Frequency-Dependent Spatiotemporal Tuning Properties of Non–Eye Movement Related Vestibular Neurons to Three-Dimensional Translations in Squirrel Monkeys

Chen-Huang, Chiju; Peterson, B. W.

doi:10.1152/jn.00904.2009

Cited by 6 publications

(15 citation statements)

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“…First, afferents from a single otolith organ differ in both spatial and temporal response properties (Fernández and Goldberg, 1976a, 1976b, 1976c; Angelaki and Dickman, 2000; Yu et al, 2012; Jamali et al, 2013) and extensive convergence in the vestibular nuclei (Kushiro et al, 2000; Straka et al, 2002; Uchino et al, 2001; Uchino and Kushiro, 2011) creates complex spatio-temporal convergence properties (Angelaki et al, 1992; Bush et al, 1993; Angelaki and Dickman, 2000; Dickman and Angelaki, 2002; Chen-Huang and Peterson, 2006, 2010). …”

Section: Discussionmentioning

confidence: 99%

“…It took several more years until some experimental evidence for spatio-temporal convergence properties was provided for neurons in the primate VN (Angelaki and Dickman, 2000; Chen-Huang and Peterson, 2006, 2010) and CN (Shaikh et al, 2005). However, to our knowledge, all previously published studies of responses of VN/CN neurons to translation used sinusoidal stimuli.…”

Section: Discussionmentioning

confidence: 99%

“…The traditional approach of testing sinusoidal responses at different frequencies to distinguish velocity from jerk contributions using linear systems analyses is complicated by the presence of non-minimum phase properties, thus making system identification challenging (Angelaki and Dickman, 2000; Dickman and Angelaki, 2002; Shaikh et al, 2005). Furthermore, if indeed response dynamics vary with stimulus direction, a complete characterization of the spatio-temporal properties requires testing cells at multiple frequencies and multiple directions in 3D (Chen-Huang and Peterson, 2006, 2010). Third, non-linearities in spatio-temporal tuning, as reported here (see also Chen et al, 2011c; Massot et al, 2012) can violate the assumptions of traditional linear systems analysis, thus rendering previous conclusions based on steady-state frequency analysis problematic.…”

Section: Discussionmentioning

confidence: 99%

“…Neural response properties in the vestibular nuclei (VN), which receive the bulk of vestibular afferent projections outside the cerebellum (Barmack, 2003; Newlands and Perachio, 2003; Angelaki and Cullen, 2008), are different. It has been proposed that spatio-temporal convergence of otolith afferents onto central VN cells results in complex, non-cosine-tuned properties, where spatial and temporal coding might not always be multiplicatively separable (Angelaki, 1991, 1992b; Angelaki et al, 1992; Angelaki, 1993; Angelaki et al, 1993; Bush et al, 1993; Angelaki and Dickman, 2000; Dickman and Angelaki, 2002; Chen-Huang and Peterson, 2006, 2010). Some studies have supported this prediction in the vestibular brainstem (Angelaki et al, 1993; Bush et al, 1993; Angelaki and Dickman, 2000; Chen-Huang and Peterson, 2006, 2010), but direct comparisons with cortical responses (e.g., Chen et al, 2011c) have never been made.…”

Section: Introductionmentioning

confidence: 99%

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Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex

Laurens

Liu

et al. 2017

eLife

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Sensory signals undergo substantial recoding when neural activity is relayed from sensors through pre-thalamic and thalamic nuclei to cortex. To explore how temporal dynamics and directional tuning are sculpted in hierarchical vestibular circuits, we compared responses of macaque otolith afferents with neurons in the vestibular and cerebellar nuclei, as well as five cortical areas, to identical three-dimensional translational motion. We demonstrate a remarkable spatio-temporal transformation: otolith afferents carry spatially aligned cosine-tuned translational acceleration and jerk signals. In contrast, brainstem and cerebellar neurons exhibit non-linear, mixed selectivity for translational velocity, acceleration, jerk and position. Furthermore, these components often show dissimilar spatial tuning. Moderate further transformation of translation signals occurs in the cortex, such that similar spatio-temporal properties are found in multiple cortical areas. These results suggest that the first synapse represents a key processing element in vestibular pathways, robustly shaping how self-motion is represented in central vestibular circuits and cortical areas.DOI: http://dx.doi.org/10.7554/eLife.20787.001

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex

Laurens

Liu

et al. 2017

eLife

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“…First, how does the heading sensitivity of otolith afferents compare with central vestibular neurons? Are central vestibular neurons more sensitive than afferents because they have greater average modulation amplitudes than afferents (16)(17)(18)(19)(20)(21)(22)(23), or do changes in response variability counteract these differences in response gain? Second, do otolith afferents show choice-related activity, and how do CPs of afferents compare with CPs measured in central neurons and cortical areas?…”

Section: Significancementioning

confidence: 99%

Neuronal thresholds and choice-related activity of otolith afferent fibers during heading perception

