In this article, we present a neural model of saccade initiation based on competitive integration of planned and reactive saccade decision signals in the intermediate layer of the superior colliculus. 
Neurons in the superficial gray layer (SGS) of the superior colliculus receive visual input and excite intermediate layer (SGI) neurons that play a critical role in initiating rapid orienting movements of the eyes, called saccades.
Some models propose that the spatial and temporal distributions of premotor activity in the intermediate layer of the superior colliculus are shaped by neuronal ensembles that give rise to local excitatory and distant inhibitory connections. We used in vitro photostimulation and whole-cell patch-clamp recording to test these models by measuring the spatial extent of synaptic interactions within the rat intermediate layer. Uncaging glutamate over whole-cell patch-clamped cells in the intermediate layer elicited long-lasting inward currents, resulting from direct activation of glutamate receptors expressed by the cells, and brief synaptic currents evoked by activation of presynaptic neurons. Large responses were commonly evoked by stimuli within 200 microm of the soma in the intermediate layer; smaller responses could occasionally be evoked from sites as distant as 500 microm.
Previously we classified randomly sampled neurons in the intermediate layer (SI) of the rat superior colliculus (SC) into six subclasses according to their firing responses to depolarizing current pulses and five subclasses based on their morphological properties in slice preparations.
By extracellular recording in intermediate layer 7 of the caudolateral tectum, we have discovered electrical activity driven by visual stimulation in the monocular visual field of the ipsilateral eye.
To examine the role of competitive and cooperative neural interactions within the intermediate layer of superior colliculus (SC), we elevated the basal SC neuronal activity by locally injecting a cholinergic agonist nicotine and analyzed its effects on saccade performance.
The medial intermediate division received projections from the intermediate layer of the superior colliculus and the lateral and interpositus posterior cerebellar nuclei, and projected to the intermediate layer of the superior colliculus, the periaqueductal gray of midbrain, and the intralaminar nuclei. The lateral intermediate divisions received projections from the pretectum, the intermediate layer of the superior colliculus, and the lateral and interpositus posterior cerebellar nuclei, and projected to the pretectum, superficial layers of the superior colliculus, and the pulvinar.
SGI neurons differed in their input from SGS and SO; neurons in the middle of the intermediate layer (SGIb) were less likely to respond to visual layer photostimulation than were those in sublayers just above and below them.
Here we show that a distinct type of neuron in the intermediate layer of the superior colliculus, the visuomotor neuron, which is known to be centrally involved in the preparation of saccades, is also active during covert shifts of attention..
By in vitro experiments we clarified that cholinergic inputs to the intermediate layer of the superior colliculus, presumably originating from the PPTN, facilitate generation of its motor outputs for the initiation of saccades.
To test its imputed role in spatial analyses, we used a battery of four spatial tasks combined with unilateral and bilateral cooling deactivation of the upper and intermediate layers of the superior colliculus. Unilateral cooling deactivation of both the superficial and intermediate layers induced a profound contralateral neglect of the auditory stimulus. Overall, unilateral SC deactivation results show that the upper and intermediate layers of the SC contribute in different ways to guiding behavioral responses to visual and auditory stimuli cues.
It is well known that the intermediate layer (SGI) of the mammalian superior colliculus (SC) receives cholinergic inputs originating from the pedunculopontine tegmental nucleus (PPTN).
In addition, the cholinergic input to the intermediate layer lowers the threshold for the bursting response and facilitates the transmission through the interlaminar connection via activation of nicotinic receptors.
The principal subcortical connections of area 7m were with the dorsal portion of the ventrolateral thalamic (VLc) nucleus, lateral posterior thalamic nucleus, lateral pulvinar, caudal mediodorsal thalamic nucleus and medial pulvinar, central lateral, central superior lateral, and central inferior intralaminar thalamic nuclei, dorsolateral caudate nucleus and putamen, middle region of the claustrum, nucleus of the diagonal band, zona incerta, pregeniculate nucleus, anterior and posterior pretectal nuclei, intermediate layer of the superior colliculus, nucleus of Darkschewitsch and dorsomedial parvicellular red nucleus (macaque cases only), dorsal, dorsolateral and lateral basilar pontine nuclei, nucleus reticularis tegmenti pontis, locus ceruleus, and superior central nucleus.
