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Computation of linear acceleration through an internal model in the macaque cerebellum.

Laurens J, Meng H, Angelaki DE - Nat. Neurosci. (2013)

Bottom Line: Although the cerebellum has been proposed as a candidate for implementation of internal models, concrete evidence from neural responses is lacking.Using unnatural motion stimuli, which induce incorrect self-motion perception and eye movements, we explored the neural correlates of an internal model that has been proposed to compensate for Einstein's equivalence principle and generate neural estimates of linear acceleration and gravity.We found that caudal cerebellar vermis Purkinje cells and cerebellar nuclei neurons selective for actual linear acceleration also encoded erroneous linear acceleration, as would be expected from the internal model hypothesis, even when no actual linear acceleration occurred.

View Article: PubMed Central - PubMed

Affiliation: Department of Otolaryngology, Washington University School of Medicine, St. Louis, Missouri, USA.

ABSTRACT
A combination of theory and behavioral findings support a role for internal models in the resolution of sensory ambiguities and sensorimotor processing. Although the cerebellum has been proposed as a candidate for implementation of internal models, concrete evidence from neural responses is lacking. Using unnatural motion stimuli, which induce incorrect self-motion perception and eye movements, we explored the neural correlates of an internal model that has been proposed to compensate for Einstein's equivalence principle and generate neural estimates of linear acceleration and gravity. We found that caudal cerebellar vermis Purkinje cells and cerebellar nuclei neurons selective for actual linear acceleration also encoded erroneous linear acceleration, as would be expected from the internal model hypothesis, even when no actual linear acceleration occurred. These findings provide strong evidence that the cerebellum might be involved in the implementation of internal models that mimic physical principles to interpret sensory signals, as previously hypothesized.

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Schematic illustrating the Tilt-While-Rotating (TWR) stimulus(a) Constant velocity earth-vertical axis rotation (EVAR, red arrow), superimposed on nose-up and nose-down pitch tilt. The yaw and roll axes of the head are represented by black arrows. (b)–(d) Representation of the induced roll rotation, the resulting head tilt estimate and the erroneous translation signal induced during steady-state TWR. The gravito-inertial acceleration (GIA) sensed by the otolith organs is represented by a pendulum. Only in the presence of a linear acceleration (translation signal, red arrow), such as shown in Fig. 1d, a pendulum would remain aligned with the head/body vertical axis while tilted.
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Figure 1: Schematic illustrating the Tilt-While-Rotating (TWR) stimulus(a) Constant velocity earth-vertical axis rotation (EVAR, red arrow), superimposed on nose-up and nose-down pitch tilt. The yaw and roll axes of the head are represented by black arrows. (b)–(d) Representation of the induced roll rotation, the resulting head tilt estimate and the erroneous translation signal induced during steady-state TWR. The gravito-inertial acceleration (GIA) sensed by the otolith organs is represented by a pendulum. Only in the presence of a linear acceleration (translation signal, red arrow), such as shown in Fig. 1d, a pendulum would remain aligned with the head/body vertical axis while tilted.

Mentions: Tilt while rotating (TWR, also known as ‘vestibular cross-coupling’ or ‘vestibular Coriolis effect’) is a disorienting and nauseating stimulus in humans commonly used in motion sickness training32–36. It consists of tilting the head while rotating continuously around an earth-vertical axis (Fig. 1a; Supplementary Movies 1a and 2a), similar as tilting the head while riding a merry-go-round. Why this stimulus causes dizziness and disorientation is outlined in Fig. 1 (see also Fig. 2 and Modeling section in Supplementary Materials). During continuous rotation, the output of the semicircular canals is attenuated over time. As a result, when the head tilts in pitch during steady-state, an erroneous roll rotation signal is generated in the canals (Fig. 1b and Supplementary Movie 1b,c). According to theory, this roll canal signal is integrated by the internal model to create an ‘erroneous’ roll tilt estimate (as if the head is tilted ear-down; Fig. 1c). Since the head is in fact upright, the output of the internal model of gravity is in conflict with the otolith cues, which signal that GIA is aligned with the head-vertical axis (Fig. 1b–d). The only inference consistent with these signals is that the head is simultaneously translating (Fig. 1d and Supplementary Movie 2b).


Computation of linear acceleration through an internal model in the macaque cerebellum.

