BOLD temporal dynamics of rat superior colliculus and lateral geniculate nucleus following short duration visual stimulation

Background

The superior colliculus (SC) and lateral geniculate nucleus (LGN) are important subcortical structures for vision. Much of our understanding of vision was obtained using invasive and small field of view (FOV) techniques. In this study, we use non-invasive, large FOV blood oxygenation level-dependent (BOLD) fMRI to measure the SC and LGN''s response temporal dynamics following short duration (1 s) visual stimulation.

Methodology/Principal Findings

Experiments are performed at 7 tesla on Sprague Dawley rats stimulated in one eye with flashing light. Gradient-echo and spin-echo sequences are used to provide complementary information. An anatomical image is acquired from one rat after injection of monocrystalline iron oxide nanoparticles (MION), a blood vessel contrast agent. BOLD responses are concentrated in the contralateral SC and LGN. The SC BOLD signal measured with gradient-echo rises to 50% of maximum amplitude (PEAK) 0.2±0.2 s before the LGN signal (p<0.05). The LGN signal returns to 50% of PEAK 1.4±1.2 s before the SC signal (p<0.05). These results indicate the SC signal rises faster than the LGN signal but settles slower. Spin-echo results support these findings. The post-MION image shows the SC and LGN lie beneath large blood vessels. This subcortical vasculature is similar to that in the cortex, which also lies beneath large vessels. The LGN lies closer to the large vessels than much of the SC.

Conclusions/Significance

The differences in response timing between SC and LGN are very similar to those between deep and shallow cortical layers following electrical stimulation, which are related to depth-dependent blood vessel dilation rates. This combined with the similarities in vasculature between subcortex and cortex suggest the SC and LGN timing differences are also related to depth-dependent dilation rates. This study shows for the first time that BOLD responses in the rat SC and LGN following short duration visual stimulation are temporally different.     

Transthalamic conduction of visual impulses to the cortex and subcortical forebrain structures in turtles

The thalamic relays for the conduction of impulses arising during photic stimulation of the eyes and electrical stimulation of the tectum in the general cortex, hyperstriatum (the dorsal ventricular ridge), and the striatum proper were studied in the turtleEmys orbicularis. Acute experiments on immobilized animals showed that anodal polarization temporarily and destruction of n. rotundus irreversibly suppress the main negative wave of the responses to tectal stimulation and to flashes in the hyperstriatum, whereas the corresponding responses in the general cortex still persist. Polarization and destruction of the lateral thalamic region, including the lateral geniculate body, have the opposite effect: responses in the hyperstriatum to photic and tectal stimulation are virtually unchanged whereas those in the general cortex disappear, except their late components. Preceding single stimulation of the tectum or n. rotundus depresses responses in the hyperstriatum evoked by flashes. However, during stimulation of the lateral thalamic region, combined potentials and single unit responses appear in the hyperstriatum and interact with responses evoked by tectal stimulation. It is concluded that the main pathways in turtles which supply visual information to the general cortex and hyperstriatum differ: the former relay in the lateral thalamic region, the latter in n. rotundus, although some overlapping of their projections in the hyperstriatum and striatum is possible.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Leningrad. Translated from Neirofiziologiya, Vol. 9, No. 5, pp. 486–494, September–October, 1977.     

Saccades differentially modulate human LGN and V1 responses in the presence and absence of visual stimulation

Saccades occur several times each second in normal human vision. The visual image moves across the retina at high velocity during a saccade, yet no blurring of the visual scene is perceived . Active suppression of visual input may account for this perceptual continuity, but the neural mechanisms underlying such saccadic suppression remain unclear. We used functional MRI to specifically examine responses in the lateral geniculate nucleus (LGN) and primary visual cortex (V1) during saccades. Activity in both V1 and LGN was strongly modulated by saccades. Furthermore, this modulation depended on whether visual stimulation was present or absent. In complete darkness, saccades led to reliable signal increases in V1 and LGN, whereas in the presence of visual stimulation, saccades led to suppression of visually evoked responses. These findings represent unequivocal evidence for saccadic suppression in human LGN and retinotopically defined V1 and are consistent with the earliest site of saccadic suppression lying at or before V1.     