Dickman

DeAngelis

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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How activity of sensory neurons leads to perceptual decisions remains a challenge to understand. Correlations between choices and single neuron firing rates have been found early in vestibular processing, in the brainstem and cerebellum. To investigate the origins of choice-related activity, we have recorded from otolith afferent fibers while animals performed a fine heading discrimination task. We find that afferent fibers have similar discrimination thresholds as central cells, and the most sensitive fibers have thresholds that are only twofold or threefold greater than perceptual thresholds. Unlike brainstem and cerebellar nuclei neurons, spike counts from afferent fibers do not exhibit trial-by-trial correlations with perceptual decisions. This finding may reflect the fact that otolith afferent responses are poorly suited for driving heading perception because they fail to discriminate self-motion from changes in orientation relative to gravity. Alternatively, if choice probabilities reflect top-down inference signals, they are not relayed to the vestibular periphery.neuronal threshold | choice probability | psychophysical threshold | otolith afferent | heading discrimination T he neural basis of perception holds a long-standing fascination for neuroscientists. How do the properties of single neurons and populations of neurons relate to, and account for, sensory perception? In all sensory systems, information about the world is first translated into neural activity by peripheral receptor neurons, and then transformed by multiple stages of subcortical and cortical processing into a perceptual decision. How and where does perception emerge from multiple neural representations that appear to be at least partially redundant? These questions have been addressed often in sensory and multisensory cortex (e.g., in refs. 1-3 for vestibular perception), but much less is known about how the activity of sensory afferents relates to perceptual sensitivity and perceptual decisions.One way to assess a potential role of sensory neurons in a perceptual task is to compare neuronal and perceptual sensitivity, measured simultaneously in the same subject (4). Although this comparison has been done many times for cortical neurons (1, 5-7), little is known about how the sensitivity of peripheral afferents compares with behavior apart from microneurography studies of tactile afferents in humans (8, 9). To our knowledge, the present study provides the first direct comparison of afferent neuronal sensitivity and perceptual sensitivity, measured simultaneously in experimental animals. Results of such comparisons have important implications for understanding how population encoding and decoding may constrain and shape the information that guides behavior.Another way that neuroscientists have explored the functional links between sensory neurons and perception is by measuring the trial-by-trial correlations between neural activity and perceptual decisions, which are typically quantified as "choice probabilities" (CPs) (10). The "bottom-...

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Diversity of vestibular nuclei neurons targeted by cerebellar nodulus inhibition

Hui

Blazquez

Dickman

et al. 2013

The Journal of Physiology

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Key points• Electrical stimulation of the cerebellar nodulus and ventral uvula decreases the time constant of the horizontal vestibulo-ocular reflex during yaw rotation.• Unlike the flocculus and ventral paraflocculus which target a particular cell group, nodulus/ventral uvula inhibition targets a large diversity of cell types in the vestibular nuclei.• Twenty per cent of nodulus/ventral uvula-target neurons were sensitive to both vestibular stimuli and eye movements, whereas the majority was only sensitive to vestibular stimuli.• Most nodulus/ventral uvula-target cells responded to both rotation and translation and only approximately half discriminated translational and gravitational accelerations.• Projections of the nodulus/ventral uvula to both eye movement-and non-eye movementsensitive vestibular nuclei neurons suggest a role in both eye movement generation and vestibulo-spinal or thalamo-cortical systems.Abstract A functional role of the cerebellar nodulus and ventral uvula (lobules X and IXc,d of the vermis) for vestibular processing has been strongly suggested by direct reciprocal connections with the vestibular nuclei, as well as direct vestibular afferent inputs as mossy fibres. Here we have explored the types of neurons in the macaque vestibular nuclei targeted by nodulus/ventral uvula inhibition using orthodromic identification from the caudal vermis. We found that all nodulus-target neurons are tuned to vestibular stimuli, and most are insensitive to eye movements. Such non-eye-movement neurons are thought to project to vestibulo-spinal and/or thalamo-cortical pathways. Less than 20% of nodulus-target neurons were sensitive to eye movements, suggesting that the caudal vermis can also directly influence vestibulo-ocular pathways. In general, response properties of nodulus-target neurons were diverse, spanning the whole continuum previously described in the vestibular nuclei. Most nodulus-target cells responded to both rotation and translation stimuli and only a few were selectively tuned to translation motion only. Other neurons were sensitive to net linear acceleration, similar to otolith afferents. These results demonstrate that, unlike the flocculus and ventral paraflocculus which target a particular cell group, nodulus/ventral uvula inhibition targets a large diversity of cell types in the vestibular nuclei, consistent with a broad functional significance contributing to vestibulo-ocular, vestibulo-thalamic and vestibulo-spinal pathways.

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Frequency-Dependent Spatiotemporal Tuning Properties of Non–Eye Movement Related Vestibular Neurons to Three-Dimensional Translations in Squirrel Monkeys

Cited by 6 publications

References 75 publications

Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex

Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex

Neuronal thresholds and choice-related activity of otolith afferent fibers during heading perception

Diversity of vestibular nuclei neurons targeted by cerebellar nodulus inhibition

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