Gravity orientation tuning in macaque anterior thalamus

Laurens, Jean; Kim, Byoung-Hoon; Dickman, J. David; Angelaki, Dora E.

doi:10.1038/nn.4423

Cited by 73 publications

(86 citation statements)

References 15 publications

(19 reference statements)

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“…It is also possible that vertical information might be more evident in the thalamus if we studied navigation in a real environment instead of a virtual environment. Recently, Laurens, Kim, Dickman, and Angelaki () found cells tuned to gravity (vertical tilt) in the macaque anterior thalamus using a rotatable apparatus (Laurens et al, ). Even though the pre‐scan immersive training and the optic flow during our scanning experiment could have enhanced the HD signal, physical head tilt and acceleration was missing in our fMRI study.…”

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Encoding of 3D head direction information in the human brain

Kim

Maguire

2018

Hippocampus

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Head direction cells are critical for navigation because they convey information about which direction an animal is facing within an environment. To date, most studies on head direction encoding have been conducted on a horizontal two‐dimensional (2D) plane, and little is known about how three‐dimensional (3D) direction information is encoded in the brain despite humans and other animals living in a 3D world. Here, we investigated head direction encoding in the human brain while participants moved within a virtual 3D “spaceship” environment. Movement was not constrained to planes and instead participants could move along all three axes in volumetric space as if in zero gravity. Using functional magnetic resonance imaging (fMRI) multivoxel pattern similarity analysis, we found evidence that the thalamus, particularly the anterior portion, and the subiculum encoded the horizontal component of 3D head direction (azimuth). In contrast, the retrosplenial cortex was significantly more sensitive to the vertical direction (pitch) than to the azimuth. Our results also indicated that vertical direction information in the retrosplenial cortex was significantly correlated with behavioral performance during a direction judgment task. Our findings represent the first evidence showing that the “classic” head direction system that has been identified on a horizontal 2D plane also seems to encode vertical and horizontal heading in 3D space in the human brain.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Encoding of 3D head direction information in the human brain

Kim

Maguire

2018

Hippocampus

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“…The fact that directional tuning was relatively normal in the initial trial suggests that otolith signals are not crucial for the directional tuning of head direction cells but, instead, contribute to the maintenance of directional tuning across changes in vertical orientation. However, it is also possible that the activity of rodent head direction cells is directly influenced by gravity, given the recent discovery of gravity-sensitive neurons in the primate anterior thalamus [46]. Further, it is important to consider the role of linear movements in path integration, given that the acceleration phase of linear movements would be detected by the otolith organs.…”

Section: Discussionmentioning

confidence: 99%

Otolith dysfunction alters exploratory movement in mice

Blankenship

Cherep

Donaldson

et al. 2017

Behavioural Brain Research

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The organization of rodent exploratory behavior appears to depend on self-movement cue processing. As of yet, however, no studies have directly examined the vestibular system’s contribution to the organization of exploratory movement. The current study sequentially segmented open field behavior into progressions and stops in order to characterize differences in movement organization between control and otoconia-deficient tilted mice under conditions with and without access to visual cues. Under completely dark conditions, tilted mice exhibited similar distance traveled and stop times overall, but had significantly more circuitous progressions, larger changes in heading between progressions, and less stable clustering of home bases, relative to control mice. In light conditions, control and tilted mice were similar on all measures except for the change in heading between progressions. This pattern of results is consistent with otoconia-deficient tilted mice using visual cues to compensate for impaired self-movement cue processing. This work provides the first empirical evidence that signals from the otolithic organs mediate the organization of exploratory behavior, based on a novel assessment of spatial orientation.

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“…Also, SVV tasks engage temporo-parietal-insular cortices (Fiori et al 2015;Kheradmand & Winnick 2017), although temporal and spatial processing of gravity may not necessarily co-localize in the same regions (Maffei et al 2016). J Physiol 597.7 Detailed electrophysiological studies in monkeys have shown that neurons carrying signals of head and body orientation relative to gravity, independent of visual landmarks, can be found in several brain regions, including the brainstem, cerebellum, thalamus, temporal, parietal and insular cortices (Angelaki et al 2004;Chen et al 2011;Laurens et al 2013Laurens et al , 2016. Several of these neurons use internal models of physics to disentangle gravitoinertial cues (Angelaki et al 2004) or visual motion cues for target interception (Cerminara et al 2009;Streng et al 2018).…”

Section: Putative Neural Substratesmentioning

confidence: 99%

Body orientation contributes to modelling the effects of gravity for target interception in humans

Scaleia

Lacquaniti

Zago

2019

The Journal of Physiology

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Key points It is known that interception of targets accelerated by gravity involves internal models coupled with visual signals. Non‐visual signals related to head and body orientation relative to gravity may also contribute, although their role is poorly understood. In a novel experiment, we asked pitched observers to hit a virtual target approaching with an acceleration that was either coherent or incoherent with their pitch‐tilt. Initially, the timing errors were large and independent of the coherence between target acceleration and observer's pitch. With practice, however, the timing errors became substantially smaller in the coherent conditions. The results show that information about head and body orientation can contribute to modelling the effects of gravity on a moving target. Orientation cues from vestibular and somatosensory signals might be integrated with visual signals in the vestibular cortex, where the internal model of gravity is assumed to be encoded. Abstract Interception of moving targets relies on visual signals and internal models. Less is known about the additional contribution of non‐visual cues about head and body orientation relative to gravity. We took advantage of Galileo's law of motion along an incline to demonstrate the effects of vestibular and somatosensory cues about head and body orientation on interception timing. Participants were asked to hit a ball rolling in a gutter towards the eyes, resulting in image expansion. The scene was presented in a head‐mounted display, without any visual information about gravity direction. In separate blocks of trials participants were pitched backwards by 20° or 60°, whereas ball acceleration was randomized across trials so as to be compatible with rolling down a slope of 20° or 60°. Initially, the timing errors were large, independently of the coherence between ball acceleration and pitch angle, consistent with responses based exclusively on visual information because visual stimuli were identical at both tilts. At the end of the experiment, however, the timing errors were systematically smaller in the coherent conditions than the incoherent ones. Moreover, the responses were significantly (P = 0.007) earlier when participants were pitched by 60° than when they were pitched by 20°. Therefore, practice with the task led to incorporation of information about head and body orientation relative to gravity for response timing. Instead, posture did not affect response timing in a control experiment in which participants hit a static target in synchrony with the last of a predictable series of stationary audiovisual stimuli.

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Gravity orientation tuning in macaque anterior thalamus

Cited by 73 publications

References 15 publications

Encoding of 3D head direction information in the human brain

Encoding of 3D head direction information in the human brain

Otolith dysfunction alters exploratory movement in mice

Body orientation contributes to modelling the effects of gravity for target interception in humans

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