Changes in the activity of cells in the lateral geniculate nucleus by stimulation of the abducens nucleus area in rabbits

These investigations are aimed at studying the influence of the electrical stimulation of the VIth nucleus (abducens nucleus) on responses of lateral geniculate cells in rabbits. The animals were prepared in the usual fashion for single cell recordings at the lateral geniculate nucleus (LGN). Results show that: Electrical stimulation of the VIth nucleus always produced excitatory discharges whose latency varied from 30 to 400 ms. Interestingly, an electrical pulse applied to the abducens nucleus was capable of enhancing the light-evoked responses without altering the spontaneous rate of firing. It thus seems that the ascending influence of the VIth nucleus manifests itself when it coincides with light responses. Most cells which were sensitive to electrical activation of the abducens nucleus had their receptive field located peripherally (greater than 50 degrees). Histological reconstructions of recording electrode tracts suggest that cells which responded to electrical stimulation were located in a narrow band lying dorsally relative to the LGN. This area can be paralleled with the perigeniculate area observed in other mammals, although not identified in rabbits. It is suggested that these extraretinal impulses which reach the LGN and emerge from an area surrounding the VIth nucleus are associated with corollary discharges.     

Response properties of auditory activated cells in the occipital cortex of the blind mole rat: an electrophysiological study

Previous studies have demonstrated that despite its blindness, the subterranean blind mole rat (Spalax ehrenbergi) possesses a noticeable lateral geniculate nucleus and a typical cyto-architectural occipital cortex that are reciprocally connected. These two areas, as revealed by the metabolic tracer 2-deoxyglucose, are activated by auditory stimuli. Using single unit recordings, we show that about 57% of 325 cells located within the occipital cortex of anesthetized mole rats responded to at least one of the following auditory stimuli — white noise, pure tones, clicks, and amplitude modulated tones — with the latter two being the most effective. About 85% of cells driven by either contralateral or ipsilateral stimulation also responded to binaural stimulation; about 13% responded only to binaural stimulation; and 2% were driven exclusively by contralateral stimulation. Comparing responsiveness and response strength to these three modes of stimulation revealed a contralateral predominance. Mean latency (±SD) of ipsilateral and contralateral responses were 48.5±32.6 ms and 33.5±9.4 ms, respectively. Characteristic frequencies could be divided into two distinct subgroups ranging between 80 and 125 Hz and between 2,500 and 4,400 Hz, corresponding to the most intensive spectral components of the vibratory intraspecific communication signals and airborne vocalizations.Abbreviations BMF best modulation frequency - CF characteristic frequency - 2-DG 2-deoxyglucose - dLGN dorsal lateral geniculate nucleus - IC inferior colliculus - LGN lateral geniculate nucleus - OC occipital cortex - MTF modulation transfer function - SAM sinusoidally amplitude modulation - SC superior colliculus     

Influence of stimulation of the ocular muscles on the formation of visual responses of the lateral geniculate nucleus of the cat

In acute experiments on anesthetized cats it was shown that a single stimulation of the ocular muscles leads to unambiguous changes in the formation of the negative and positive components of the evoked response of the lateral geniculate nucleus to the presentation of a light stimulus. It was established that the nature of the muscular influences on the formation of these components of the evoked response of the lateral geniculate nucleus depends on the interval between conditioning muscular and test light stimuli.A. I. Karaev Institute of Physiology, Academy of Sciences of the Azerbaidzhan Republic, Baku. Translated from Neirofiziologiya, Vol. 23, No. 4, pp. 451–455, July–August, 1991.     

Optokinetic visual detection in the rat visual centres. A [14C]-2-deoxy-D-glucose study

Following forty-five min of binocular optokinetic stimulation (OKS) the autoradiographic maps of [14C]-2-deoxy-D-glucose (2DG) assumption of Long-Evans brain reveal clearly different patterns of optical density within visual centres. The most superficial layers of superior colliculus (SC) and a pretectal area including the nucleus of the optic tract (NOT) appear symmetrically, strongly darker than other visual structures such as lateral geniculate nucleus (LGN) and visual cortex (VC). Whereas the lack of metabolic increase at LGN and VC levels entirely confirms the non-involvement of the geniculo-cortical path in mediating the optomotor response following OKS in Rodents, it is postulated that the symmetrical increase of 2DG uptake even upon unidirectional OKS found even at pretectal level may represent a commissural transfer of visual information between homologous pretectal areas like the nuclei of the optic tract.     