In each of these cases, the activity patterns of "neurons" within the model closely resemble actual cell behavior in the intermediate layer of the SC.
We investigated the electrophysiological properties of transient outward currents (TOCs) in neurons with different firing patterns, regular-spiking, fast-spiking and late-spiking neurons, in the intermediate layer (SGI) of the superior colliculus using the whole-cell patch clamp technique in slice preparations obtained from young rats (post-natal days 17-22).
Nor was the stimulation effect due to the activation of superficial layer visual neurons rather than the intermediate layers of the SC because stimulation of the superficial layers produced effects opposite to those found with intermediate layer stimulation.
In vitro whole-cell patch-clamp methods were used to examine the contribution of one component of intracollicular circuitry, the superficial gray layer, to the generation of bursts of action potentials that occur in the intermediate layer and that command head and eye movements in vivo. Applying a single brief (0.5 ms) pulse of current to the superficial layer of rat collicular slices evoked prolonged bursts of excitatory postsynaptic currents (EPSCs) in the cells of the intermediate layer. To examine the contribution of neurons within the superficial layer to the production of these bursts, we determined how superficial neurons respond to the same current pulses that evoke bursts in the intermediate layer. Nine of these 19 neurons were wide- and narrow-field vertical cells, which are known to project to the intermediate layer and could contribute to producing the EPSC bursts.
The activity of neurons located in the deep intermediate and adjacent deep layers (hereafter called just deep intermediate layer neurons) of the superior colliculus (SC) in monkeys was recorded during saccades interrupted by electrical stimulation of the brainstem omnipause neuron (OPN) region. During saccade interruption about 70% of deep intermediate layer neurons experienced a major reduction (30% or greater) in their activity, but discharge recovered quickly after the termination of the stimulation as the eyes resumed their movement to finish the saccade on the target. Therefore, the pattern of activity recorded in most of the deep intermediate layer neurons during interrupted saccades qualitatively resembled that previously reported for the saccade-related burst neurons which tend to be located more dorsally in the intermediate layer. Because all the more dorsally located burst neurons and the majority of our deep intermediate layer neurons show a total or major suppression in their discharge during interrupted saccades, it seems unlikely that the colliculus by itself could maintain an accurate memory of the desired saccadic goal or the remaining dynamic motor error required to account for the accuracy of the resumed movement which occurs following the interruption.
Although these cell types were found in all three layers of the SC, the majority of tonic theta-ON cells were recorded in the intermediate layer, and the tonic theta-OFF cells were dispersed evenly between the intermediate layer and the deep layer of the SC.
To clarify the role of cholinergic inputs to the intermediate layer of the superior colliculus (SC), we examined the effect of microinjection of nicotine into the SC on visually guided saccades in macaque monkeys.
To begin characterizing the neural elements underlying the dynamic properties of local circuits in the mammalian superior colliculus (SC), electrophysiological and morphological properties of individual neurons in the intermediate layer [ stratum griseum intermediale (SGI)] were investigated using whole cell patch-clamp recording and intracellular staining with biocytin in slice preparations from young (17-22 days old) and adult rats (7-8 wk old).
Excitatory synaptic responses, which reversed at membrane potentials near 0 mV, could be evoked by uncaging glutamate anywhere within 75 microm of an intermediate layer neuron. Our results indicate the presence of extensive local excitatory circuits in the intermediate layer of the superior colliculus and support the hypothesis that such intrinsic circuitry contributes to the development of presaccadic command bursts..
Intrinsic circuit of the superior colliculus (SC), in particular the pathway from the optic tract (OT) to neurons in the intermediate layer (SGI), was investigated by whole-cell patch-clamp recording in slice preparations obtained from 17- to 24-d-old rats.
