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.     

Characteristics of residual neurons during retrograde degeneration in the cat lateral geniculate body

The dynamics of structural and functional characteristics of residual neurons in the degenerating lateral geniculate body was studied in cats during the 4–12 months after division of all cortico-subcortical projection connections, including axons of relay cells of the lateral geniculate body [9]. Spontaneous and evoked activity of the residual cells, their number, and also the dimensions of the cell bodies were investigated. With lengthening of the postoperative period a decrease in the number of cells of the lateral geniculate body responding to photic stimulation and also destruction of their receptive fields were observed; 12 months after the operation the residual neurons of the lateral geniculate body lose their sensitivity to photic stimulation. Morphological investigation revealed a progressive reduction in the number of neurons in the degenerating lateral geniculate body and predominance of small neurons among them. The nature of interneuronal relations in the lateral geniculate body are discussed on the basis of the results.Research Institute of Experimental Medicine, Academy of Medical Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 9, No. 6, pp. 575–582, November–December, 1977.     

The effect of the superior colliculus on the function of the contralateral lateral geniculate body in the cat

In acute experiments on rats it was shown that stimulation of the superior colliculus [correction of upper bimounding] leads to the formation in the contralateral lateral geniculate [correction of external geniculated] body of a colliculus-geniculate response. The nature of the changes in a considerable degree is determined by the fact, to which neurones of the lateral geniculate [correction of external geniculated] body, the effect of contralateral superior colliculus [correction of upper bimounding] is addressed.     

Influence of the motor cortex on lateral geniculate responses evoked in the cat by contralateral superior colliculus stimulation

It is shown that in nembutal anesthetized cats, a single stimulation of motor cortex (MC) causes a response in lateral geniculate nucleus (LGN). The development of this response had a conditioning effect on the LGN response evoked by stimulation of the contralateral superior colliculus (SC), markedly inhibiting it. The degree of this inhibition depended on the time interval between the cortical conditioning stimulation and the tectal test stimulation. A single conditioning MC stimulation did not noticeably change the LGN responses evoked by a light stimulus, but markedly inhibited visual responses from deep SC layers (those regions which on stimulation gave rise to LGN responses). From the results, it is suggested that the MC monitors the execution of tectal influences on LGN function at the tectal level rather than the geniculate level, and it is precisely by this means that it regulates saccadic suppression of LGN function, in the realization of which, as presumed earlier, the SC takes part.A. I. Karaev Institute of Physiology, Azerbaijan Academy of Sciences, Baku. Translated from Neirofiziologiya, Vol. 24, No. 4, July–August 1992.     

Cytoplasmic organelles in neurons of the dorsal lateral geniculate nucleus of aged rats

The ultrastructural characteristics of the neurons containing complex convolutions have been studied in the dorsal lateral geniculate nucleus of the 31-month-old rat. Neurons were seen to contain oval or round dense bodies which were surrounded by a nuclear membrane and granular endoplasmic reticulum. Their perikarya showed rarely clusters of pleomorphic and small clear vesicles intermingled with a few larger vesicles of dense material. Dendrites occasionally exhibited intermediate forms between laminated bodies and complex convolutions. The significance of these features has been discussed.     

On the neurons and synapses of the lateral geniculate nucleus of the monkey,and the effects of eye enucleation

Summary Two neuron types are distinguished by electron microscopy in the lateral geniculate nucleus (LGN) of the monkey-a large cell (P cell) interpreted as a geniculostriate relay cell, and a small cell (I cell) interpreted as an inhibitory interneuron. The I cell, distinguished by its small size, infolded nucleus, small mitochondria, cilium and small granular bodies, forms about 10% of the total neuron population. It could not be determined whether this cell has an axon, but its dendrites, which contain aggregates of flattened vesicles, are thought to form a proportion of the F processes, profiles which are post-synaptic to the retinal (RLP) axons and presynaptic to the dendrites of the P cells. The small dark (RSD) axon terminals of unknown origin contact the dendrites of both cell types.After eye enucleation the P cells of the affected laminae of the LGN shrink and partially withdraw their dendrites from the neuropil. By 29 months' survival, they have only a narrow cytoplasmic rim around the nucleus. A necrotic process also occurs, affecting fine dendrites by 22 days and large profiles by 45 days, but it is not clear whether whole cells are destroyed by this process. At 45 days the I cells are commonly seen to form somatodendritic synapses. The appearance of these synapses is interpreted as the result of a withdrawal to the soma of the presynaptic dendrites.It is concluded that the I cells are probably inhibitory interneurons subject to excitation and presynaptic inhibition by the RLP and RSD axons, and a diagram is presented to demonstrate the possible significance of these connections for the transmission of information through the LGN.The author wishes to thank Dr. J. Campos-Ortega for much practical advice.     

The role of cortical feedback in the generation of the temporal receptive field responses of lateral geniculate nucleus neurons: a computational modelling study

The influence of cortical feedback on thalamic visual responses has been a source of much discussion in recent years. In this study we examine the possible role of cortical feedback in shaping the spatiotemporal receptive field (STRF) responses of thalamocortical (TC) cells in the lateral geniculate nucleus (LGN) of the thalamus. A population-based computational model of the thalamocortical network is used to generate a representation of the STRF response of LGN TC cells within the corticothalamic feedback circuit. The cortical feedback is shown to have little influence on the spatial response properties of the STRF organization. However, the model suggests that cortical feedback may play a key role in modifying the experimentally observed biphasic temporal response property of the STRF, that is, the reversal over time of the polarity of ON and OFF responses of the centre and surround of the receptive field, in particular accounting for the experimentally observed mismatch between retinal cells and TC cells in respect of the magnitude of the second (rebound) phase of the temporal response. The model results also show that this mismatch may result from an anti-phase corticothalamic feedback mechanism.     