Spatial resolution and nonlinearities of simple cells in the cat visual cortex measured with parallel line pairs

The spatial resolution of simple cells in cat visual cortex was measured by stimulation with pairs of 6 wide parallel light bars of various spacings. These double lines were moved across the receptive field and were taken as resolved if there was a 10% deflection between the double peak responses of cells. As a control, recordings were also made from several geniculate fibers. The smallest bar separations resolved by simple cells were larger than those which have been found for cells of the lateral geniculate nucleus (LGN), although the smallest cortical receptive field centers were as small as those of LGN-cells. The correlation between optimal resolving power of a cell and the width of its excitatory receptive field was much weaker in cortical simple cells than in LGN cells. In contrast to the LGN, the double line responses of most simple cells differ markedly from an additive superposition of two single line responses spaced according to the actual interline distance. As possible mechanisms underlying these nonlinearities three different connectivity schemes were investigated. Two of these models were based on receptive field concepts; the third one used intracortical circuits. Only the latter model could explain all the nonlinear effects seen in the neurophysiological experiments.     

Attenuation of the responses to repeated cholinergic interventions in the isolated dog atrium

In the isolated, blood-perfused canine right atrium, which was pretreated with propranolol, negative chronotropic and inotropic responses were evoked by stimulation of the intramural parasympathetic nerve fibers or by intra-arterial infusion of acetylcholine (ACh). Successive cholinergic interventions were applied; first, a conditioning intervention for 2 min was given, then this was followed by a test intervention for 4 min. The two interventions were separated by a rest period that varied from 15 to 240 s. The cardiac responses to the conditioning parasympathetic nerve stimulation quickly reached maximum levels, and then they "faded" or progressively diminished back toward the control level. The inotropic responses to the conditioning infusion of ACh (1 microgram/min) faded slightly but the chronotropic response did not. After the rest period, the test nerve stimulation evoked responses that also gradually faded with time. The maximal amplitude of the responses to the test stimuli were less than those to the conditioning stimuli. This reduction in the maximal amplitude of the cardiac responses to the test stimuli was more pronounced with high frequency stimulation (30 Hz) than with low frequency stimulation (5 Hz). The decrement was also more pronounced the shorter the rest period, and it was greater at earlier times after beginning the stimulation. Conversely, the maximal cardiac responses to test infusions of ACh were not appreciably less than the responses to the conditioning infusions. We conclude, therefore, that the diminution of the cardiac responses to the second test stimulation of the parasympathetic nerve fibers was mainly ascribable to a prejunctional rather than to a postjunctional mechanism.     

Dynamic encoding of natural luminance sequences by LGN bursts

In the lateral geniculate nucleus (LGN) of the thalamus, visual stimulation produces two distinct types of responses known as tonic and burst. Due to the dynamics of the T-type Ca ²⁺ channels involved in burst generation, the type of response evoked by a particular stimulus depends on the resting membrane potential, which is controlled by a network of modulatory connections from other brain areas. In this study, we use simulated responses to natural scene movies to describe how modulatory and stimulus-driven changes in LGN membrane potential interact to determine the luminance sequences that trigger burst responses. We find that at low resting potentials, when the T channels are de-inactivated and bursts are relatively frequent, an excitatory stimulus transient alone is sufficient to evoke a burst. However, to evoke a burst at high resting potentials, when the T channels are inactivated and bursts are relatively rare, prolonged inhibitory stimulation followed by an excitatory transient is required. We also observe evidence of these effects in vivo, where analysis of experimental recordings demonstrates that the luminance sequences that trigger bursts can vary dramatically with the overall burst percentage of the response. To characterize the functional consequences of the effects of resting potential on burst generation, we simulate LGN responses to different luminance sequences at a range of resting potentials with and without a mechanism for generating bursts. Using analysis based on signal detection theory, we show that bursts enhance detection of specific luminance sequences, ranging from the onset of excitatory sequences at low resting potentials to the offset of inhibitory sequences at high resting potentials. These results suggest a dynamic role for burst responses during visual processing that may change according to behavioral state.     

