained their selectivity. Similar results were obtained for free viewing in darkness. Our findings indicate that MT neurons do not show genuine vestibular responses to self-motion; rather, their tuning in the vestibular rotation condition can be explained by retinal slip due to a residual vestibulo-ocular reflex. Thus, the robust vestibular signals observed in area MSTd do not arise through inputs from area MT.
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Project description:Multisensory integration helps the brain build reliable models of the world and resolve ambiguities. Visual interactions with sound and touch are well established but vestibular influences on vision are less well studied. Here, we test the vestibular influence on vision using horizontally opposed motions presented one to each eye so that visual perception is unstable and alternates irregularly. Passive, whole-body rotations in the yaw plane stabilized visual alternations, with perceived direction oscillating congruently with rotation (leftward motion during leftward rotation, and vice versa). This demonstrates a purely vestibular signal can resolve ambiguous visual motion and determine visual perception. Active self-rotation following the same sinusoidal profile also entrained vision to the rotation cycle - more strongly and with a lesser time lag, likely because of efference copy and predictive internal models. Both experiments show that visual ambiguity provides an effective paradigm to reveal how vestibular and motor inputs can shape visual perception.
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Project description:Detection of the state of self-motion, such as the instantaneous heading direction, the traveled trajectory and traveled distance or time, is critical for efficient spatial navigation. Numerous psychophysical studies have indicated that the vestibular system, originating from the otolith and semicircular canals in our inner ears, provides robust signals for different aspects of self-motion perception. In addition, vestibular signals interact with other sensory signals such as visual optic flow to facilitate natural navigation. These behavioral results are consistent with recent findings in neurophysiological studies. In particular, vestibular activity in response to the translation or rotation of the head/body in darkness is revealed in a growing number of cortical regions, many of which are also sensitive to visual motion stimuli. The temporal dynamics of the vestibular activity in the central nervous system can vary widely, ranging from acceleration-dominant to velocity-dominant. Different temporal dynamic signals may be decoded by higher level areas for different functions. For example, the acceleration signals during the translation of body in the horizontal plane may be used by the brain to estimate the heading directions. Although translation and rotation signals arise from independent peripheral organs, that is, otolith and canals, respectively, they frequently converge onto single neurons in the central nervous system including both the brainstem and the cerebral cortex. The convergent neurons typically exhibit stronger responses during a combined curved motion trajectory which may serve as the neural correlate for complex path perception. During spatial navigation, traveled distance or time may be encoded by different population of neurons in multiple regions including hippocampal-entorhinal system, posterior parietal cortex, or frontal cortex.
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Project description:During the course of daily activity, our level of engagement with the world varies on a moment-to-moment basis. Although these fluctuations in vigilance have critical consequences for our thoughts and actions, almost nothing is known about the neuronal substrates governing such dynamic variations in task engagement. We investigated the hypothesis that the posterior cingulate cortex (CGp), a region linked to default-mode processing by hemodynamic and metabolic measures, controls such variations. We recorded the activity of single neurons in CGp in 2 macaque monkeys performing simple tasks in which their behavior varied from vigilant to inattentive. We found that firing rates were reliably suppressed during task performance and returned to a higher resting baseline between trials. Importantly, higher firing rates predicted errors and slow behavioral responses, and were also observed during cued rest periods when monkeys were temporarily liberated from exteroceptive vigilance. These patterns of activity were not observed in the lateral intraparietal area, an area linked to the frontoparietal attention network. Our findings provide physiological confirmation that CGp mediates exteroceptive vigilance and are consistent with the idea that CGp is part of the "default network" of brain areas associated with control of task engagement.
