GABAergic and Glutamatergic Modulation of Spontaneous and Motor-Cortex-Evoked Complex Spike Activity

2002 ◽  
Vol 87 (4) ◽  
pp. 1993-2008 ◽  
Author(s):  
Eric J. Lang
Keyword(s):  
Motor Cortex ◽  
Banding Pattern ◽  
Spike Activity ◽  
Afferent Input ◽  
Excitatory Input ◽  
Relative Strength ◽  
Spike Synchrony ◽  
Complex Spike ◽  
Electrotonic Coupling ◽  
Inferior Olivary

Olivocerebellar activity is organized such that synchronous complex spikes occur primarily among Purkinje cells located within the same parasagittally oriented strip of cortex. Previous findings have shown that this synchrony distribution is modulated by the release of GABA and glutamate within the inferior olive, which probably act by controlling the efficacy of the electrotonic coupling between olivary neurons. The relative strengths of these two neurotransmitters in modulating the patterns of synchrony were compared by obtaining multiple electrode recordings of spontaneous crus 2a complex spike activity during intraolivary injection of solutions containing a GABAA (picrotoxin) and/or AMPA [1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide disodium (NBQX)] receptor antagonist. Injection of either antagonist led to increased synchrony between cells located within the same parasagittally oriented ≈250-μm-wide cortical strip. Picrotoxin also increased complex spike synchrony among cells located in different cortical strips, leading to a less prominent banding pattern, whereas injections of NBQX tended to decrease complex spike synchrony among such cells, enhancing the banding pattern. The relative strength of these two classes of olivary afferents was assessed by first injecting one of the antagonists alone and then in combination with the other. The enhanced banding pattern of complex spike synchrony following injection of NBQX alone remained during the subsequent combined injection of both antagonists. Furthermore, the widespread synchronization of complex spike activity following injection of picrotoxin alone was partially or completely reversed by combined injection of picrotoxin and NBQX. Changes in the climbing fiber reflex induced by the intraolivary injections paralleled the changes observed for spontaneous complex spike activity, indicating that the effects of picrotoxin and NBQX on the synchrony distribution reflect changes in the pattern of effective coupling of inferior olivary neurons and demonstrating that synchronous complex spike activity does not require simultaneous excitatory input to olivary cells. Finally the pattern of synchrony during motor cortical stimulation was examined. It was found that the patterns of synchrony for motor-cortex-evoked complex spike activity were similar to those of spontaneous activity, indicating an important role for electrotonic coupling in determining the response of the olivocerebellar system to afferent input. Moreover, intraolivary injections of picrotoxin increased the spatial distribution of the evoked response. In sum, the results provide evidence for the hypothesis that electrotonic coupling of inferior olivary neurons via gap junctions is the mechanism underlying complex spike synchrony and that this coupling plays an important role in determining the responses of the olivocerebellar system to synaptic input.

Complex Spike Activity in the Flocculus Signals More than the Eye Can See

2002 ◽  
Vol 978 (1 THE CEREBELLU) ◽  
pp. 232-236 ◽  
Author(s):  
J. I. SIMPSON ◽  
T. BELTON ◽  
M. SUH ◽  
B. WINKELMAN
Keyword(s):  
Spike Activity ◽  
Complex Spike

scholarly journals Generation and Propagation of Subthreshold Waves in a Network of Inferior Olivary Neurons

2002 ◽  
Vol 87 (6) ◽  
pp. 3059-3069 ◽  
Author(s):  
Anna Devor ◽  
Yosef Yarom
Keyword(s):  
Optical Imaging ◽  
Phase Difference ◽  
Maximum Amplitude ◽  
Nmda Receptor Antagonist ◽  
Oscillatory Activity ◽  
Electrotonic Coupling ◽  
Cell Pair ◽  
Subthreshold Oscillations ◽  
High Level ◽  
Inferior Olivary