Finally, severing the superficial layers from the slice had no effect on intermediate layer responses to intrinsic stimulation.
We examined synaptic transmission between these layers in vitro by stimulating the superficial layer while using whole-cell patch-clamp methods to measure the responses of intermediate layer neurons. Our results indicate the presence of functional connections between the superficial and intermediate layers and show that such connections could play a significant role in the generation of visually guided saccades..
Among 108 neurons recorded in the intermediate layer, 13 were of a visuomotor type, 15 were of a mnemonic motor type, and 13 were of an attention type.
The phasic component was characterized by a movement field resembling that seen in a typical intermediate layer neurone.
On the other hand, the medial portion of the prestriate cortex and caudal OAa and PGa targeted the superficial and intermediate laminae, i.e., SZ, SGS, SO, and stratum griseum intermediale (SGI), whereas caudal area POa projected primarily to the intermediate layer SGI.
The intermediate layer cells were always arranged in a single continuous layer, but in young animals they overlapped extensively with one another toward their edges whereas in the oldest animals they became extremely flat and non-overlapping. The inner layer included an outer tier of cells with their bases adhering to the intermediate layer, and an inner tier of cells detached from both the intermediate layer and the basal lamina overlying the brain parenchyma.
Because LIP projects strongly to the intermediate layers of the superior colliculus, we sought to demonstrate similar predictive responses in the monkey colliculus. We studied the behavior of 90 visually responsive neurons in the superficial and intermediate layers of the superior colliculus of two rhesus monkeys (Macaca mulatta) when visual stimuli or the locations of remembered stimuli were brought into their receptive fields by a saccade. Thirty percent (18/60) of intermediate layer visuomovement cells responded predictively before a saccade outside the movement field of the neuron when that saccade would bring the location of a stimulus into the receptive field. These neurons were located in the deeper parts of the intermediate layers and had relatively larger receptive fields and movement fields than the cells at the top of the intermediate layers. The visual response of neurons in the intermediate layers of the colliculus is suppressed during the saccade itself. Three neurons in the intermediate layers responded tonically from stimulus appearance to saccade without a presaccadic burst.
Every LM sector receives abundant projections from the polymodal sylvian anterior cortical area, the reticular thalamic nucleus, and the stratum opticum and intermediate layer of the superior colliculus.
We focused our study on the superficial gray layer, the intermediate layer, and the deep layers of the superior colliculus, the periaqueductal gray matter (PAGM), and the medial intercollicular region.
Although more TST somata are usually found in the intermediate layer, there are no useful relationships for predicting the number in one layer given the number in the other.
Small cells in the intermediate layer and giant cells in the deep layers of the superior colliculus were densely cabp(+).
While the heaviest anterogradely labeled ascending projections were observed to the contralateral ventral posterolateral nucleus of the thalamus, pars oralis (VPLo), efferent projections were also observed to the contralateral ventrolateral thalamic nucleus (VLc) and central lateral (CL) nucleus of the thalamic intralaminar complex, magnocellular (and to a lesser extent parvicellular) red nucleus, nucleus of Darkschewitsch, zona incerta, nucleus of the posterior commissure, lateral intermediate layer and deep layer of the superior colliculus, dorsolateral periaqueductal gray, contralateral nucleus reticularis tegmenti pontis and basilar pontine nuclei (especially dorsal and peduncular), and dorsal (DAO) and medial (MAO) accessory olivary nuclei, ipsilateral lateral (external) cuneate nucleus (LCN) and lateral reticular nucleus (LRN), and to a lesser extent the caudal medial vestibular nucleus (MVN) and caudal nucleus prepositus hypoglossi (NPH), and dorsal medullary raphe.
Lesser projections were observed to the intermediate layer of the superior colliculus, nucleus of the posterior commissure, and prerubral field.