Monomodal convergence in the visual system of the alert cat

In chronic experiments on waking cats, the interaction between signals evoked by simultaneous stimulation of the lateral geniculate body (LGB) and pulvinar was mainly of occlusive type which was more pronounced in the visual than in the associative cortical area. Conditioning stimulation of LGB depressed the response to testing stimulation of the pulvinar at delays of 10 ms. Delays of 20-60 ms facilitated the response. At short delays between the stimuli, the conditioning pulvinar stimulation either did not change significantly the response to testing LGB stimulation or facilitated it. At long (80-200 ms) delays the same conditioning stimulation produced a depression of the response to the testing stimulation. The results obtained point to monomodal convergence in the system of the cat visual analyzer and also to a relative autonomy and predominance of the cortical input from LGB and to dependence of pulvinar input functioning on the degree of activation of the geniculo-cortical path.     

Interaction between visceral,somatic, and visual excitation on single neurons of the lateral geniculate body in cats

Acute experiments on cats anesthetized with pentobarbital and immobilized with diplacin or listhenon showed that visceral and somatic excitation may either facilitate or inhibit single unit activity in the lateral geniculate body evoked by photic stimulation. The manifestations of facilitation were: a modulatory type of enhancement of responses of silent neurons and neurons with a low level of spontaneous activity; enhancement of responses accompanied by simultaneous depression of spontaneous activity — a sensory contrast effect; enhancement of long-latency responses; appearance of a short-latency discharge from cells with an inhibitory response to light; the appearance of responses to light in neurons not responding previously or stabilization of responses in neurons responding to light irregularly. The inhibitory effects were manifested as immediate inhibition of responses, usually long-latency, and the filling up of the inhibitory pauses of the response to light with spikes, leading to a decrease in the signal-noise ratio. Somatic stimulation was more effective and more frequently evoked facilitation of responses to light (in 74% of cells). Similar results were obtained by stimulation of the mesencephalic reticular formation. Visceral excitation gave rise to facilitatory and inhibitory effects to an almost equal degree. The results show that excitation arising as the result of visceral and somatic stimulation affects the conduction of visual information in the neuronal system of the lateral geniculate body.Ivano-Frankovsk Medical Institute. Institute of Experimental Medicine, Academy of Medical Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 5, No. 6, pp. 636–643, November–December, 1973.     

Corticalization of two divisions of the visual system during vertebrate evolution

Data on the evolution of the visual system in vertebrate phylogeny are described. Visual projections are demonstrated in the telencephalon of cyclostomata (lampreys). The existence of a retino-thalamo-telencephalic pathway is demonstrated in elasmobranchs (skates). Two visual pathways are present in amphibians (frogs) and reptiles (turtles): retino-thalamo-telencephalic and retino-tecto-thalamo-telencephalic, and these overlap partly at the thalamic level in the lateral geniculate nucleus and completely in the telencephalon. In turtles the earliest visual and tectal impulses relay on their way to the telencephalon in the lateral geniculate body, and later impulses relay in the nucleus rotundus. In mammals (rats) visual tecto-cortical connections are seen; judging from the latent period of potentials arising in the visual cortex in response to stimulation of the superior colliculi these connections have one synaptic relay in the thalamus. The much shorter latent periods of visual evoked potentials recorded in the tectum of the monkey than in turtles (under identical chronic experimental conditions) confirm the views of morphologists on the progressive development of the tectal division of the visual system in vertebrate phylogeny. It is concluded that corticalization of both divisions of the visual system, i.e., the existence of telencephalic representation, appears in the early stages of vertebrate evolution.     

Saccadic eye movements modulate visual responses in the lateral geniculate nucleus

We studied the effects of saccadic eye movements on visual signaling in the primate lateral geniculate nucleus (LGN), the earliest stage of central visual processing. Visual responses were probed with spatially uniform flickering stimuli, so that retinal processing was uninfluenced by eye movements. Nonetheless, saccades had diverse effects, altering not only response strength but also the temporal and chromatic properties of the receptive field. Of these changes, the most prominent was a biphasic modulation of response strength, weak suppression followed by strong enhancement. Saccadic modulation was widespread, and affected both of the major processing streams in the LGN. Our results demonstrate that during natural viewing, thalamic response properties can vary dramatically, even over the course of a single fixation.     

