Responses of cerebellar Purkinje cells to slip of a hand-held object

1992 ◽  
Vol 67 (3) ◽  
pp. 483-495 ◽  
Author(s):  
C. Dugas ◽  
A. M. Smith

1. Two monkeys were trained to grasp, lift, and hold a device between the thumb and forefinger for 1 s. The device was equipped with a position transducer and strain gauges that measured the horizontal grip force and the vertical lifting or load force. On selected blocks of 20-30 trials, a force-pulse perturbation was applied to the object during static holding to simulate object slip. The animals were required to resist this displacement by stiffening the joints of their wrists and fingers to obtain a fruit juice reward. Single cells in the hand representation area of the paravermal anterior lobe of the cerebellar cortex were recorded during perturbed and unperturbed holding. If conditions permitted, the cell discharge was also recorded during lifting of objects of various weights (15, 65, or 115 g) or different surface textures (sandpaper or polished metal), and when possible the cutaneous or proprioceptive fields of the neurons were characterized with the use of natural stimulation. 2. On perturbed trials, the force pulse was always applied to the manipulandum after it had been held stationary within the position window for 750 ms. The perturbation invariably elicited a reflexlike increase of electromyographic (EMG) activity in wrist and finger muscles, resulting in a time-locked increase in grip force that peaked at a latency between 50 and 100 ms. 3. The object-slip perturbation had a powerful effect on cerebellar cortical neurons at a mean latency of 45 +/- 14 (SD) ms. Reflexlike increases or decreases in simple spike discharge occurred in 55% (53/97) of unidentified cells and 49% (21/43) of Purkinje cells recorded in the anterior paravermal and lateral cerebellar cortex. 4. The perturbation failed to evoke complex spike responses from any of the Purkinje cells examined. All the perturbation-evoked activity changes involved modulation of the simple spike discharge. The perturbations stimulated the simple-spike receptive field of most Purkinje cells recorded here, which suggests that the short-latency unit responses were triggered by afferent stimulation. Only one Purkinje cell was found with a distinct complex-spike receptive field on the thumb, but this neuron did not respond to the perturbation. It appears that simple- and complex-spike to receptive fields are not always identical or even closely related. 5. The majority of Purkinje and unidentified neurons that responded to the perturbation had cutaneous receptive fields, although some had proprioceptive fields. Seventy-seven neurons were examined for peripheral receptive fields and were also tested with the perturbation.(ABSTRACT TRUNCATED AT 400 WORDS)

1990 ◽  
Vol 64 (3) ◽  
pp. 698-714 ◽  
Author(s):  
E. Espinoza ◽  
A. M. Smith

1. Three monkeys (2.5-3.5 kg) were trained to pinch an object between the thumb and forefinger and to lift it a vertical distance of 1.0-2.0 cm. Either the object weight (15, 65, or 115 g) or the surface texture (sand paper or polished metal) contacting the fingers could be varied. The object was equipped with a vertical position transducer, an accelerometer, and strain gauges that measured the grip force and the vertical load force. 2. In accordance with similar previously published studies on human subjects, it was found that monkeys appropriately scaled the grip forces according to the weight and coefficient of friction of the object. The grip force preceded the load force by 25 ms, and they both covaried with the changes in surface friction. 3. An analysis of electromyograms (EMGs) recorded intramuscularly from the muscles of the wrist and fingers including both flexors and extensors indicated that 26 muscles were active during pinching and lifting. Of these, 17 produced the maximum activity for the slippery surface and the greatest weight and the least activity with the roughest surface and lightest weight. 4. A total of 59 Purkinje cells and 123 unidentified units recorded from the paravermal and lateral cerebellar cortex were found to change their firing frequency during lifting the experimental object. 5. Increased discharge during the grasping and lifting was found for 56% (33/59) of the Purkinje cells and 80% (98/123) of the unidentified neurons, whereas 44% (26/59) of the Purkinje cells and 20% of the unidentified neurons decreased activity during the same period. 6. Significant modulations of the firing frequency with surface texture or object weight occurred for 59% (35/59) of the Purkinje cells and 67% (82/123) of the unidentified neurons. 7. One hundred and three Purkinje and unidentified neurons recorded in the paravermal and lateral region of the cerebellar cortex were examined for peripheral receptive fields, and of these, 43/103 (42%) responded exclusively to imposed displacements and tapping of muscles suggesting afferents originating from proprioceptors. A further 28/103 (27%) had exclusively cutaneous receptive fields on the hand that could be stimulated by brushing the skin lightly with a sable hair brush. Only six neurons demonstrated convergent cutaneous and proprioceptive receptive fields and no response to peripheral stimulation could be found for 26 neurons. No difference was found between the receptive fields of Purkinje cells and those of the unidentified neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1987 ◽  
Vol 57 (3) ◽  
pp. 787-802 ◽  
Author(s):  
J. H. Kim ◽  
J. J. Wang ◽  
T. J. Ebner

