Neural Organization From the Superior Colliculus to Motoneurons in the Horizontal Oculomotor System of the Cat

1999 ◽  
Vol 81 (6) ◽  
pp. 2597-2611 ◽  
Author(s):  
Y. Izawa ◽  
Y. Sugiuchi ◽  
Y. Shinoda
Keyword(s):  
Superior Colliculus ◽  
Reticular Formation ◽  
Wheat Germ ◽  
Abducens Nerve ◽  
Vestibular Nuclei ◽  
Oculomotor System ◽  
Abducens Nucleus ◽  
Axon Terminals ◽  
Neural Organization ◽  
Premotor Neurons

Neural organization from the superior colliculus to motoneurons in the horizontal oculomotor system of the cat. The neural organization of the superior colliculus (SC) projection to horizontal ocular motoneurons was analyzed in anesthetized cats using intracellular recording and transneuronal labeling. Intracellular responses to SC stimulation were analyzed in lateral rectus (LR) and medial rectus (MR) motoneurons and internuclear neurons in the abducens nucleus (AINs). LR motoneurons and AINs received excitation from the contralateral SC and inhibition from the ipsilateral SC. The shortest excitation (0.9–1.9 ms) and inhibition (1.4–2.4 ms) were mainly disynaptic from the SC and were followed by tri- and polysynaptic responses evoked with increasing stimuli or intensity. All MR motoneurons received excitation from the ipsilateral SC, whereas none of them received any short-latency inhibition from the contralateral SC, but some received excitation. The latency of the ipsilateral excitation in MR motoneurons (1.7–2.8 ms) suggested that this excitation was trisynaptic via contralateral AINs, because conditioning SC stimulation spatially facilitated trisynaptic excitation from the ipsilateral vestibular nerve. To locate interneurons mediating the disynaptic SC inputs to LR motoneurons, last-order premotor neurons were labeled transneuronally after injecting wheat germ agglutinin–conjugated horseradish peroxidase into the abducens nerve, and tectoreticular axon terminals were labeled after injecting dextran-biotin into the ipsilateral or contralateral SC in the same preparations. Transneuronally labeled neurons were mainly distributed ipsilaterally in the paramedian pontine reticular formation (PPRF) rostral to retrogradely labeled LR motoneurons and the vestibular nuclei, and contralaterally in the paramedian pontomedullary reticular formation (PPMRF) caudomedial to the abducens nucleus and the vestibular nuclei. Among the last-order premotor neuron areas, orthogradely labeled tectoreticular axon terminals were observed only in the PPRF and the PPMRF contralateral to the injected SC and seemed to make direct contacts with many of the labeled last-order premotor neurons in the PPRF and the PPMRF. These morphological results confirmed that the main excitatory and inhibitory connections from the SC to LR motoneurons are disynaptic and that the PPRF neurons that receive tectoreticular axon terminals from the contralateral SC terminate on ipsilateral LR motoneurons, whereas the PPMRF neurons that receive tectoreticular axon terminals from the contralateral SC terminate on contralateral LR motoneurons.

Comparison of Saccade-Associated Neuronal Activity in the Primate Central Mesencephalic and Paramedian Pontine Reticular Formations

2007 ◽  
Vol 98 (2) ◽  
pp. 835-850 ◽  
Author(s):  
Jason A. Cromer ◽  
David M. Waitzman
Keyword(s):  
Reticular Formation ◽  
Motor Neurons ◽  
Oculomotor System ◽  
Mesencephalic Reticular Formation ◽  
Abducens Nucleus ◽  
Premotor Neurons ◽  
Saccade Velocity ◽  
Saccade Control ◽  
Decomposition Models ◽  
Component Velocity

The oculomotor system must convert signals representing the target of an intended eye movement into appropriate input to drive the individual extraocular muscles. Neural models propose that this transformation may involve either a decomposition of the intended eye displacement signal into horizontal and vertical components or an implicit process whereby component signals do not predominate until the level of the motor neurons. Thus decomposition models predict that premotor neurons should primarily encode component signals while implicit models predict encoding of off-cardinal optimal directions by premotor neurons. The central mesencephalic reticular formation (cMRF) and paramedian pontine reticular formation (PPRF) are two brain stem regions that likely participate in the development of motor activity since both structures are anatomically connected to nuclei that encode movement goal (superior colliculus) and generate horizontal eye movements (abducens nucleus). We compared cMRF and PPRF neurons and found they had similar relationships to saccade dynamics, latencies, and movement fields. Typically, the direction preference of these premotor neurons was horizontal, suggesting they were related to saccade components. To confirm this supposition, we studied the neurons during a series of oblique saccades that caused “component stretching” and thus allowed the vectorial (overall) saccade velocity to be dissociated from horizontal component velocity. The majority of cMRF and PPRF neurons encoded component velocity across all saccades, supporting decomposition models that suggest horizontal and vertical signals are generated before the level of the motoneurons. However, we also found novel vectorial eye velocity encoding neurons that may have important implications for saccade control.

