scholarly journals Cerebellar complex spikes multiplex complementary behavioral information

PLoS Biology ◽  
2021 ◽  
Vol 19 (9) ◽  
pp. e3001400
Author(s):  
Akshay Markanday ◽  
Junya Inoue ◽  
Peter W. Dicke ◽  
Peter Thier

Purkinje cell (PC) discharge, the only output of cerebellar cortex, involves 2 types of action potentials, high-frequency simple spikes (SSs) and low-frequency complex spikes (CSs). While there is consensus that SSs convey information needed to optimize movement kinematics, the function of CSs, determined by the PC’s climbing fiber input, remains controversial. While initially thought to be specialized in reporting information on motor error for the subsequent amendment of behavior, CSs seem to contribute to other aspects of motor behavior as well. When faced with the bewildering diversity of findings and views unraveled by highly specific tasks, one may wonder if there is just one true function with all the other attributions wrong? Or is the diversity of findings a reflection of distinct pools of PCs, each processing specific streams of information conveyed by climbing fibers? With these questions in mind, we recorded CSs from the monkey oculomotor vermis deploying a repetitive saccade task that entailed sizable motor errors as well as small amplitude saccades, correcting them. We demonstrate that, in addition to carrying error-related information, CSs carry information on the metrics of both primary and small corrective saccades in a time-specific manner, with changes in CS firing probability coupled with changes in CS duration. Furthermore, we also found CS activity that seemed to predict the upcoming events. Hence PCs receive a multiplexed climbing fiber input that merges complementary streams of information on the behavior, separable by the recipient PC because they are staggered in time.

1989 ◽  
Vol 61 (4) ◽  
pp. 780-798 ◽  
Author(s):  
O. Hikosaka ◽  
M. Sakamoto ◽  
S. Usui

1. We recorded single cell activities in the caudate nucleus of the monkeys trained to perform a series of visuomotor tasks. In the first part of this paper, we summarize the types and locations of neurons in the monkey caudate nucleus. In the second part, we report the characteristics of neurons related to saccadic eye movements. 2. Neurons were classified into two types in terms of spontaneous discharge pattern. A majority of the neurons (2,287/2,559, 89%) had very low-frequency discharges (mostly less than 1 Hz). The rest (n = 272) showed irregular-tonic discharges (3-8 Hz) with broad spikes. 3. Of 2,559 neurons tested, 867 showed spike activity related to some aspects of the tasks; 502 neurons showed discharges in response to environmental changes outside, not in relation to, the tasks. None of the neurons responsive in or outside the tasks belonged to the irregular-tonic type. 4. The task-related activities were classified as: Saccade-related, Visual, Auditory, Cognitive, Fixation-related, and Reward-related. The activities detected outside the tasks were classified into: Visual, Auditory, Movement-related, Reward-related, and Other. Few neurons had both task-related and task-unrelated activities. 5. The locations of recorded neurons were determined using a coordinate system based on the anterior and posterior commissures. Task-related neurons were clustered longitudinally in the central part of the caudate. Neurons responsive outside the tasks were more widely distributed; specifically, auditory neurons were in the medial part, whereas movement-related neurons were in the lateral part. The irregular-tonic neurons were dispersed all over the caudate. 6. The monkey was trained to fixate on a spot of light on the screen and, when the spot moved, to follow it by making a saccade. A visually guided saccade occurred when the spot moved to another location without a time gap (saccade task). A memory-guided saccade occurred when the spot first disappeared and after a time gap reappeared at a fixed location (saccade with gap task). By delivering a cue stimulus while the monkey was fixating, a memory-guided saccade was elicited to a randomly chosen location (delayed saccade task).(ABSTRACT TRUNCATED AT 400 WORDS)


2018 ◽  
Vol 115 (38) ◽  
pp. E8987-E8995 ◽  
Author(s):  
Yoshiko Kojima ◽  
Robijanto Soetedjo

When movements become dysmetric, the resultant motor error induces a plastic change in the cerebellum to correct the movement, i.e., motor adaptation. Current evidence suggests that the error signal to the cerebellum is delivered by complex spikes originating in the inferior olive (IO). To prove a causal link between the IO error signal and motor adaptation, several studies blocked the IO, which, unfortunately, affected not only the adaptation but also the movement itself. We avoided this confound by inactivating the source of an error signal to the IO. Several studies implicate the superior colliculus (SC) as the source of the error signal to the IO for saccade adaptation. When we inactivated the SC, the metrics of the saccade to be adapted were unchanged, but saccade adaptation was impaired. Thus, an intact rostral SC is necessary for saccade adaptation. Our data provide experimental evidence for the cerebellar learning theory that requires an error signal to drive motor adaptation.