The cells of the inferior olivary (IO) nucleus generate a large repertoire of electrical signals, among them subthreshold oscillations of the membrane potential (STO). To date, subthreshold oscillations have been studied at the level of single-cell recordings, from which network properties were inferred. In this study we used whole cell patch recordings and optical imaging to address the following issues: 1) synchrony of STO in neighboring neurons; 2) stability of the oscillatory activity in the temporal and spatial domain; and 3) the size of the oscillating network. Recordings were made from 126 pairs of IO neurons in 13- to 30-day-old rats. An additional 262 neurons were recorded individually. The frequency of STO varied from 0.8 to 8.6 Hz. The frequency distribution revealed two subpopulations with peaks at about 3 and 6 Hz. The maximum amplitude among the cells varied from 2 to 25 mV. Oscillations in most neurons showed ongoing modulations in both frequency and amplitude. These modulations were largely abolished following bath application of 40 μM 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX), a competitive non– N-methyl-d-aspartate (non-NMDA) receptor antagonist, suggesting that they were caused by glutamatergic action. In 35 of 61 recorded pairs at least one neuron exhibited STO permitting us to compare frequency and phase relations. In 22 pairs there was coherent activity with zero phase difference between oscillations in the 2 cells. In these pairs, frequency and amplitude modulation occurred simultaneously in both neurons. Electrotonic coupling was tested in 13 pairs, that had coherent STO, and it was detected in 12. An additional seven pairs showed coherent oscillations but with a phase difference of 20–50 ms. Electrotonic coupling was observed in three of these pairs. Electrotonic coupling was also observed in two of five pairs in which only one neuron oscillated. No coupling was detected in one pair where both neurons oscillated but at different frequencies. Optical imaging using a voltage-sensitive dye (RH 414) was performed on 40 IO slices using an array of 128 photodiodes. Patches of oscillatory activity were observed in 10 slices. Among them six showed spontaneous oscillations, and four exhibited oscillations following extracellular stimulation. In agreement with cell pair recording, optical imaging demonstrated phase-shifted activity in the form of propagating waves of activity within an oscillating patch. We conclude that 1) STO exhibit ongoing modulations of frequency and amplitude that are probably caused by extrinsic inputs to the IO nucleus; 2) electrotonically coupled neurons show a high level of STO synchrony; and 3) the oscillatory activity can propagate within a network of coupled olivary neurons.

scholarly journals Patterns of Spontaneous Purkinje Cell Complex Spike Activity in the Awake Rat

1999 ◽  
Vol 19 (7) ◽  
pp. 2728-2739 ◽  
Author(s):  
Eric J. Lang ◽  
Izumi Sugihara ◽  
John P. Welsh ◽  
Rodolfo Llinás
Keyword(s):  
Purkinje Cell ◽  
Spike Activity ◽  
Cell Complex ◽  
Complex Spike ◽  
Awake Rat

Electrotonic Coupling in the Inferior Olivary Nucleus Revealed by Simultaneous Double Patch Recordings

2002 ◽  
Vol 87 (6) ◽  
pp. 3048-3058 ◽  
Author(s):  
Anna Devor ◽  
Yosef Yarom
Keyword(s):  
Coupling Coefficient ◽  
Direct Calculation ◽  
Physiological Data ◽  
Inferior Olivary Nucleus ◽  
Potential Oscillations ◽  
Electrotonic Coupling ◽  
Cell Pair ◽  
Coupling Resistance ◽  
The Difference ◽  
Inferior Olivary

Electrotonic coupling in the inferior olivary (IO) nucleus is assumed to play a crucial role in generating the subthreshold membrane potential oscillations in olivary neurons and in synchronizing climbing fiber input into the cerebellar cortex. We studied the strength and spatial distribution of the coupling by simultaneous double patch recordings from olivary neurons in the brain slice preparation. Electrotonic coupling was observed in 50% of the cell pairs. The coupling coefficient ( CC), defined as the ratio between voltage responses of the post- and the prejunctional cell, varied between 0.002 and 0.17; most of the pairs were weakly coupled. In more than 75% of the pairs, the CCwas <0.05. The coupling resistance varied between 0.7 to 19.8 GΩ, and 68% of the values fell between 0.7 to 8 GΩ. The difference between the coupling coefficient measured on stimulation of cell 1 or cell 2 of a coupled pair was 27 ± 16%. Direct calculation of the coupling resistance revealed an asymmetry of 24 ± 12%, suggesting a directional preference of coupling. The coupling was voltage independent, although depolarization of either the pre- or the postjunctional neuron reduced the CC. The chance of a cell pair being coupled was 80% in immediate neighboring cells, but dropped to about 30% at a distance of 40 μm. No coupled pairs were observed at distances larger than 70 μm. In 52% of staining experiments neurobiotin injection into an olivary neuron produced indirect labeling of 1–11 nearby cells with an average of 3.8 ± 2.9. All indirectly labeled cells were found in, or immediately adjacent, to the dendritic field of the directly stained neuron. Two distinct morphological types of olivary neurons, “curly” and “straight” cells, were found. In each case all neurons stained indirectly by dye passage through gap junctions belonged to the same type. Using the physiological data we estimated that each olivary neuron is directly coupled to about 50 neurons. Since somatic recordings may not reveal coupling through remote dendrites, we conclude that each neuron is directly connected to ≥50 neurons forming two distinct networks of curly and straight cells.