Neural Organization of the Pathways From the Superior Colliculus to Trochlear Motoneurons

2007 ◽  
Vol 97 (5) ◽  
pp. 3696-3712 ◽  
Author(s):  
Yoshiko Izawa ◽  
Yuriko Sugiuchi ◽  
Yoshikazu Shinoda
Keyword(s):  
Superior Colliculus ◽  
Interstitial Nucleus Of Cajal ◽  
Saccadic System ◽  
Neural Organization ◽  
Premotor Neurons ◽  
Monosynaptic Inhibition ◽  
Disynaptic Inhibition ◽  
Forel's Field H ◽  
Stimulation Of ◽  
Monosynaptic Excitation

The neural organization of the pathways from the superior colliculus (SC) to trochlear motoneurons was analyzed in anesthetized cats using intracellular recording and transneuronal labeling techniques. Stimulation of the ipsilateral or contralateral SC evoked excitation and inhibition in trochlear motoneurons with latencies of 1.1–2.3 and 1.1–3.8 ms, respectively, suggesting that the earliest components of excitation and inhibition were disynaptic. A midline section between the two SCs revealed that ipsi- and contralateral SC stimulation evoked disynaptic excitation and inhibition in trochlear motoneurons, respectively. Premotor neurons labeled transneuronally after application of wheat germ agglutinin-conjugated horseradish peroxidase into the trochlear nerve were mainly distributed ipsilaterally in the Forel's field H (FFH) and bilaterally in the interstitial nucleus of Cajal (INC). Consequently, we investigated these two likely intermediaries between the SC and trochlear nucleus electrophysiologically. Stimulation of the FFH evoked ipsilateral mono- and disynaptic excitation and contralateral disynaptic inhibition in trochlear motoneurons. Preconditioning stimulation of the ipsilateral SC facilitated FFH-evoked monosynaptic excitation. Stimulation of the INC evoked ipsilateral monosynaptic excitation and inhibition, and contralateral monosynaptic inhibition in trochlear motoneurons. Preconditioning stimulation of the contralateral SC facilitated contralateral INC-evoked monosynaptic inhibition. These results revealed a reciprocal input pattern from the SCs to vertical ocular motoneurons in the saccadic system; trochlear motoneurons received disynaptic excitation from the ipsilateral SC via ipsilateral FFH neurons and disynaptic inhibition from the contralateral SC via contralateral INC neurons. These inhibitory INC neurons were considered to be a counterpart of inhibitory burst neurons in the horizontal saccadic system.

scholarly journals Removal of inhibition uncovers latent movement potential during preparation

2017 ◽  
Author(s):  
Uday K. Jagadisan ◽  
Neeraj J. Gandhi
Keyword(s):  
Superior Colliculus ◽  
Neural Activity ◽  
Motor System ◽  
Reaction Times ◽  
Motor Command ◽  
Oculomotor System ◽  
Movement Planning ◽  
Necessary Condition ◽  
Movement Initiation ◽  
Premotor Neurons

AbstractThe motor system prepares for movements well in advance of their execution. In the gaze control system, premotor neurons that produce a burst of activity for the movement are also active leading up to the saccade. The dynamics of preparatory neural activity have been well described by stochastic accumulator models, and variability in the accumulation dynamics has been shown to be correlated with reaction times of the eventual saccade, but it is unclear whether this activity is purely preparatory in nature or has features indicative of a hidden movement command. We explicitly tested whether preparatory neural activity in premotor neurons of the primate superior colliculus has “motor potential”. We removed inhibition on the saccadic system using reflex blinks, which turn off downstream gating, and found that saccades can be initiated before underlying activity reaches levels seen under normal conditions. Accumulating low-frequency activity was predictive of eye movement dynamics tens of milliseconds in advance of the actual saccade, indicating the presence of a latent movement command. We also show that reaching threshold is not a necessary condition for movement initiation, contrary to the postulates of accumulation-to-threshold models. The results bring into question extant models of saccade generation and support the possibility of a concurrent representation for movement preparation and generation.Significance StatementHow the brain plans for upcoming actions before deciding to initiate them is a central question in neuroscience. Popular theories suggest that movement planning and execution occur in serial stages, separated by a decision boundary in neural activity space (e.g., “threshold”), which needs to be crossed before the movement is executed. By removing inhibitory gating on the motor system, we show here that the activity required to initiate a saccade can be flexibly modulated. We also show that evolving activity during movement planning is a hidden motor command. The results have important implications for our understanding of how movements are generated, in addition to providing useful information for decoding movement intention based on planning-related activity.Impact StatementNon-invasive disinhibition of the oculomotor system shows that ongoing preparatory activity in the superior colliculus has movement-generating potential and need not rise to threshold in order to produce a saccade.