2005 ◽  
Vol 93 (2) ◽  
pp. 1042-1054 ◽  
Author(s):  
Michael Ariel

Responses of separate regions of rat cerebellar cortex (Cb) to inferior olive (IO) stimulation occur with the same latency despite large differences in climbing fiber (CF) lengths. Here, the olivocerebellar path of turtle was studied because its Cb is an unfoliated sheet on which measurements of latency and CF length can be made directly across its entire surface in vitro. During extracellular DC recordings at a given Cb position below the molecular layer, IO stimulation evoked a large negative field potential with a half-width duration of ∼6.5 ms. On this response were smaller oscillations similar to complex spikes. The stimulating electrode was moved to map the IO and the CF path from the brain stem to the Cb. The contralateral brain stem region that evoked these responses was tightly circumscribed within the medulla, lateral and deep to the obex. This response remained when the brain stem was bathed in solutions that blocked synaptic transmission. The Cb response to IO stimulation had a peak latency of ∼10 ms that was not dependent on the position of the recording electrode across the entire 8-mm rostrocaudal length of the Cb. However, for a constant Cb recording position, moving the stimulation across the midline to the ipsilateral brain stem and along the lateral wall of the fourth ventricle toward the peduncle did shorten the response latency. Therefore a synchronous Cb response to CF stimulation seems to be caused by changes in its conduction velocity within the entire cerebellar cortex but not within the brain stem.


2021 ◽  
Vol 15 ◽  
Author(s):  
Lea Hehenberger ◽  
Luka Batistic ◽  
Andreea I. Sburlea ◽  
Gernot R. Müller-Putz

Motor imagery is a popular technique employed as a motor rehabilitation tool, or to control assistive devices to substitute lost motor function. In both said areas of application, artificial somatosensory input helps to mirror the sensorimotor loop by providing kinesthetic feedback or guidance in a more intuitive fashion than via visual input. In this work, we study directional and movement-related information in electroencephalographic signals acquired during a visually guided center-out motor imagery task in two conditions, i.e., with and without additional somatosensory input in the form of vibrotactile guidance. Imagined movements to the right and forward could be discriminated in low-frequency electroencephalographic amplitudes with group level peak accuracies of 70% with vibrotactile guidance, and 67% without vibrotactile guidance. The peak accuracies with and without vibrotactile guidance were not significantly different. Furthermore, the motor imagery could be classified against a resting baseline with group level accuracies between 76 and 83%, using either low-frequency amplitude features or μ and β power spectral features. On average, accuracies were higher with vibrotactile guidance, while this difference was only significant in the latter set of features. Our findings suggest that directional information in low-frequency electroencephalographic amplitudes is retained in the presence of vibrotactile guidance. Moreover, they hint at an enhancing effect on motor-related μ and β spectral features when vibrotactile guidance is provided.


2000 ◽  
Author(s):  
Grzegorz Kawiecki

Abstract The purpose of this paper is to show the feasibility of applying neural networks and arrays of piezotransducers for condition monitoring of basic structural components. It is shown that simple neural networks can be used to interpret damage-related anomalies in signals transferred between elements of a piezotransducer array. These relatively low frequency signals in the 0 Hz–1 kHz range carry enough information to determine damage location and size with a reasonable accuracy. The feasibility of a neural network-based expert system for signal processing is shown using a simple closed-form model of a thin, homogeneous vibrating plate. A new type of a rosette piezotransducer is presented. This type of a piezotransducer can generate and sense complex strain fields containing more damage-related information.


2019 ◽  
Author(s):  
Gil Zur ◽  
Mati Joshua

AbstractThe challenge of spike sorting has been addressed by numerous electrophysiological studies. These methods tend to focus on the information conveyed by the high frequencies, but ignore the potentially informative signals at lower frequencies. Activation of Purkinje cells in the cerebellum by input from the climbing fibers results in a large amplitude dendritic spike concurrent with a high frequency burst known as a complex spike. Due to the variability in the high frequency component of complex spikes, previous methods have struggled to sort these complex spikes in an accurate and reliable way. However, complex spikes have a prominent extracellular low frequency signal generated by the input from the climbing fibers. We exploited this to improve complex spike sorting by applying Principal Component Analysis (PCA) on the low frequencies of the signal and show that the low frequency first PC achieves a better separation of the complex spikes from noise. The low frequency data are more effective in detecting events entering into the analysis, and therefore can be harnessed to analyze the data with a larger signal to noise ratio. These two advantages make our method more effective for complex spike sorting. Our characterization of the dendritic low frequency components of complex spikes can be applied in other studies to gain insights into processing in the cerebellum.