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

1995 ◽  
Vol 73 (4) ◽  
pp. 1329-1340 ◽  
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)

Functional properties of single neurons in the face primary motor cortex of the primate. II. Relations with trained orofacial motor behavior

1992 ◽  
Vol 67 (3) ◽  
pp. 759-774 ◽  
Author(s):  
G. M. Murray ◽  
B. J. Sessle
Keyword(s):  
Motor Cortex ◽  
Cortical Neurons ◽  
Primary Motor Cortex ◽  
Motor Behavior ◽  
Afferent Input ◽  
Single Neurons ◽  
Tongue Protrusion ◽  
Input And Output ◽  
The Face ◽  
Tongue Movements

1. The previous paper has described in detail the input and output features of single neurons located at sites within primate face motor cortex from which intracortical microstimulation (ICMS, less than or equal to 20 microA) evoked tongue movements at the lowest threshold ("tongue-MI" sites); for comparative purposes, we also reported on the input and output features of a smaller number of neurons recorded at sites from which ICMS could evoke jaw movements ("jaw-MI" sites), facial movements ("face-MI" sites), or, at a few sites, tongue movements and, at the same threshold intensity, either a jaw movement or a facial movement. 2. Our findings of an extensive and diverse representation of sites within face motor cortex of monkeys for the generation of elemental components of tongue movement, and the relatively few sites from which jaw-closing movements could be evoked, were consistent with our recent observations that reversible, cooling-induced inactivation of the face motor cortex severely impaired the performance by monkeys of a tongue-protrusion task but had only relatively minor effects on the performance of a biting task. In an attempt to establish a neuronal correlate for these different behavioral relations, the present study has documented the task-related activities of those single neurons that were characterized in the previous paper in terms of afferent input and ICMS-defined output features. 3. Each task required the development and maintenance by each monkey of a fixed force level for a minimum period of time to obtain a fruit-juice reward. During one or both of these tasks, we characterized the activities of 231 single face motor cortical neurons that were located at the above-mentioned ICMS-defined sites. Neurons were said to be related to a particular task if they showed statistically significant differences in firing rates during the task in comparison with a control pretrial period (PTP). 4. In tongue-MI, there was a significantly higher proportion of neurons (63% of 156 neurons tested) that were related to the tongue-protrusion task than to the biting task (15% of 65). However, in jaw-MI the proportion of neurons that were biting task-related (63% of 19) was significantly higher than the proportion related to the tongue-protrusion task (11% of 9); the proportion of biting task-related neurons at ICMS-defined jaw-closing sites was also higher than that at jaw-opening sites.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Isochrony in the olivocerebellar system underlies complex spike synchrony

2006 ◽  
Vol 573 (1) ◽  
pp. 277-279 ◽  
Author(s):  
Eric J. Lang ◽  
Rodolfo Llinás ◽  
Izumi Sugihara
Keyword(s):  
Spike Synchrony ◽  
Complex Spike

Effect of afferent input on motor cortex excitability during stroke recovery

2012 ◽  
Vol 123 (12) ◽  
pp. 2429-2436 ◽  
Author(s):  
Kristina Laaksonen ◽  
Erika Kirveskari ◽  
Jyrki P. Mäkelä ◽  
Markku Kaste ◽  
Satu Mustanoja ◽  
...  
Keyword(s):  
Motor Cortex ◽  
Afferent Input ◽  
Stroke Recovery ◽  
Motor Cortex Excitability
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