Trigeminal premotor neurons in the bulbar parvocellular reticular formation participating in induction of rhythmical activity of trigeminal motoneurons by repetitive stimulation of the cerebral cortex in the guinea pig

1993 ◽  
Vol 69 (2) ◽  
pp. 595-608 ◽  
Author(s):  
S. Nozaki ◽  
A. Iriki ◽  
Y. Nakamura
Keyword(s):  
Cerebral Cortex ◽  
Reticular Formation ◽  
Field Potential ◽  
Repetitive Stimulation ◽  
Motoneuron Pool ◽  
Postsynaptic Potential ◽  
Rhythmical Activity ◽  
Premotor Neurons ◽  
Trigeminal Motoneurons ◽  
Stimulation Of

1. Single-unit activity was recorded from neurons in the bulbar parvocellular reticular formation (PCRF) dorsal and dorsolateral to the gigantocellular reticular nucleus near its caudal boundary, and the roles of these reticular neurons in induction of rhythmical activity of trigeminal motoneurons by repetitive stimulation of the cerebral cortex (the cortical masticatory area, CMA) were studied in the paralyzed guinea pig anesthetized with urethan or with ketamine and chlorpromazine. 2. One hundred nine PCRF neurons were activated antidromically by microstimulation in either the masseter (MA) or anterior digastric (AD) motoneuron pool in the ipsilateral trigeminal motor nucleus, and orthodromically by stimulation in the contralateral CMA. Repetitive CMA stimulation induced rhythmical burst activity in these PCRF neurons in association with the rhythmical field potential in the contralateral AD motoneuron pool induced by the same CMA stimulation. The burst was synchronous with the rhythmical AD field potential in 81 neurons, 44 and 37 of which responded antidromically to stimulation in the MA and AD motoneuron pools, respectively. The remaining 28 neurons antidromically responded to stimulation in the MA motoneuron pool, and their burst corresponded in time with the period between successive AD field potentials. 3. Spike-triggered averaging of the intracellular potentials of MA and AD motoneurons (MNs) by simultaneously recorded spontaneous spikes of the PCRF neurons, which showed rhythmical burst responses during the jaw-opening phase to repetitive CMA stimulation, revealed a monosynaptic inhibitory postsynaptic potential in MA.MNs in 12 of 34 tested pairs and a monosynaptic excitatory postsynaptic potential (EPSP) in AD.MNs in 14 of 26 tested pairs. An EPSP was also found in MA.MNs after a monosynaptic latency from triggering spikes in 11 of 37 tested PCRF neurons that showed burst activity during the jaw-closing phase. 4. We conclude that both excitatory and inhibitory premotor neurons projecting to MA.MNs as well as excitatory premotor neurons projecting to AD.MNs are located in the PCRF, and that these premotor neurons relay the output of the central rhythm generator for rhythmical jaw movements in the medial bulbar reticular formation to trigeminal motoneurons, and thus participate in induction of rhythmical activities of trigeminal motoneurons by repetitive CMA stimulation.

Recruitment of a Head-Turning Synergy by Low-Frequency Activity in the Primate Superior Colliculus

2008 ◽  
Vol 100 (1) ◽  
pp. 397-411 ◽  
Author(s):  
Sam Rezvani ◽  
Brian D. Corneil
Keyword(s):  
Superior Colliculus ◽  
Low Frequency ◽  
Oculomotor System ◽  
Muscle Synergy ◽  
Emg Activity ◽  
Neck Muscle ◽  
Muscle Recruitment ◽  
Head Turning ◽  
Head Restraint ◽  
Reward Expectancy

Low-frequency activity within the oculomotor system helps bridge sensation and action. Given ocular stability, low-frequency activity sustained by some neurons within the intermediate and deep superior colliculus (dSC) is assumed to be separated from motor output. However, the dSC is an orienting structure and the influence of low-frequency dSC activity at other effectors remains untested. We studied this by simultaneously recording activity from saccade-related dSC neurons and electromyographic (EMG) activity from neck muscles that turn the head. Monkeys performed a gap-saccade paradigm with varying levels of reward expectancy. Despite head restraint and even for relatively small target eccentricities (≤10°), increasing reward expectancy for a given target increased the level of low-frequency activity on dSC neurons encoding saccades to the rewarded target and increased the recruitment of a neck muscle synergy that would turn the head toward the target. The magnitude of neck muscle recruitment correlated positively on a trial-by-trial basis with the level of low-frequency dSC activity, and such correlations were optimized when neck muscle activity was shifted about 20 ms later to account for delays in the tecto-reticulo-spinal pathway. Further, dSC activity discriminated about the side of target presentation approximately 11 ms earlier than neck EMG activity. Considered alongside neck EMG responses evoked causally by SC stimulation, our results are consistent with low-frequency dSC activity recruiting a head-turning synergy. Our results support a brain stem circuit wherein the magnitude of neck muscle recruitment reflects the difference in comparative low-frequency activation across both dSCs, perhaps because of mutually inhibitory interactions within downstream head premotor circuits.

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