Computation of responses to color and brightness differences of neurons in the rabbit lateral geniculate nucleus

Changes in activity of 51 neurons in the rabbit lateral geniculate nucleus evoked by the replacement of eight color and eight achromatic stimuli in pairs were analyzed. It was found that neurons displayed the earliest phasic (within 50-90 ms after the replacement) and tonic response components. The earliest component strongly correlated with differences between stimuli, whereas the tonic component depended on stimuli intensity. Analysis of phasic component revealed two neuronal populations: the first group of cells was specialized for stimuli differentiation only by their intensities, and, and the second group could measure differences in colors and intensities. Neuronal perceptual spaces were reconstructed using the average of the earliest response component as a measure of differences between stimuli. Spaces of 44 neurons (86%) were two-dimensional with brightness and darkness axes. Such neurons had the same structures of space for color and achromatic stimuli. Spaces of 7 neurons (14%) were four-dimensional with two chromatic and two achromatic axes. The structures of perceptual space reconstructed from neurons in the lateral geniculate nucleus were identical to the spaces calculated from the neurons in the primary visual cortex. The structure of the perceptual space reconstructed from neuronal spikes was also similar to space calculated from the N85 visual evoked potential component recorded under similar conditions and to another space reconstructed on the basis of rabbit's instrumental learning. This fact confirmed the general principle of vector coding in the visual system. The tonic component of the most of neurons in the lateral geniculate nucleus showed a linear correlation with changes in intensities, thereby these neurons could be characterized as pre-detectors for cortical selective detectors.     

Extended difference-of-Gaussians model incorporating cortical feedback for relay cells in the lateral geniculate nucleus of cat

A striking feature of the organization of the early visual pathway is the significant feedback from primary visual cortex to cells in the dorsal lateral geniculate nucleus (LGN). Despite numerous experimental and modeling studies, the functional role for this feedback remains elusive. We present a new firing-rate-based model for LGN relay cells in cat, explicitly accounting for thalamocortical loop effects. The established DOG model, here assumed to account for the spatial aspects of the feedforward processing of visual stimuli, is extended to incorporate the influence of thalamocortical loops including a full set of orientation-selective cortical cell populations. Assuming a phase-reversed push-pull arrangement of ON and OFF cortical feedback as seen experimentally, this extended DOG (eDOG) model exhibits linear firing properties despite non-linear firing characteristics of the corticothalamic cells. The spatiotemporal receptive field of the eDOG model has a simple algebraic structure in Fourier space, while the real-space receptive field, as well as responses to visual stimuli, are found by evaluation of an integral. As an example application we use the eDOG model to study effects of cortical feedback on responses to flashing circular spots and patch-grating stimuli and find that the eDOG model can qualitatively account for experimental findings.     

Paracrine and autocrine actions of neurotrophic factors

Neurotrophic factors are proteins that promote the survival and growth of neurons in the vertebrate nervous system. Although it is well known that many neurons obtain these factors from the regions to which their axons project, studies of the sites of neurotrophic factor synthesis have raised the possibility that at least some neurons may obtain these factors from other sources. Alternative sources of neurotrophic factors include cells along a neuron's axon shaft and cells or other axons terminals within the vicinity of a neuron's cell body and dendritic arbour. In addition, recent experimental studies have shown that at certain stages of development neurotrophic factor autocrine loops operate in some neurons. The evidence for and the potential physiological significance of these different modes of action of neurotrophic factors will be discussed. Special issue dedicated to Dr. Hans Thoenen.     

An account of responses of spectrally opponent neurons in macaque lateral geniculate nucleus to successive contrast

Coloured surfaces in the normal environment may be brighter or dimmer than the mean adaptation level. Changes in the firing rate of cells of the parvocellular layers of macaque lateral geniculate nucleus were studied with such stimuli; chromatic mixtures briefly replaced a white adaptation field. This paradigm is therefore one of successive contrast. Families of intensity-response curves for different wavelengths were measured. When taking sections at different luminance ratios through these families of curves, strongly opponent cells displayed spectrally selective responses at low luminance ratios, while weakly opponent cells had higher chromatic thresholds and responded well to stimuli at higher luminance ratios, brighter than the adaptation field. Strength of cone opponency, defined as the weight of the inhibitory cone mechanism relative to the excitatory one, was thus related to the range of intensity in which cells appeared to operate most effectively. S-cone inputs, as tested with lights lying along tritanopic confusion lines, could either be excitatory or inhibitory. Families of curves for different wavelengths can be simulated mathematically for a given cell by a simple model by using known cone absorption spectra. Hyperbolic response functions relate cone absorption to the output signals of the three cone mechanisms, which are assumed to interact linearly. Parameters from the simulation provided estimates of strength of cone opponency and cone sensitivity which were shown to be continuously distributed. Cell activity can be related to cone excitation in a trichromatic colour space with the help of the model, to give an indication of suprathreshold coding of colour and lightness.     

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.     

An analysis of extracellular potentials from single neurons in the lateral geniculate nucleus of the cat

The lateral geniculate nucleus of the cat was explored with micropipettes having submicroscopic tips. The only reliably recorded intracellular activity was from axons. Following orthodromic stimulation, the potentials recorded by the extracellular electrodes registered the net flow of current across the soma-dendritic membrane of the principal cell bodies. The current has three phases of flow away from the soma-dendritic membrane followed by a flow of current toward this membrane. The first component is ascribed to synaptic activity. Subsequent components are ascribed to the activity of the initial segment of the axon and a limited area of high threshold membrane on the soma. The evidence is interpreted as suggesting that most of the soma-dendritic membrane is excited synaptically to produce a postsynaptic potential, but is not excited electrically and does not produce a propagating spike.     

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.