2010 ◽  
Vol 103 (1) ◽  
pp. 262-277 ◽  
Author(s):  
Kiyoshi Kurata

It has been suggested that the dorsal premotor cortex (PMd) may contribute to conditional motor behavior. Thus when a selection is instructed by arbitrary conditional cues, it is possible that the unilateral PMd affects behavior, regardless of which arm, contra- or ipsilateral, is to be used. We examined this possibility by recording neuronal activity and injecting muscimol into the caudal PMd (PMdc) of monkeys while they were performing a reaching task toward visuospatial targets with either the right or left arm, as instructed by low-frequency or high-frequency tone signals. Following the injection of a small amount of muscimol (1 μL; 5 μg/μL) into the unilateral PMdc, monkeys exhibited two major deficits in behavioral performance: 1) erroneous selection of the arm not indicated by the instruction (selection errors) and 2) no movement initiation in response to a visuospatial target cue serving as a trigger signal for reaching within the reaction time limit (movement initiation errors). Errors were observed following unilateral muscimol injection into both right and left PMdc, although selection errors occurred with significantly greater frequency in the arm contralateral to the injection site. By contrast, movement initiation errors were more commonly observed in left-arm trials, regardless of whether the right or left PMdc was inactivated. Notably, errors rarely occurred following a ventral PM muscimol injection. These results suggest that the left and right PMdc cooperate to transform conditional sensory cues into appropriate motor output and can affect both contra- and ipsilateral body movement.


2007 ◽  
Vol 97 (1) ◽  
pp. 701-714 ◽  
Author(s):  
Brian D. Corneil ◽  
Douglas P. Munoz ◽  
Etienne Olivier

Large, rapid gaze shifts necessitate intricate coordination of the eyes and head. Brief high-frequency bursts of activity within the intermediate and deeper layers of the superior colliculus (dSC) encode desired gaze shifts regardless of component movements of the eyes and head. However, it remains unclear whether low-frequency activity emitted by oculomotor neurons within the dSC and elsewhere has any role in eye-head gaze shifts. Here we test the hypothesis that such low-frequency activity contributes to eye-head coordination by selectively priming head premotor circuits. We exploited the capacity for short-duration (10 ms, 4 pulses) dSC stimulation to evoke neck muscle responses without compromising ocular stability, stimulating at various intervals of a “gap-saccade” task. Low-frequency neural activity in many oculomotor areas (including the dSC) is known to increase during the progression of the gap-saccade task. Stimulation was passed during either a fixation-interval while a central fixation point was illuminated, a 200-ms gap-interval between fixation point offset and target onset, or a movement-interval following target onset. In the two monkeys studied, the amplitude of evoked responses on multiple neck muscles tracked the known increases in low-frequency oculomotor activity during the gap-saccade task, being greater following stimulation passed at the end of the gap- versus the fixation-interval, and greater still when the location of stimulation during the movement interval coincided with the area of the dSC generating the ensuing saccade. In one of these monkeys, we obtained a more detailed timeline of how these results co-varied with low-frequency oculomotor activity by stimulating, across multiple trials, at different times within the fixation-, gap- and movement-intervals. Importantly, in both monkeys, baseline levels of neck EMG taken immediately prior to stimulation onset did not co-vary with the known pattern of low-frequency oculomotor activity up until the arrival of a transient burst associated with visual target onset. These baseline results demonstrate that any priming of the head premotor circuits occurs without affecting the output of neck muscle motoneurons, We conclude that low-frequency oculomotor activity primes head premotor circuits well in advance of gaze shift initiation, and in a manner distinct from its effects on the eye premotor circuits. Such distinctions presumably aid the temporal coordination of the eyes and head despite fundamentally different biomechanics.


2019 ◽  
Vol 121 (6) ◽  
pp. 2153-2162 ◽  
Author(s):  
Robijanto Soetedjo ◽  
Yoshiko Kojima ◽  
Albert F. Fuchs

The neuronal substrate underlying the learning of a sophisticated task has been difficult to study. However, the advent of a behavioral paradigm that deceives the saccadic system into thinking it is making an error has allowed the mechanisms of the adaptation that corrects this error to be revealed in a primate. The neural elements that fashion the command signal for the generation of accurate saccades involve subcortical structures in the brain stem and cerebellum. In this review we show that sites in both those structures also are involved with the gradual adaptation of saccade size, a form of motor learning. Pharmacological manipulation of the oculomotor vermis (lobules VIc and VII) impairs mechanisms that either increase or decrease saccade size during adaptation. The net saccade-related simple spike (SS) activity of its Purkinje cells is correlated with the changes in saccade characteristics that occur during adaptation. These changes in SS activity are driven by an error signal delivered over climbing fibers, which create complex spikes whose probability of occurrence reflects the motor error between the actual and desired saccade size. These climbing fibers originate in the part of the inferior olive that receives projections from the superior colliculus (SC). Disabling the SC prevents adaptation and stimulation of the SC just after a normal saccade produces a surrogate error signal that drives adaptation without an actual visual error. Therefore, the SC provides not only the initial command that generates a saccade, as shown by others, but also the error signal that ensures that saccades remain accurate.


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