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

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.


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)


1988 ◽  
Vol 60 (6) ◽  
pp. 2073-2090 ◽  
Author(s):  
C. S. Leonard ◽  
J. I. Simpson ◽  
W. Graf

1. Single-unit responses to large-field visual stimuli were recorded extracellularly from neurons in the dorsal cap of Kooy of the inferior olive in anesthetized, paralyzed rabbits. The visually modulated neurons in the dorsal cap responded optimally to slow rotation of random dot stimuli, which were produced using handheld patterns or a planetarium projector. 2. Neurons had either monocular or binocular receptive fields. For binocular receptive field neurons, monocular stimulation of one eye, called the dominant eye, elicited greater modulation than did stimulation of the other eye. Rotation about a particular axis, called the preferred axis, produced both maximal excitation and inhibition. On the basis of differences in preferred axis orientation and in eye dominance, three neuron classes called Vertical Axis, Anterior (45 degrees) Axis, and Posterior (135 degrees) Axis were distinguished. 3. Vertical Axis neurons were modulated exclusively from the eye contralateral to the inferior olive recording site. This cell type responded strongly to large-field visual stimuli rotating about the vertical axis. Excitation resulted from movement in the temporal to nasal direction, and inhibition occurred during movement in the nasal to temporal direction. 4. Two subclasses of Anterior (45 degrees) Axis neurons were distinguished according to whether the receptive field was monocular or binocular. For both subclasses, the dominant eye was ipsilateral. The receptive field organization of the dominant eye was bipartite as described in the previous paper (51) for neurons in the midbrain visual tegmental relay zone. Anterior (45 degrees) Axis neurons were maximally excited when the stimulus pattern moved upward and posterior above the horizon in the anterior quadrant of the ipsilateral visual field, from 0 degrees (nose) to approximately 45 degrees azimuth. From 45 to 180 degrees azimuth (occiput) and above the horizon, these neurons were excited by downward and posterior movement. Inhibition occurred with oppositely directed movements. For rotating stimuli presented to the dominant eye, this class of neurons responded best to rotation of the visual world about an axis oriented near the horizontal plane and approximately 45 degrees azimuth. 5. The receptive field of Posterior (135 degrees) Axis neurons was always binocular, with the dominant eye contralateral. For the contralateral receptive field, from 0 degree (nose) to 135 degrees azimuth and above the horizon, excitation occurred during upward and posterior movement.(ABSTRACT TRUNCATED AT 400 WORDS)


1993 ◽  
Vol 69 (2) ◽  
pp. 303-317 ◽  
Author(s):  
H. S. Tan ◽  
J. van der Steen ◽  
J. I. Simpson ◽  
H. Collewijn

1. Three-dimensional rotations of both eyes were measured in alert rabbits during optokinetic stimulation about axes lying in the horizontal plane or about an earth-vertical axis, with either one or both eyes viewing the stimulus. Optokinetic stimulus speed was 2 degrees /s, either continuous or alternating in polarity (triangular stimulus). In addition to the gains of the responses, the orientations of the response axes relative to the stimulus axes were determined. 2. In comparison to the response to constant-speed optokinetic stimulation about the vertical axis, the response to constant-speed optokinetic stimulation about horizontal axes was characterized by the lack of a speed buildup. In many cases, slow phase tracking was good as long as the eye was within the central oculomotor range but deteriorated when eye deviation became more eccentric and fast phases failed to be generated. These features suggest that the optokinetic reflex about horizontal axes functions as a position-control system, rather than as a velocity-control system. 3. Binocular optokinetic stimulation at constant speed (2 degrees/s) about the roll axis (0 degrees azimuth horizontal axis) elicited disconjugate responses. Although the gain of the response was not significantly different in the two eyes (0.38 for downward and 0.44 for upward stimulation), the response axes of the two eyes differed by as much as 51 degrees. 4. Monocular, horizontal axis optokinetic stimulation at constant speed elicited responses that were grossly dissociated between the two eyes. The magnitude of the responses was anisotropic in that it varied with the azimuthal orientation of the stimulus axis; the maximum gain for each eye (0.41 for the seeing and 0.33 for the covered eye) was at 135 degrees azimuth for each eye. The axis orientation and direction (sense of rotation) of the optokinetic stimulus eliciting the maximal response for each eye coincided with the optic flow normally associated with the maximal excitation of the corresponding ipsilateral anterior canal. 5. Binocular, triangular optokinetic stimulation with small excursions (+/- 10 degrees), which avoided the saturation problems of constant-speed stimulation, elicited adequate responses without systematic directional asymmetries. Gain was approximately 0.9 for all stimulus axis orientations in the horizontal plane. 6. During monocular stimulation with triangular stimuli, the response of the seeing eye showed a gain of approximately 0.5 for all orientations of the stimulus axis. In contrast, the covered eye showed anisotropic responses, with a maximum gain of approximately 0.5 during stimulation of the seeing eye about its 45 degree axis.(ABSTRACT TRUNCATED AT 400 WORDS)


