Complex Spike Activity of Purkinje Cells in the Ventral Uvula and Nodulus of Pigeons in Response to Translational Optic Flow

Wylie, Douglas R. W. and Barrie J. Frost. Complex spike activity of Purkinje cells in the ventral uvula and nodulus of pigeons in response to translational optic flow. J. Neurophysiol. 81: 256–266, 1999. The complex spike (CS) activity of Purkinje cells in the ventral uvula and nodulus of the vestibulocerebellum was recorded from anesthetized pigeons in response to translational optic flow. Translational optic flow was produced using a “translator” projector: a mechanical device that projected a translational optic flowfield onto the walls, ceiling, and floor of the room and encompassed the entire binocular visual field. CS activity was broadly tuned but maximally modulated in response to translational optic flow along a “best” axis. Each neuron was assigned a vector representing the direction in which the animal would need to translate to produce the optic flowfield that resulted in maximal excitation. The vector is described with reference to a standard right-handed coordinate system, where the vectors, + x, + y, and + z represent, rightward, upward, and forward translation of the animal, respectively. Neurons could be grouped into four response types based on the vector of maximal excitation. + y neurons were modulated maximally in response to a translational optic flowfield that results from self-motion upward along the vertical ( y) axis. − y neurons also responded best to translational optic flow along the vertical axis but showed the opposite direction preference. The two remaining groups responded best to translational optic flow along horizontal axes: − x + z neurons and − x− z neurons. In summary, our results suggest that the olivocerebellar system dedicated to the analysis of translational optic flow is organized according to a reference frame consisting of three approximately orthogonal axes: the vertical axis, and two horizontal axes oriented 45° to either side the midline. Previous research has shown that the rotational optic flow system, the eye muscles, the vestibular semicircular canals and the postural control system all share a similar spatial frame of reference.

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Modulation of complex spike activity differs between zebrin-positive and -negative Purkinje cells in the pigeon cerebellum

Journal of Neurophysiology ◽

10.1152/jn.00797.2017 ◽

2018 ◽

Vol 120 (1) ◽

pp. 250-262 ◽

Cited By ~ 4

Author(s):

Rebecca M. Long ◽

Janelle M. P. Pakan ◽

David J. Graham ◽

Peter L. Hurd ◽

Cristian Gutierrez-Ibañez ◽

...

Keyword(s):

Molecular Markers ◽

Purkinje Cells ◽

Optic Flow ◽

Spike Activity ◽

Functional Unit ◽

Mossy Fiber ◽

Vestibular Nuclei ◽

Uniform Structure ◽

Complex Spike ◽

Zebrin Ii

The cerebellum is organized into parasagittal zones defined by its climbing and mossy fiber inputs, efferent projections, and Purkinje cell (PC) response properties. Additionally, parasagittal stripes can be visualized with molecular markers, such as heterogeneous expression of the isoenzyme zebrin II (ZII), where sagittal stripes of high ZII expression (ZII+) are interdigitated with stripes of low ZII expression (ZII−). In the pigeon vestibulocerebellum, a ZII+/− stripe pair represents a functional unit, insofar as both ZII+ and ZII− PCs within a stripe pair respond best to the same pattern of optic flow. In the present study, we attempted to determine whether there were any differences in the responses between ZII+ and ZII− PCs within a functional unit in response to optic flow stimuli. In pigeons of either sex, we recorded complex spike activity (CSA) from PCs in response to optic flow, marked recording sites with a fluorescent tracer, and determined the ZII identity of recorded PCs by immunohistochemistry. We found that CSA of ZII+ PCs showed a greater depth of modulation in response to the preferred optic flow pattern compared with ZII− PCs. We suggest that these differences in the depth of modulation to optic flow stimuli are due to differences in the connectivity of ZII+ and ZII− PCs within a functional unit. Specifically, ZII+ PCs project to areas of the vestibular nuclei that provide inhibitory feedback to the inferior olive, whereas ZII− PCs do not. NEW & NOTEWORTHY Although the cerebellum appears to be a uniform structure, Purkinje cells (PCs) are heterogeneous and can be categorized on the basis of the expression of molecular markers. These phenotypes are conserved across species, but the significance is undetermined. PCs in the vestibulocerebellum encode optic flow resulting from self-motion, and those that express the molecular marker zebrin II (ZII+) exhibit more sensitivity to optic flow than those that do not express zebrin II (ZII−).