The relationship of the climbing fiber afferent discharge to the unperturbed and perturbed step cycle was evaluated in the cat. Following a precollicular-premamillary decerebration, cats walked spontaneously on a motorized treadmill. Purkinje cells were recorded extracellularly and simple and complex spikes were discriminated. Right forelimb displacement, biceps and triceps EMG activity, as well as treadmill velocity, were also monitored. In some animals pressure measurements of the contact of the footpad with the treadmill were obtained. Cells were studied during both “normal” and perturbed locomotion. The perturbation consisted of a braking of the treadmill at different phases in the step cycle. Histograms of the simple and complex spike activity, and averages of the right forelimb displacement, biceps, and triceps EMG activity and treadmill velocity were constructed. The complex spike activity of 163 Purkinje cells was averaged through a minimum of 50 sweeps in either normal and/or perturbed locomotion. Statistical analysis revealed that the probability of the climbing fiber afferent discharge in 54% of the cells (36/67) studied during normal locomotion was significantly modulated with the step cycle. For most Purkinje cells the onset of the increase in climbing fiber afferent discharge was coupled to triceps activity and the onset of stance phase. A group of cells exhibited complex spike discharge in association with biceps onset and swing. These observations suggest that complex spike discharge occurs preferentially at the phase transition periods in the step cycle when the trajectory of the forelimb changes from swing to stance or stance to swing. During treadmill braking 51% of the cells exhibited complex spike modulation (70/137). A number of different patterns of climbing fiber afferent modulation occurred. The most common pattern was an increase in complex spike discharge with the resumption of the treadmill movement and locomotion. Analysis of the time of these periods of increased climbing fiber activity suggests that, although in some cells the response is coupled to the treadmill onset, in other cells the modulation occurs at longer latencies. Subsequent analysis aligning the EMG, displacement, and treadmill velocity signals with the times of the climbing fiber afferent discharge suggested some responses were coupled to the reinitiation of the locomotor cycle. The second most common pattern was an increase in climbing fiber afferent discharge at the onset of the perturbation. Also, in some cells, complex spike discharge decreased during the period in which the step cycle was arrested.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 60 (6) ◽  
pp. 2091-2121 ◽  
Author(s):  
W. Graf ◽  
J. I. Simpson ◽  
C. S. Leonard

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)


2000 ◽  
Vol 84 (6) ◽  
pp. 2945-2960 ◽  
Author(s):  
Maninder Kahlon ◽  
Stephen G. Lisberger

We followed simple- and complex-spike firing of Purkinje cells (PCs) in the floccular complex of the cerebellum through learned modifications of the pursuit eye movements of two monkeys. Learning was induced by double steps of target speed in which initially stationary targets move at a “learning” speed for 100 ms and then change to either a higher or lower speed in the same direction. In randomly interleaved control trials, targets moved at the learning speed in the opposite direction. When the learning direction was theon direction for simple-spike responses, learning was associated with statistically significant changes in simple-spike firing for 10 of 32 PCs. Of the 10 PCs that showed significant expressions of learning, 8 showed changes in simple-spike output in the expected direction: increased or decreased firing when eye acceleration increased or decreased through learning. There were no statistically significant changes in simple-spike responses or eye acceleration during pursuit in the control direction. When the learning direction was in the off direction for simple-spike responses, none of 15 PCs showed significant correlates of learning. Although changes in simple-spike firing were recorded in only a subset of PCs, analysis of the population response showed that the same relationship between population firing and eye acceleration obtained before and after learning. Thus learning is associated with changes that render the modified population response appropriate to drive the changed behavior. To analyze complex-spike firing during learning we correlated complex-spike firing in the second, third, and fourth 100 ms after the onset of target motion with the retinal image motion in the previous 100 ms. Data were largely consistent with previous evidence that image motion drives complex spikes with a direction selectivity opposite that for simple spikes. Comparison of complex-spike responses at different times after the onset of control and learning target motions in the learning direction implied that complex spikes could guide learning during decreases but not increases in eye acceleration. Learning caused increases or decreases in the sensitivity of complex spikes to image motion in parallel with changes in eye acceleration. Complex-spike responses were similar in all PCs, including many in which learning did not modify simple-spike responses. Our data do not disprove current theories of cerebellar learning but suggest that these theories would have to be modified to account for simple- and complex-spike firing of floccular Purkinje cells reported here.


