Unreferenced spatial localization under monocular and dichoptic viewing conditions

Knowledge of eye position in the brain is critical for localization of objects in space. To investigate the accuracy and precision of eye position feedback in an unreferenced environment, subjects with normal ocular alignment attempted to localize briefly presented targets during monocular and dichoptic viewing. In the task, subjects’ used a computer mouse to position a response disk at the remembered location of the target. Under dichoptic viewing (with red (right eye)–green (left eye) glasses), target and response disks were presented to the same or alternate eyes, leading to four conditions [green target–green response cue (LL), green–red (LR), red–green (RL), and red–red (RR)]. Time interval between target and response disks was varied and localization errors were the difference between the estimated and real positions of the target disk. Overall, the precision of spatial localization (variance across trials) became progressively worse with time. Under dichoptic viewing, localization errors were significantly greater for alternate-eye trials as compared to same-eye trials and were correlated to the average phoria of each subject. Our data suggests that during binocular dissociation, spatial localization may be achieved by combining a reliable versional efference copy signal with a proprioceptive signal that is unreliable perhaps because it is from the wrong eye or is too noisy.

Age-related changes in leg proprioception: implications for postural control

In addition to being a prerequisite for many activities of daily living, the ability to maintain steady upright standing is a relevant model to study sensorimotor integrative function. Upright standing requires managing multimodal sensory inputs to produce finely tuned motor output that can be adjusted to accommodate changes in standing conditions and environment. The sensory information used for postural control mainly arises from the vestibular system of the inner ear, vision, and proprioception. Proprioception (sense of body position and movement) encompasses signals from mechanoreceptors (proprioceptors) located in muscles, tendons, and joint capsules. There is general agreement that proprioception signals from leg muscles provide the primary source of information for postural control. This is because of their exquisite sensitivity to detect body sway during unperturbed upright standing that mainly results from variations in leg muscle length induced by rotations around the ankle joint. However, aging is associated with alterations of muscle spindles and their neural pathways, which induce a decrease in the sensitivity, acuity, and integration of the proprioceptive signal. These alterations promote changes in postural control that reduce its efficiency and thereby may have deleterious consequences for the functional independence of an individual. This narrative review provides an overview of how aging alters the proprioceptive signal from the legs and presents compelling evidence that these changes modify the neural control of upright standing.

Coding of whisker motion across the mouse face

Haptic perception synthesizes touch with proprioception, the sense of body position. Humans and mice alike experience rich active touch of the face. Because most facial muscles lack proprioceptor endings, the sensory basis of facial proprioception remains unsolved. Facial proprioception may instead rely on mechanoreceptors that encode both touch and self-motion. In rodents, whisker mechanoreceptors provide a signal that informs the brain about whisker position. Whisking involves coordinated orofacial movements, so mechanoreceptors innervating facial regions other than whiskers could also provide information about whisking. To define all sources of sensory information about whisking available to the brain, we recorded spikes from mechanoreceptors innervating diverse parts of the face. Whisker motion was encoded best by whisker mechanoreceptors, but also by those innervating whisker pad hairy skin and supraorbital vibrissae. Redundant self-motion responses may provide the brain with a stable proprioceptive signal despite mechanical perturbations during active touch.

Coding of whisker motion across the mouse face

Haptic perception synthesizes touch with proprioception, or sense of body position. Humans and mice alike experience rich active touch of the face. Because most facial muscles lack proprioceptor endings, the sensory basis of facial proprioception remains unsolved. Facial proprioception may instead rely on mechanoreceptors that encode both touch and self-motion. In rodents, whisker mechanoreceptors provide a signal that informs the brain about whisker position. Whisking involves coordinated orofacial movements, so mechanoreceptors innervating facial regions other than whiskers could also provide information about whisking. To define all sources of sensory information about whisking available to the brain, we recorded spikes from mechanoreceptors innervating diverse parts of the face. Whisker motion was encoded best by whisker mechanoreceptors, but also by those innervating whisker pad hairy skin and supraorbital vibrissae. Redundant self-motion responses may provide the brain with a stable proprioceptive signal despite mechanical perturbations such as whisker growth and active touch.