Laurens J, Meng H, Angelaki DE - Nat. Neurosci. (2013)

Schematic illustrating the Tilt-While-Rotating (TWR) stimulus(a) Constant velocity earth-vertical axis rotation (EVAR, red arrow), superimposed on nose-up and nose-down pitch tilt. The yaw and roll axes of the head are represented by black arrows. (b)–(d) Representation of the induced roll rotation, the resulting head tilt estimate and the erroneous translation signal induced during steady-state TWR. The gravito-inertial acceleration (GIA) sensed by the otolith organs is represented by a pendulum. Only in the presence of a linear acceleration (translation signal, red arrow), such as shown in Fig. 1d, a pendulum would remain aligned with the head/body vertical axis while tilted.
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Related In: Results  -  Collection

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Figure 1: Schematic illustrating the Tilt-While-Rotating (TWR) stimulus(a) Constant velocity earth-vertical axis rotation (EVAR, red arrow), superimposed on nose-up and nose-down pitch tilt. The yaw and roll axes of the head are represented by black arrows. (b)–(d) Representation of the induced roll rotation, the resulting head tilt estimate and the erroneous translation signal induced during steady-state TWR. The gravito-inertial acceleration (GIA) sensed by the otolith organs is represented by a pendulum. Only in the presence of a linear acceleration (translation signal, red arrow), such as shown in Fig. 1d, a pendulum would remain aligned with the head/body vertical axis while tilted.
Mentions: Tilt while rotating (TWR, also known as ‘vestibular cross-coupling’ or ‘vestibular Coriolis effect’) is a disorienting and nauseating stimulus in humans commonly used in motion sickness training32–36. It consists of tilting the head while rotating continuously around an earth-vertical axis (Fig. 1a; Supplementary Movies 1a and 2a), similar as tilting the head while riding a merry-go-round. Why this stimulus causes dizziness and disorientation is outlined in Fig. 1 (see also Fig. 2 and Modeling section in Supplementary Materials). During continuous rotation, the output of the semicircular canals is attenuated over time. As a result, when the head tilts in pitch during steady-state, an erroneous roll rotation signal is generated in the canals (Fig. 1b and Supplementary Movie 1b,c). According to theory, this roll canal signal is integrated by the internal model to create an ‘erroneous’ roll tilt estimate (as if the head is tilted ear-down; Fig. 1c). Since the head is in fact upright, the output of the internal model of gravity is in conflict with the otolith cues, which signal that GIA is aligned with the head-vertical axis (Fig. 1b–d). The only inference consistent with these signals is that the head is simultaneously translating (Fig. 1d and Supplementary Movie 2b).

Bottom Line: Although the cerebellum has been proposed as a candidate for implementation of internal models, concrete evidence from neural responses is lacking.Using unnatural motion stimuli, which induce incorrect self-motion perception and eye movements, we explored the neural correlates of an internal model that has been proposed to compensate for Einstein's equivalence principle and generate neural estimates of linear acceleration and gravity.We found that caudal cerebellar vermis Purkinje cells and cerebellar nuclei neurons selective for actual linear acceleration also encoded erroneous linear acceleration, as would be expected from the internal model hypothesis, even when no actual linear acceleration occurred.

View Article: PubMed Central - PubMed

Affiliation: Department of Otolaryngology, Washington University School of Medicine, St. Louis, Missouri, USA.

ABSTRACT
A combination of theory and behavioral findings support a role for internal models in the resolution of sensory ambiguities and sensorimotor processing. Although the cerebellum has been proposed as a candidate for implementation of internal models, concrete evidence from neural responses is lacking. Using unnatural motion stimuli, which induce incorrect self-motion perception and eye movements, we explored the neural correlates of an internal model that has been proposed to compensate for Einstein's equivalence principle and generate neural estimates of linear acceleration and gravity. We found that caudal cerebellar vermis Purkinje cells and cerebellar nuclei neurons selective for actual linear acceleration also encoded erroneous linear acceleration, as would be expected from the internal model hypothesis, even when no actual linear acceleration occurred. These findings provide strong evidence that the cerebellum might be involved in the implementation of internal models that mimic physical principles to interpret sensory signals, as previously hypothesized.

Show MeSH
Related in: MedlinePlus