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Sensorimotor aspects of high-speed artificial gravity: II. The effect of head position on illusory self motion

Journal of Vestibular Research ◽

10.3233/ves-2003-125-608 ◽

2003 ◽

Vol 12 (5-6) ◽

pp. 283-289

Author(s):

Fred W. Mast ◽

Nathaniel J. Newby ◽

Laurence R. Young

Keyword(s):

Healthy Subjects ◽

Horizontal Plane ◽

High Speed ◽

Semicircular Canals ◽

Vertical Axis ◽

Head Position ◽

Artificial Gravity ◽

Axis Of Rotation ◽

Self Motion

The effects of cross-coupled stimuli on the semicircular canals are shown to be influenced by the position of the subject's head with respect to gravity and the axis of rotation, but not by the subject's head position relative to the trunk. Seventeen healthy subjects made head yaw movements out of the horizontal plane while lying on a horizontal platform (MIT short radius centrifuge) rotating at 23 rpm about an earth-vertical axis. The subjects reported the magnitude and duration of the illusory pitch or roll sensations elicited by the cross-coupled rotational stimuli acting on the semicircular canals. The results suggest an influence of head position relative to gravity. The magnitude estimation is higher and the sensation decays more slowly when the head's final position is toward nose-up (gravity in the subject's head x-z-plane) compared to when the head is turned toward the side (gravity in the subject's head y-z-plane). The results are discussed with respect to artificial gravity in space and the possible role of pre-adaptation to cross-coupled angular accelerations on earth.

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Nonclock behavior of inferior olive neurons: interspike interval of Purkinje cell complex spike discharge in the awake behaving monkey is random

Journal of Neurophysiology ◽

10.1152/jn.1995.73.4.1329 ◽

1995 ◽

Vol 73 (4) ◽

pp. 1329-1340 ◽

Cited By ~ 128

Author(s):

J. G. Keating ◽

W. T. Thach

Keyword(s):

Fourier Transform ◽

Purkinje Cells ◽

Spike Activity ◽

Interspike Interval ◽

Inferior Olive ◽

Fourier Transforms ◽

Wrist Movement ◽

General Role ◽

Complex Spike ◽

Bodily Movement

1. Complex spikes of cerebellar Purkinje cells recorded from awake, behaving monkeys were studied to determine the extent to which their discharge could be quantified as periodic. Three Rhesus monkeys were trained to perform up to five different tasks involving rotation of the wrist in relation to a visual cue. Complex spike activity was recorded during task performance and intertrial time. Interspike intervals were determined from the discharge of each of 89 Purkinje cells located throughout lobules IV, V, and VI. Autocorrelation and Fourier transform of the autocorrelation function were performed on the data. In addition, the activity from one cell was transformed so that the discharge occurred on the beat of a 10-Hz clock, and in a further transformation, on the beat of a noisy 10-Hz clock. These transformed data were then analyzed as described above. 2. Fourier transform of the autocorrelogram function of the data that had been transformed to a 10-Hz clock, and that of the noisy 10-Hz clock, both showed a prominent peak at 10 Hz. However, the autocorrelograms and the Fourier transforms of the autocorrelogram functions failed to reveal a prominent periodicity for the actual discharge of any of cells, at any frequency up to 100 Hz: the discharge appeared random with respect to the interspike interval. The discharge was not random with respect to behavior. Complex spike activity was commonly time locked to the start of wrist movement. We examined this discharge to see whether oscillatory discharge could be seen after alignment of the data on the start of wrist movement, or after alignment of the data on the complex spike occurring peri-start of wrist movement. No oscillation was seen for either alignment. 3. The inferior olive, which sends its climbing fibers to the cerebellum, has been implicated in such different activities as 1) pathological tremor of the soft palate, 2) physiological tremor, 3) the normal initiation of all bodily movement, and 4) motor learning. Previous work in pharmacologically or surgically treated animals has shown that, under some conditions, the discharge of these neurons is periodic and synchronous. This firing pattern has been interpreted to support a role in the first two activities. But measurements reported here in the awake monkey show just the opposite: the discharge is aperiodic to the extent of being random. As such, the inferior olive cannot be a "motor clock" in the general role that has been proposed.(ABSTRACT TRUNCATED AT 400 WORDS)

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Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells

Journal of Neurophysiology ◽

10.1152/jn.1988.60.6.2091 ◽

1988 ◽

Vol 60 (6) ◽

pp. 2091-2121 ◽

Cited By ~ 198

Author(s):

W. Graf ◽

J. I. Simpson ◽

C. S. Leonard

Keyword(s):