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Project description:Sixty vestibular nuclei neurons antidromically activated by electrical stimulation of the ventroposterior thalamus were recorded in two alert squirrel monkeys. The majority of these neurons were monosynaptically activated by vestibular nerve electrical stimulation. Forty-seven neurons responded to animal rotations around the earth-vertical axis; 16 of them also responded to translations in the horizontal plane. The mean sensitivity to 0.5-Hz rotations of 80 degrees /s velocity was 0.40 +/- 0.31 spikes.s(-1).deg(-1).s(-1). Rotational responses were in phase with stimulus velocity. Sensitivities to 0.5-Hz translations of 0.1 g acceleration varied from 92.2 to 359 spikes.s(-1).g(-1) and response phases varied from 10.1 degrees lead to -98 degrees lag. The firing behavior in 28 neurons was studied during rotation of the whole animal, of the trunk, and voluntary and involuntary rotations of the head. Two classes of vestibulothalamic neurons were distinguished. One class of neurons generated signals related to movement of the head that were similar either when the head and trunk move together or when the head moves on the stationary trunk. A fraction of these neurons fired during involuntary head movements only. A second class of neurons generated signals related to movement of the trunk. They responded when the trunk moved alone or simultaneously with the head, but did not respond to head rotations while the trunk was stationary.
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Project description:There is accumulating evidence that the brain's neural coding strategies are constrained by natural stimulus statistics. Here we investigated the statistics of the time varying envelope (i.e. a second-order stimulus attribute that is related to variance) of rotational and translational self-motion signals experienced by human subjects during everyday activities. We found that envelopes can reach large values across all six motion dimensions (~450 deg/s for rotations and ~4 G for translations). Unlike results obtained in other sensory modalities, the spectral power of envelope signals decreased slowly for low (< 2 Hz) and more sharply for high (>2 Hz) temporal frequencies and thus was not well-fit by a power law. We next compared the spectral properties of envelope signals resulting from active and passive self-motion, as well as those resulting from signals obtained when the subject is absent (i.e. external stimuli). Our data suggest that different mechanisms underlie deviation from scale invariance in rotational and translational self-motion envelopes. Specifically, active self-motion and filtering by the human body cause deviation from scale invariance primarily for translational and rotational envelope signals, respectively. Finally, we used well-established models in order to predict the responses of peripheral vestibular afferents to natural envelope stimuli. We found that irregular afferents responded more strongly to envelopes than their regular counterparts. Our findings have important consequences for understanding the coding strategies used by the vestibular system to process natural second-order self-motion signals.
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Project description:Precise heading estimate requires integration of visual optic flow and vestibular inertial motion originating from distinct spatial coordinates (eye- and head-centered, respectively). To explore whether the two heading signals may share a common reference frame along the hierarchy of cortical stages, we explored two multisensory areas in macaques: the smooth pursuit area of the frontal eye field (FEFsem) closer to the motor side, and the dorsal portion of medial superior temporal area (MSTd) closer to the sensory side. In both areas, vestibular signals are head-centered, whereas visual signals are mainly eye-centered. However, visual signals in FEFsem are more shifted towards the head coordinate compared to MSTd. These results are robust being largely independent on: (1) smooth pursuit eye movement, (2) motion parallax cue, and (3) behavioral context for active heading estimation, indicating that the visual and vestibular heading signals may be represented in distinct spatial coordinate in sensory cortices.
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Project description:Motion processing regions apart from V5+/MT+ are still relatively poorly understood. Here, we used functional magnetic resonance imaging to perform a detailed functional analysis of the recently described cingulate sulcus visual area (CSv) in the dorsal posterior cingulate cortex. We used distinct types of visual motion stimuli to compare CSv with V5/MT and MST, including a visual pursuit paradigm. Both V5/MT and MST preferred 3D flow over 2D planar motion, responded less yet substantially to random motion, had a strong preference for contralateral versus ipsilateral stimulation, and responded nearly equally to contralateral and to full-field stimuli. In contrast, CSv had a pronounced preference to 2D planar motion over 3D flow, did not respond to random motion, had a weak and nonsignificant lateralization that was significantly smaller than that of MST, and strongly preferred full-field over contralateral stimuli. In addition, CSv had a better capability to integrate eye movements with retinal motion compared with V5/MT and MST. CSv thus differs from V5+/MT+ by its unique preference to full-field, coherent, and planar motion cues. These results place CSv in a good position to process visual cues related to self-induced motion, in particular those associated to eye or lateral head movements.
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