2004 ◽  
Vol 19 (3) ◽  
pp. 687-697 ◽  
Author(s):  
H. H. L. M. Goossens ◽  
F. E. Hoebeek ◽  
A. M. van Alphen ◽  
J. van der Steen ◽  
J. S. Stahl ◽  
...  

2015 ◽  
Vol 113 (2) ◽  
pp. 578-591 ◽  
Author(s):  
Marife Arancillo ◽  
Joshua J. White ◽  
Tao Lin ◽  
Trace L. Stay ◽  
Roy V. Sillitoe

Purkinje cell activity is essential for controlling motor behavior. During motor behavior Purkinje cells fire two types of action potentials: simple spikes that are generated intrinsically and complex spikes that are induced by climbing fiber inputs. Although the functions of these spikes are becoming clear, how they are established is still poorly understood. Here, we used in vivo electrophysiology approaches conducted in anesthetized and awake mice to record Purkinje cell activity starting from the second postnatal week of development through to adulthood. We found that the rate of complex spike firing increases sharply at 3 wk of age whereas the rate of simple spike firing gradually increases until 4 wk of age. We also found that compared with adult, the pattern of simple spike firing during development is more irregular as the cells tend to fire in bursts that are interrupted by long pauses. The regularity in simple spike firing only reached maturity at 4 wk of age. In contrast, the adult complex spike pattern was already evident by the second week of life, remaining consistent across all ages. Analyses of Purkinje cells in alert behaving mice suggested that the adult patterns are attained more than a week after the completion of key morphogenetic processes such as migration, lamination, and foliation. Purkinje cell activity is therefore dynamically sculpted throughout postnatal development, traversing several critical events that are required for circuit formation. Overall, we show that simple spike and complex spike firing develop with unique developmental trajectories.


1983 ◽  
Vol 50 (1) ◽  
pp. 205-219 ◽  
Author(s):  
T. J. Ebner ◽  
Q. X. Yu ◽  
J. R. Bloedel