The time course of the tonic oculomotor proprioceptive signal in area 3a of somatosensory cortex

A proprioceptive representation of eye position exists in area 3a of primate somatosensory cortex (Wang X, Zhang M, Cohen IS, Goldberg ME. Nat Neurosci 10: 640–646, 2007). This eye position signal is consistent with a fusimotor response (Taylor A, Durbaba R, Ellaway PH, Rawlinson S. J Physiol 571: 711–723, 2006) and has two components during a visually guided saccade task: a short-latency phasic response followed by a tonic response. While the early phasic response can be excitatory or inhibitory, it does not accurately reflect the eye's orbital position. The late tonic response appears to carry the proprioceptive eye position signal, but it is not clear when this component emerges and whether the onset of this signal is reliable. To test the temporal dynamics of the tonic proprioceptive signal, we used an oculomotor smooth pursuit task in which saccadic eye movements and phasic proprioceptive responses are suppressed. Our results show that the tonic proprioceptive eye position signal consistently lags the actual eye position in the orbit by ∼60 ms under a variety of eye movement conditions. To confirm the proprioceptive nature of this signal, we also studied the responses of neurons in a vestibuloocular reflex (VOR) task in which the direction of gaze was held constant; response profiles and delay times were similar in this task, suggesting that this signal does not represent angle of gaze and does not receive visual or vestibular inputs. The length of the delay suggests that the proprioceptive eye position signal is unlikely to be used for online visual processing for action, although it could be used to calibrate an efference copy signal.

Decreased Visual Attention Further from the Perceived Direction of Gaze for Equidistant Retinal Targets

The oculomotor and spatial attention systems are interconnected. Whereas a link between motor commands and spatial shifts in visual attention is demonstrated, it is still unknown whether the recently discovered proprioceptive signal in somatosensory cortex impacts on visual attention, too. This study investigated whether visual targets near the perceived direction of gaze are detected more accurately than targets further away, despite the equal eccentricity of their retinal projections. We dissociated real and perceived eye position using left somatosensory repetitive transcranial magnetic stimulation (rTMS), which decreases cortical processing of eye muscle proprioceptive inflow and produces an underestimation of the rotation of the right eye. Participants detected near-threshold visual targets presented in the left or right visual hemifield at equal distance from fixation. We have previously shown that when the right eye is rotated to the left of the parasagittal plane, TMS produces an underestimation of this rotation, shifting perceived eye position to the right. Here we found that, in this condition, TMS also decreased target detection in the left visual hemifield and increased it in the right. This effect depended on the direction of rotation of the right eye. When the right eye was rotated rightward and TMS, we assume, shifted perceived gaze direction in opposite direction, leftward, visual accuracy decreased now in the right hemifield. We suggest that the proprioceptive eye position signal modulates the spatial distribution of visual processing resources, producing “pseudo-neglect” for objects located far relative to near the perceived direction of gaze.

Influence of Bilateral Vestibular Loss on Spinal Stabilization in Humans

The control of upper body (UB) orientation relative to the pelvis in the frontal plane was characterized in bilateral vestibular loss subjects (BVLs) and compared with healthy control subjects (Cs). UB responses to external perturbations were evoked using continuous pelvis tilts (eyes open and eyes closed) at various amplitudes. Lateral sway of the lower body was prevented on all tests. UB sway was summarized using root-mean-square measures and dynamic behavior was characterized using frequency response functions (FRFs) from 0.023 to 10.3 Hz. Both subject groups had similar FRF variations as a function of stimulus frequency and were relatively unaffected by visual availability, indicating that visual orientation cues contributed very little to UB control. BVLs had larger UB sway at frequencies below ∼1 Hz compared with Cs. A feedback model of UB orientation control was used to identify sensory contributions to spinal stability and differences between subject groups. The model-based interpretation of experimental results indicated that a phasic proprioceptive signal encoding the angular velocity of UB relative to lower body motion was a major contributor to overall system damping. Parametric system identification showed that BVLs used proprioceptive information that oriented the UB toward the pelvis to a greater extent compared with Cs. Both subject groups used sensory information that oriented the UB vertical in space to a greater extent as pelvis tilt amplitudes increased. In BVLs, proprioceptive information signaling the UB orientation relative to the fixed lower body provided the vertical reference, whereas in Cs, vestibular information also contributed to the vertical reference.