By stimulation of the deep or intermediate layer of the SC, upward augmenting neurons (ANs) and one long-lead downward burst neuron (BN) were found to be activated monosynaptically, while medium-lead BNs were activated disynaptically.
Cells in its intermediate layer show a burst of spikes before saccades to the contralateral disc.
Eye movements with deviation toward the upward or contralateral side were elicited by electrical stimulation in the intermediate layer of the superior colliculus.
In addition, a patchy distribution of HRP-WGA or of radioactivity was found in the intermediate layer of the superior colliculus. Nigral projections to the intermediate layer of the superior colliculus were visualized over the whole mediocaudal and laterorostral extent when [ 14C]amino acids were injected into the rostral part of the SNR.
Future olfactory bulb and tubercle possess an intermediate layer.
By contrast the injection of kainic acid into the colliculus leaves the intermediate layer lattice intact while causing a local reduction in the superficial layer. Thus, it is concluded that the lattice in the intermediate layers is mainly dependent on afferents from the laterodorsal tegmental and pedunculopontine nuclei while the sheet in the superficial layers is mainly dependent on intrinsic cells..
In other instances, the afferent-fiber clusters seemed to be arranged in the acetylcholinesterase-poor parts of the intermediate layer in a fashion independent of, but not significantly overlapping, the acetylcholinesterase-positive patches.
Major afferent projections to the vPRN arise from the ipsilateral nucleus of Darkschewitsch and the intermediate layer of the contralateral superior colliculus.
Injections into the dorsal cMRF, at sites where small saccades were induced, caused labelling of cells in the rostral intermediate layer of SC. Injections into the ventral cMRF, at points where large saccades were elicited, caused labelling of cells in the caudal intermediate layer of SC. We interpret these findings to indicate that the intermediate layers of SC send axonal projections to the horizontal eye movement region of the MRF in a topographic fashion. The projection from the intermediate layer is organized so that regions in SC and cMRF related to small or to large eye movements are interconnected.
More moderate projections go to the medial division of the periaqueductal gray (PAGm), the cuneiform nucleus (CF), the mesencephalic reticular formation (MRF), lateral part of the deep layer of the superior colliculus (SP) and magnocellular medial geniculate nucleus (GMmc), while scattered spinal fibers are present in the dorsal part of the periaqueductal gray (PAGd), the external inferior collicular nucleus (IX), the intermediate layer of the superior colliculus (SI), the lateral part of the red nucleus (NR) and in the Edinger-Westphal portion of the oculomotor nucleus (3).
Most of them were located in the lateral site of the profound layer, a few in the lateral site of the intermediate layer. The mean first-spike latency of the intermediate layer neurons (7.2 ms) elicited by electrical stimulation of the periodontal ligament was shorter than that of the profound-layer neurons (13.8 ms).
On ED 15 a lamination typical for embyronic CNS with ventricular, subventricular, intermediate layers and stratum zonale can be observed in the area of presumptive colliculus superior. During early prenatal development, cells which originate on one single day can autoradiographically be demonstrated in different cell layers and particularly over the whole width of the intermediate layer, while towards the end of gestation time of cell origin and location inside the mesencephalic roofs are closely correlated: cells that originate on ED 13 can be found predominantly in deeper cell layers (stratum griseum profundum, lower stratum griseum intermedium), while cells originating on EDs 15 and 17 are on ED 21 situated in the upper cell layers (upper stratum griseum intermedium, stratum griseum superficiale).
We investigated the characteristics of cells in the intermediate layers of the superior colliculus that increase their rate of discharge before saccadic eye movements. The onset of the cell discharge led the eye movement by less time and the duration of the discharge was shorter as the cell was located closer to the dorsal edge of the intermediate layers. A new type of eye movement-related cell has been found which usually lies at the border between the superficial and intermediate layers. A vigorous discharge of these cells before an eye movement was dependent on the presence of a visual target; the cells seemed to combine the visual input of superficial layer cells and the movement-related input of the intermediate layer cells.
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