These experiments were designed to test the hypothesis that climbing fiber inputs evoked by a peripheral stimulus increase the responsiveness of Purkinje cells to mossy fiber inputs. This hypothesis was based on a previous series of observations demonstrating that spontaneous climbing fiber inputs are associated with an accentuation of the Purkinje cell responses to subsequent mossy fiber inputs (10, 12). Furthermore, short-term nonpersistent interactions between climbing and mossy fiber inputs have been an important aspect of many theories of cerebellar function (5, 7, 8, 12, 36). Extracellular unitary recordings were made from Purkinje cells in lobule V of decerebrate, unanesthetized cats. To activate mossy and climbing fiber inputs, the forepaw was passively flexed by a Ling vibrator system. A data analysis was developed to sort the simple spike trials into two groups, based on the presence or absence of complex spikes activated by the stimulus. In addition, during those trials in which complex spikes were activated, the simple spike train was aligned on the occurrence of the complex spike. For each simple spike response to the forepaw input, the average firing rate during the response was compared to background both in those trials in which complex spikes were activated and in those in which they were not. The ratio of the response amplitudes in the histograms constructed from these two groups of trials permitted a quantification of the change in responsiveness when climbing fiber inputs were activated. The results show that both excitatory and inhibitory simple spike responses are accentuated when associated with the activation of a complex spike. Using an arbitrary level of a gain change ratio of 120% as indicating a significant modification, 64% of the response components analyzed increased their amplitude when climbing fiber input was present. Simple spike response components occurring prior to complex spike activation were usually not accentuated, although in a few cells the amplitude of this component of the response increased. In addition, in a small number of cells the occurrence of complex spikes was associated with a new simple spike component. For excitatory responses, the magnitude of the gain change ratio was shown to be inversely related to the amplitude of the simple spike response evoked by the mossy fiber inputs. The data obtained is consistent with the hypothesis that the climbing fiber input is associated with an increase in the responsiveness of Purkinje cells to mossy fiber inputs. The increased responsiveness occurs whether the simple spike modulation evoked by the peripheral stimulus is excitatory or inhibitory. The change in responsiveness is short term and nonpersistent. It is argued that the activation of climbing fiber inputs to the cerebellar cortex is associated with an increase in the gain of Purkinje cells to mossy fiber inputs activated by natural peripheral stimuli.


1997 ◽  
Vol 77 (4) ◽  
pp. 1747-1758 ◽  
Author(s):  
C. I. De Zeeuw ◽  
S.K.E. Koekkoek ◽  
D.R.W. Wylie ◽  
J. I. Simpson

De Zeeuw, C. I., S.K.E. Koekkoek, D.R.W. Wylie, and J. I. Simpson. Association between dendritic lamellar bodies and complex spike synchrony in the olivocerebellar system. J. Neurophysiol. 77: 1747–1758, 1997. Dendritic lamellar bodies have been reported to be associated with dendrodendritic gap junctions. In the present study we investigated this association at both the morphological and electrophysiological level in the olivocerebellar system. Because cerebellar GABAergic terminals are apposed to olivary dendrites coupled by gap junctions, and because lesions of cerebellar nuclei influence the coupling between neurons in the inferior olive, we postulated that if lamellar bodies and gap junctions are related, then the densities of both structures will change together when the cerebellar input is removed. Lesions of the cerebellar nuclei in rats and rabbits resulted in a reduction of the density of lamellar bodies, the number of lamellae per lamellar body, and the density of gap junctions in the inferior olive, whereas the number of olivary neurons was not significantly reduced. The association between lamellar bodies and electrotonic coupling was evaluated electrophysiologically in alert rabbits by comparing the occurrence of complex spike synchrony in different Purkinje cell zones of the flocculus that receive their climbing fibers from olivary subnuclei with different densities of lamellar bodies. The complex spike synchrony of Purkinje cell pairs, that receive their climbing fibers from an olivary subnucleus with a high density of lamellar bodies, was significantly higher than that of Purkinje cells, that receive their climbing fibers from a subnucleus with a low density of lamellar bodies. To investigate whether the complex spike synchrony is related to a possible synchrony between simple spikes, we recorded simultaneously the complex spike and simple spike responses of Purkinje cell pairs during natural visual stimulation. Synchronous simple spike responses did occur, and this synchrony tended to increase as the synchrony between the complex spikes increased. This relation raises the possibility that synchronously activated climbing fibers evoke their effects in part via the simple spike response of Purkinje cells. The present results indicate that dendritic lamellar bodies and dendrodendritic gap junctions can be downregulated concomitantly, and that the density of lamellar bodies in different olivary subdivisions is correlated with the degree of synchrony of their climbing fiber activity. Therefore these data support the hypothesis that dendritic lamellar bodies can be associated with dendrodendritic gap junctions. Considering that the density of dedritic lamellar bodies in the inferior olive is higher than in any other area of the brain, this conclusion implies that electrotonic coupling is important for the function of the olivocerebellar system.


1999 ◽  
Vol 81 (1) ◽  
pp. 256-266 ◽  
Author(s):  
Douglas R. W. Wylie ◽  
Barrie J. Frost

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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