Lecture IV. Sensory processing during active versus passive movements
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1 Lecture IV Sensory processing during active versus passive movements
2 The ability to distinguish sensory inputs that are a consequence of our own actions (reafference) from those that result from changes in the external world (exafference) is essential for perceptual stability. For example: Targets rapidly jump across the retina as we move our eyes to make saccades. Yet, we do not see the world move over our retina. In contrast, Hemhlotz (1867) made the salient observation that tapping on the canthus of the eye, results in an illusionary shift of the visual world. How can continually changing retinal inputs to the visual system result in the perception of a stable visual world during eye movements?
3 The ability to distinguish reafference and exafference is not only crucial for perceptual stability, but it is also required to produce accurate neural representations of the environment in order to accurately guide behaviour. Consider: The vestibular system provides information about head motion relative to space that is necessary for the maintenance of posture, computation of spatial orientation and perception of self-motion. How are sensory inputs processed during active movements where an intact reflex could be counter productive relative to the behavioral goal?
4 Von Holst and Mittelstaedt (1950) originally proposed that to distinguish between reafference and exafference 1) The central nervous system sends a parallel efference copy of the motor command to sensory areas. 2) In turn, this anticipatory signal is subtracted from the incoming sensory signal to selectively remove that portion due to the animal s own actions. In this lecture, I consider recent experiments that have addressed this idea and will focus on experiments in the primate vestibular system.
5 Simplified Schema: Reafference Principle of Von Holst and Mittelstaedt
6 The Vestibular System Semicircular canals - sense angular rotation Otoliths - sense linear acceleration Provide information about head motion relative to space and gravity to: 1) Maintain head and body posture 2) Stabilize the visual axis 3) Compute spatial orientation 4) Navigation
7 Vestibular Nuclei: Inputs from the Labyrinth Inputs: Superior/Medial predominantly canal Lateral canal and otolith Descending predominantly otolith
8 Inputs to the Vestibular Nuclei Cortical Inputs - parietoinsular vest. cortex - premotor area 6, 6pa - cingulate cortex areas 23cd, 23cv, 6c - somatosensory area 3a - intraparietal sulcus area 2v - superior temporal cortex Oculomotor Inputs -reticular formation -prepositus Cerebellar Inputs - flocculus/paraflocculus - uvula/nodulus Neck Proprioception - via central cervical nucleus Semicircular Canals
9 Does this convergence of inputs at the level of the vestibular nuclei alter the processing of vestibular information during active versus passive head movements? And if so, how?
10 Passive Whole-Body Rotation Active Head-on-Body Rotation
11 H Vestibular Nuclei Position-vestibularpause Abducens Vestibulo-ocular Reflex (stabilize image on the retina) Horizontal Canal Vestibular Only Neck Motoneurons Vestibulo-collic Reflex (stabilize the head on the body)
12 First Consider: Vestibular-only neurons in the vestibular nuclei H Vestibular Nuclei Vestibular Only Horizontal Canal Neck Motoneurons Vestibulo-collic Reflex (stabilize the head on the body)
13 H Vestibular Nuclei Vestibular Only Horizontal Canal nodulus - uvula Neck Motoneurons Vestibulo-collic Reflex (stabilize the head on the body) Cerebellum Thalamus/Cortex?
14 Experimental Setup Torque motor Spring system Laser target Head coil placed close to eye Huterer and Cullen, 2002
15 VO Neurons: Traditional Characterization Roy and Cullen, J. Neurosci., 2001
16 Vestibular Only neuron Active head-on-body motion A. Gaze shifts G B. Population 50 deg 400 deg/s 200 sp/s E H G E H pwbr model FR Normalized mean head velocity sensitivity relative to pwbrd pwbr * * * * * Gaze shift amplitude 100 ms Roy and Cullen, J. Neurosci., 2001
17 Vestibular Only neuron Simultaneous Passive and Active head-in-space motion Chair rotation 200 deg/s H-in-space H-on-neck G 100 sp/s 1 sec E H-in-space model passive model FR Roy and Cullen, J. Neurosci., 2001
18 Possible mechanisms for the selective gating-out of active head velocity signals H Horizontal Canal Vestibular Afferents 1) Neck Proprioception 2) Cognitive Inputs 3) Efference copy of neck motor command OR Vestibular Nuclei VO Neck Motoneurons VCR
19 Possible mechanisms for the selective gating-out of active head velocity signals H Horizontal Canal Vestibular Afferents 1) Neck Proprioception 2) Cognitive Inputs 3) Efference copy of neck motor command OR Vestibular Nuclei VO Neck Motoneurons VCR
20 1.) Do neck proprioceptive inputs play a role? A. Passive head-on-body rotation 200 deg/s 100 sp/s 4 sec G E B S H B H model B FR B. Body-under-neck rotation 200 deg/s 1 Nm 200 sp/s 1 sec G E H torque (this paradigm) torque (saccades to food) N N model prediction N model estimate FR torque sensor Roy and Cullen, J. Neurosci., 2001
21 2.) Do cognitive inputs play a role? Switch 200 deg/s G E H B Turntable 100 sp/s 2 sec H S FR = pwbr model B S Roy and Cullen, J. Neurosci., 2001
22 2.) Do cognitive inputs play a role? steering wheel 200 deg/s G E laser targets 100 sp/s 500 msec H B H S pwbr model FR = BS Roy and Cullen, J. Neurosci., 2001
23 Vestibular Only neurons Normalized mean head velocity sensitivity relative to pwbrd PWBRc Roy and Cullen, J. Neurosci., 2001 Passive rotation Passive Hrotation B PWBR head-unrestrained Voluntary H B Gaze shift Gaze redirection Gaze pursuit Post gaze shift Gaze stabilization Voluntary H S(= B) S Driving task
24 Possible mechanisms for the selective gating-out of active head velocity signals A. B. H H Horizontal Canal Vestibular Afferents Horizontal Canal Vestibular Afferents 1) Neck Proprioception 2) Cognitive inputs OR Vestibular Nuclei VO Neck Proprioception Gate OR Vestibular Nuclei VO 3) Efference copy of neck motor command Neck Motoneurons VCR Efference copy of neck motor command Neck Motoneurons VCR
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