Purkinje Cells ◽

Horizontal Plane ◽

Rotation Axis ◽

Modulation Depth ◽

Vertical Axis ◽

Axis Orientation ◽

Complex Spike ◽

Full Field ◽

Simple Spike ◽

Dominant Eye

1. Complex and simple spike responses of Purkinje cells were recorded in the flocculus of anesthetized, paralyzed rabbits during rotating full-field visual stimuli produced by a three-axis planetarium projector. 2. On the basis of the spatial properties of their complex spike responses, floccular Purkinje cells could be placed into three distinct classes called Vertical Axis, Anterior (45 degrees) Axis and Posterior (135 degrees) Axis. The first two classes occurred in both monocular and binocular forms; the third class was encountered only in binocular form. For the binocular response forms, stimulation through one eye, called the dominant eye, elicited a stronger modulation of the complex spike firing rate than did stimulation of the other eye. The approximate orientation of that axis about which full-field rotation elicited the deepest modulation (the preferred axis) when presented to the dominant eye served as the class label. These classes are the same as those determined qualitatively for inferior olive neurons in the previous paper (47). The present study provides a quantitative description of their spatial tuning. 3. For Vertical Axis cells, the dominant eye was ipsilateral with respect to the flocculus recording site. The preferred axis was vertical and null (no-response) axes were in the horizontal plane. For the binocular response form of Vertical Axis cells (less than 10% of this class), the direction preferences for the two eyes were synergistic with respect to rotation about the vertical axis. 4. The dominant eye for the Anterior (45 degrees) Axis cells was contralateral, with the preferred axis oriented in the horizontal plane at approximately 45 degrees contralateral azimuth. The modulation depth showed a close to cosine relation with the angle between the preferred axis and the stimulus rotation axis. The average orientation (n = 10) for the dominant eye preferred axis, determined by the best-fit sinusoid, was 47 degrees contralateral azimuth. The preferred axis orientation for the ipsilateral (nondominant) eye in the binocular response forms was between 45 and 90 degrees azimuth in the horizontal plane. A null axis for each eye was at approximately 90 degrees to the preferred axis. 5. The Posterior (135 degrees) Axis cells were encountered only in binocular response forms. The dominant eye was ipsilateral, with the preferred axis oriented at approximately 135 degrees ipsilateral azimuth close to the horizontal plane. The modulation depth showed a close to cosine relation with the angle between the preferred axis and the stimulus rotation axis.(ABSTRACT TRUNCATED AT 400 WORDS)

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Adaptive Balance in Posterior Cerebellum

Frontiers in Neurology ◽

10.3389/fneur.2021.635259 ◽

2021 ◽

Vol 12 ◽

Author(s):

Neal H. Barmack ◽

Vito Enrico Pettorossi

Keyword(s):

Purkinje Cells ◽

Stellate Cell ◽

Semicircular Canals ◽

Mossy Fibers ◽

Vestibular Nuclei ◽

Three Dimensions ◽

Optokinetic Stimulation ◽

Afferent Pathways ◽

Vestibular Nuclear Neurons ◽

Self Motion

Vestibular and optokinetic space is represented in three-dimensions in vermal lobules IX-X (uvula, nodulus) and hemisphere lobule X (flocculus) of the cerebellum. Vermal lobules IX-X encodes gravity and head movement using the utricular otolith and the two vertical semicircular canals. Hemispheric lobule X encodes self-motion using optokinetic feedback about the three axes of the semicircular canals. Vestibular and visual adaptation of this circuitry is needed to maintain balance during perturbations of self-induced motion. Vestibular and optokinetic (self-motion detection) stimulation is encoded by cerebellar climbing and mossy fibers. These two afferent pathways excite the discharge of Purkinje cells directly. Climbing fibers preferentially decrease the discharge of Purkinje cells by exciting stellate cell inhibitory interneurons. We describe instances adaptive balance at a behavioral level in which prolonged vestibular or optokinetic stimulation evokes reflexive eye movements that persist when the stimulation that initially evoked them stops. Adaptation to prolonged optokinetic stimulation also can be detected at cellular and subcellular levels. The transcription and expression of a neuropeptide, corticotropin releasing factor (CRF), is influenced by optokinetically-evoked olivary discharge and may contribute to optokinetic adaptation. The transcription and expression of microRNAs in floccular Purkinje cells evoked by long-term optokinetic stimulation may provide one of the subcellular mechanisms by which the membrane insertion of the GABAA receptors is regulated. The neurosteroids, estradiol (E2) and dihydrotestosterone (DHT), influence adaptation of vestibular nuclear neurons to electrically-induced potentiation and depression. In each section of this review, we discuss how adaptive changes in the vestibular and optokinetic subsystems of lobule X, inferior olivary nuclei and vestibular nuclei may contribute to the control of balance.