The Consequences of Short-Range Stiffness and Fluctuating Muscle Activity for Proprioception of Postural Joint Rotations: The Relevance to Human Standing

Proprioception comes from muscles and tendons. Tendon compliance, muscle stiffness, and fluctuating activity complicate transduction of joint rotation to a proprioceptive signal. These problems are acute in postural regulation because of tiny joint rotations and substantial short-range muscle stiffness. When studying locomotion or perturbed balance these problems are less applicable. We recently measured short-range stiffness in standing and considered the implications for load stability. Here, using an appropriately simplified model we analyze the conversion of joint rotation to spindle input and tendon tension while considering the effect of short-range stiffness, tendon compliance, fluctuating muscle activity, and fusimotor activity. Basic principles determine that when muscle stiffness and tendon compliance are high, fluctuating muscle activity is the greatest factor confounding registration of postural movements, such as ankle rotations during standing. Passive and isoactive muscle, uncomplicated by active length fluctuations, enable much better registration of joint rotation and require fewer spindles. Short-range muscle stiffness is a degrading factor for spindle input and enhancing factor for Golgi input. Constant fusimotor activity does not enhance spindle registration of postural joint rotations in actively modulated muscle: spindle input remains more strongly associated with muscle activity than joint rotation. A hypothesized rigid α–γ linkage could remove this association with activity but would require large numbers of spindles in active postural muscles. Using microneurography, the existence of a rigid α–γ linkage could be identified from the correlation between spindle output and muscle activity. Basic principles predict a proprioceptive “dead zone” in the active agonist muscle that is related to the short-range muscle stiffness.

Gaze Anchoring to a Pointing Target Is Present During the Entire Pointing Movement and Is Driven by a Non-Visual Signal

A well-coordinated pattern of eye and hand movements can be observed during goal-directed arm movements. Typically, a saccadic eye movement precedes the arm movement, and its occurrence is temporally correlated with the start of the arm movement. Furthermore, the coupling of gaze and aiming movements is also observable after pointing initiation. It has recently been observed that saccades cannot be directed to new target stimuli, away from a pointing target stimulus. Saccades directed to targets presented during the final phase of a pointing movement were delayed until after pointing movement offset (“gaze anchoring”). The present study investigated whether ocular gaze is anchored to a pointing target during the entire pointing movement. In experiment 1, new targets were presented at various times during the duration of a pointing movement, triggered by the kinematics arm moment itself (movement onset, peak acceleration/velocity/deceleration, and offset). Subjects had to make a saccade to the new target as fast as possible while maintaining the pointing movement to the initial target. Saccadic latencies were increased by an amount of time that approximately equaled the remaining pointing time after saccadic target presentation, with the majority of saccades executed after pointing movement offset. The nature of the signal driving gaze stabilization during pointing was investigated in experiment 2. In previous experiments where ocular gaze was anchored to a pointing target, subjects could always see their moving arm, thus it was unknown whether a visual image of the moving arm, an afferent (proprioceptive) signal or an efferent (motor control related) signal produced gaze anchoring. In experiment 2 subjects had to point with or without vision of the moving arm to test whether a visual signal is used to anchor gaze to a pointing target. Results indicate that gaze anchoring was also observed without vision of the moving arm. The findings support the existence of a mechanism enforcing ocular gaze anchoring during the entire duration of a pointing movement. Moreover, such a mechanism uses an internally generated, or proprioceptive, nonvisual signal. Possible neural substrates underlying these processes are discussed, as well as the role of selective attention.