Simultaneous Recording of Input and Output of Lateral Geniculate Neurones

TO understand the way in which the cat dorsal lateral geniculate nucleus (LGN) processes visual information it would be useful to know the number and type of retinal inputs to individual LGN neurones. Using electrical stimulation of the optic nerve Bishop et al.¹concluded that an impulse in a single optic nerve fibre is sufficient to excite a single LGN neurone. From the appearance of excitatory postsynaptic potentials (EPSPs) recorded essentially intracellularly, Creutzfeldt suggested that LGN neurones are driven by perhaps one² or a few³ retinal ganglion cells. Hubel and Wiesel⁴ proposed models of convergence of several retinal inputs on single LGN neurones based on analyses of receptive fields. Guillery⁵ produced anatomical evidence that some types of LGN neurones receive inputs from several different retinal fibres. Now we report direct observations which were made by recording simultaneously from single LGN neurones and from individual retinal ganglion cells which provided excitatory input to them. We shall not consider inhibitory influences, which are currently under study.     

Investigation of the stability of the potentials of the dorsal surface evoked by single and paired stimulations of the afferent nerve

In spinal and anesthetized cats in the region of the lumbosacral thickening we have recorded the potentials of the dorsal surface (PDS) in response to single or paired stimulation of the peripheral nerves. The intervals between the stimuli were 400, 100, and 20 msec. The recording was made once every 15 sec. We have constructed the histograms of the changes in the N₁-component recorded on conditioning and single stimulation. After conversion of the histograms for single responses we established agreement of the newly obtained histograms with those constructed for the conditioned responses. The coefficients of variance for both cases proved to be practically identical. In applying single stimulation of different strengths the coefficient of variance increased if the amplitude of the responses fell. The coefficient of variance for the low amplitude responses did not change on conditioning unlike that for the responses evoked by weak single stimulation. It has been shown that the confidence limits of change in the coefficient of variance for a confidence probability of 0.99 and 0.95 obtained in experiments with conditioning practically concur with the intervals for the single stimulation. It is concluded that presynaptic inhibition has no appreciable antifluctuation influences on the N₁-component of the PDS.Dnepropetrovsk State University. Translated from Neirofiziologiya, Vol. 2, No. 1, pp. 10–16, January–February, 1970.     

Control of conduction of afferent impulses across the lateral geniculate body by the side of the superior colliculus in alert rabbits

On alert rabbits it was shown that the stimulation of the superior colliculus inhibit visual evoked potential both of the ipsi- and contralateral geniculate body. Besides, the suppression of amplitude of the contralateral geniculate body's evoked potential was more significant than amplitude of the ipsilateral geniculate body's evoked potential. On the basis of the obtained results the authors suppose that superior colliculus is involved in organization of the effect of saccadic suppression of lateral geniculate body's visual responses.     

Electrophysiological maturation of neurons of the lateral geniculate nucleus after lesion of ponto-geniculo-occipital pathways in kittens

Bilateral mesencephalic lesions, which suppress the PGO activity in the lateral geniculate nucleus (LGN), were performed at two weeks of age in the kitten, and the effects on the electrophysiological development of this nucleus were analyzed at 6 weeks of age. The latencies of LGN cells after electrical stimulation of the optic chiasma were larger, and the number of the differentiated X cells was smaller than those of age paired controls. However, the response of the ganglion fibers was not modified. These results, compared to those obtained on 30 days old kittens, and on animals with a unilateral lesion, suggest that the suppression of PGO inputs to the LGN induced a delay in the electrophysiological maturation of this nucleus.     

Dendritic and sustained shifts in potential to electrical stimulation of the anuran tectal surface.

1. Recordings of dendritic potentials and sustained potential shifts (SPS) were made from the brain of immobilised frogs during surface tectal electrical stimulation. 2. Single pulses evoked dendritic responses; trains caused decay of dendritic responses on the background of the evoked SPS. 3. The tectal surface SPS declined with distance from the stimulating electrode. 4. The negative surface SPS declined with tectal depth to ca 300 microns, then reversed polarity and increased in amplitude with depth up to 700 microns.