Neuroreport ◽  
1997 ◽  
Vol 8 (2) ◽  
pp. 523-529 ◽  
Author(s):  
Qing-Gong Fu ◽  
Carolyn R. Mason ◽  
Didier Flament ◽  
Jonathon D. Coltz ◽  
Timothy J. Ebner

eNeuro ◽  
2017 ◽  
Vol 4 (2) ◽  
pp. ENEURO.0036-17.2017 ◽  
Author(s):  
Laurentiu S. Popa ◽  
Martha L. Streng ◽  
Timothy J. Ebner

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Haibo Zhou ◽  
Zhanmin Lin ◽  
Kai Voges ◽  
Chiheng Ju ◽  
Zhenyu Gao ◽  
...  

Due to the uniform cyto-architecture of the cerebellar cortex, its overall physiological characteristics have traditionally been considered to be homogeneous. In this study, we show in awake mice at rest that spiking activity of Purkinje cells, the sole output cells of the cerebellar cortex, differs between cerebellar modules and correlates with their expression of the glycolytic enzyme aldolase C or zebrin. Simple spike and complex spike frequencies were significantly higher in Purkinje cells located in zebrin-negative than zebrin-positive modules. The difference in simple spike frequency persisted when the synaptic input to, but not intrinsic activity of, Purkinje cells was manipulated. Blocking TRPC3, the effector channel of a cascade of proteins that have zebrin-like distribution patterns, attenuated the simple spike frequency difference. Our results indicate that zebrin-discriminated cerebellar modules operate at different frequencies, which depend on activation of TRPC3, and that this property is relevant for all cerebellar functions.


2015 ◽  
Vol 113 (7) ◽  
pp. 2524-2536 ◽  
Author(s):  
Haibo Zhou ◽  
Kai Voges ◽  
Zhanmin Lin ◽  
Chiheng Ju ◽  
Martijn Schonewille

The massive computational capacity of the cerebellar cortex is conveyed by Purkinje cells onto cerebellar and vestibular nuclei neurons through their GABAergic, inhibitory output. This implies that pauses in Purkinje cell simple spike activity are potentially instrumental in cerebellar information processing, but their occurrence and extent are still heavily debated. The cerebellar cortex, although often treated as such, is not homogeneous. Cerebellar modules with distinct anatomical connectivity and gene expression have been described, and Purkinje cells in these modules also differ in firing rate of simple and complex spikes. In this study we systematically correlate, in awake mice, the pausing in simple spike activity of Purkinje cells recorded throughout the entire cerebellum, with their location in terms of lobule, transverse zone, and zebrin-identified cerebellar module. A subset of Purkinje cells displayed long (>500-ms) pauses, but we found that their occurrence correlated with tissue damage and lower temperature. In contrast to long pauses, short pauses (<500 ms) and the shape of the interspike interval (ISI) distributions can differ between Purkinje cells of different lobules and cerebellar modules. In fact, the ISI distributions can differ both between and within populations of Purkinje cells with the same zebrin identity, and these differences are at least in part caused by differential synaptic inputs. Our results suggest that long pauses are rare but that there are differences related to shorter intersimple spike intervals between and within specific subsets of Purkinje cells, indicating a potential further segregation in the activity of cerebellar Purkinje cells.


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