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Time Course and Magnitude of Illusory Translation Perception During Off-Vertical Axis Rotation

Journal of Neurophysiology ◽

10.1152/jn.00613.2005 ◽

2006 ◽

Vol 95 (3) ◽

pp. 1571-1587 ◽

Cited By ~ 23

Author(s):

R.A.A. Vingerhoets ◽

W. P. Medendorp ◽

J.A.M. Van Gisbergen

Keyword(s):

Motion Perception ◽

Time Constant ◽

Time Course ◽

Interaction Model ◽

Semicircular Canals ◽

Vertical Axis ◽

Original Proposal ◽

Axis Rotation ◽

Motion Percept ◽

Self Motion

Human spatial orientation relies on vision, somatosensory cues, and signals from the semicircular canals and the otoliths. The canals measure rotation, whereas the otoliths are linear accelerometers, sensitive to tilt and translation. To disambiguate the otolith signal, two main hypotheses have been proposed: frequency segregation and canal–otolith interaction. So far these models were based mainly on oculomotor behavior. In this study we investigated their applicability to human self-motion perception. Six subjects were rotated in yaw about an off-vertical axis (OVAR) at various speeds and tilt angles, in darkness. During the rotation, subjects indicated at regular intervals whether a briefly presented dot moved faster or slower than their perceived self-motion. Based on such responses, we determined the time course of the self-motion percept and characterized its steady state by a psychometric function. The psychophysical results were consistent with anecdotal reports. All subjects initially sensed rotation, but then gradually developed a percept of being translated along a cone. The rotation percept could be described by a decaying exponential with a time constant of about 20 s. Translation percept magnitude typically followed a delayed increasing exponential with delays up to 50 s and a time constant of about 15 s. The asymptotic magnitude of perceived translation increased with rotation speed and tilt angle, but never exceeded 14 cm/s. These results were most consistent with predictions of the canal–otolith-interaction model, but required parameter values that differed from the original proposal. We conclude that canal–otolith interaction is an important governing principle for self-motion perception that can be deployed flexibly, dependent on stimulus conditions.

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Topography and Reciprocal Activity of Cerebellar Purkinje Cells in the Uvula-Nodulus Modulated by Vestibular Stimulation

Journal of Neurophysiology ◽

10.1152/jn.1997.78.6.3083 ◽

1997 ◽

Vol 78 (6) ◽

pp. 3083-3094 ◽

Cited By ~ 58

Author(s):

H. Fushiki ◽

N. H. Barmack

Keyword(s):

Purkinje Cell ◽

Purkinje Cells ◽

Semicircular Canals ◽

Vertical Axis ◽

Longitudinal Axis ◽

Vestibular Stimulation ◽

Climbing Fiber ◽

Null Plane ◽

Cerebellar Purkinje Cells ◽

Vertical Semicircular Canals

Fushiki, H. and N. H. Barmack. Topography and reciprocal activity of cerebellar Purkinje cells in the uvula-nodulus modulated by vestibular stimulation. J. Neurophysiol. 78: 3083–3094, 1997. In the rabbit uvula-nodulus, vestibular and optokinetic information is mapped onto parasagittal zones by climbing fibers. These zones are related functionally to different pairs of vertical semicircular canals, otolithic inputs and horizontal optokinetic inputs. Vestibular stimulation restricted to one of these zones modulates climbing fiber responses (CFRs). Within each of these zones, simple spikes (SSs) are modulated reciprocally with CFRs. In rabbits anesthetized with chloralose-urethan, we have used vestibular and optokinetic stimulation to evoke CFRs within a parasagittal zone while recording from Purkinje cells in adjacent zones. We have examined whether the CFRs evoked by vestibular stimulation in one zone influence the SSs of an adjacent zone. CFRs and SSs were recorded during roll vestibular stimulation. The orientation of the head of the rabbit with respect to the axis of rotation was varied systematically so that a climbing fiber null plane could be determined. This null plane was the orientation of the head about the vertical axis at which no modulation of the CFR was observed during rotation about the longitudinal axis of the vestibular rate table. In the left uvula-nodulus, a medial sagittal strip extending through all the folia contained Purkinje cells with CFRs that had optimal planes of stimulation coplanar with the left posterior-right anterior semicircular canals (LPC-RAC). Lateral to this strip was a strip of Purkinje cells with CFRs that were characterized by optimal planes corresponding to stimulation of the left anterior-right posterior semicircular canals (LAC-RPC). SSs in Purkinje cells were modulated out of phase with CFRs from the same Purkinje cell. The depth of modulation of both CFRs and SSs was reduced during rotation in the climbing fiber “null plane”. The depth of modulation of SSs was greatest when recorded from Purkinje cells located at the center of semicircular canal-related strip. We observed that 1) all folia of the uvula-nodulus receive vestibular climbing fiber inputs; 2) these climbing fiber inputs convey information from the vertical semicircular canals and otoliths but not the horizontal semicircular canals; 3) CFRs evoked in a particular sagittal zone do not influence SSs in adjacent zones; 4) modulation of a CFRs in a particular Purkinje cell can occur without modulation of SSs in the same Purkinje cell, although modulation of SSs was not observed in the absence of CFR modulation; and 5) modulation of SSs sometimes preceded that of CFRs in the same cell, implying that interneuronal pathways may contribute to SS modulation. Climbing fiber-driven Golgi cells, the inhibitory axon terminals of which end on granule cell dendrites in the classic glomerular synapse, may provide this interneuronal mechanism.

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