Chapter 5.14 - Exploring the pulvinar path to visual cortex

Chapter 4 Serotonin modulates retinotectal and corticotectal convergence in the superior colliculus

The distribution of beta-1- and beta-2-adrenergic receptors of normal and reeler mouse brain: An in vitro autoradiographic study

The cholinergic input to the superficial layers of the superior colliculus: an ultrastructural immunocytochemical study in the ferret

A number of questions deriving from a previous electron microscopic study of the superficial layers of the rat superior colliculus pointed out the need for a comprehensive study of the cell types of the superior colliculus and their detailed morphology. In the present Golgi study the cells of the superficial layers of the superior colliculus were found to be of five major types; marginal cells, horizontal cells, narrow field vertical cells, wide field vertical cells, and stellate cells. Some of these categories were further subdivided. Each cell type has a distinctive set of dendritic field characteristics, a regional distribution, and consistent axon characteristics. The horizontal cells were found to have a preference in the orientation of their dendrites along the vertical and horizontal axes of the visual field projection upon the superior colliculus. It is argued that the horizontal cells are the presynaptic elements in the majority of the dendrodendritic synapses.

The physiological aging process is well known for functional decline in visual abilities. Among the components of the visual system, the dorsal lateral geniculate nucleus (DLG) and superior colliculus (SC) provide a good model for aging investigations, as these structures constitute the main visual pathways for retinal inputs reaching the visual cortex. However, there are limited data available on quantitative morphological and neurochemical aspects in DLG and SC across lifespan. Here, we used optical density to determine immunoexpression of glial fibrillary acidic protein (GFAP) and design-based stereological probes to estimate the neuronal number, total volume, and layer volume of the DLG and SC in marmosets (Callithrix jacchus), ranging from 36 to 143 months of age. Our results revealed an age-related increase in total volume and layer volume of the DLG, with an overall stability in SC volume. Furthermore, a stable neuronal number was demonstrated in DLG and superficial layers of SC (SCv). A decrease in GFAP immunoexpression was observed in both visual centers. The results indicate region-specific variability in volumetric parameter, possibly attributed to structural plastic events in response to inflammation and compensatory mechanisms at the cellular and subcellular level. Additionally, the DLG and SCv seem to be less vulnerable to aging effects in terms of neuronal number. The neuropeptidergic data suggest that reduced GFAP expression may reflect morphological atrophy in the astroglial cells. This study contributes to updating the current understanding of aging effects in the visual system and stablishes a crucial foundation for future research on visual perception throughout the aging process.

Visual areas I and II of cerebral cortex of rabbit.

We investigated the BOLD response of visual cortical and sub-cortical regions to fast drifting motion presented over wide fields, including the far periphery. Stimuli were sinusoidal gratings of 50% contrast moving at moderate and very high speeds (38 and 570 °/s), projected to a large field of view (~60°). Both stimuli generated strong and balanced responses in the lateral geniculate nucleus and the superior colliculus. In visual cortical areas, responses were evaluated at three different eccentricities: central 0–15°; peripheral 20–30°; and extreme peripheral 30–60°. “Ventral stream” areas (V2, V3, V4) preferred moderate-speeds in the central visual field, while motion area MT+ responded equally well to both speeds at all eccentricities. In all other areas and eccentricities BOLD responses were significant and equally strong for both types of moving stimuli. Support vector machine showed that the direction of the fast-speed motion could be successfully decoded from the BOLD response in all visual areas, suggesting that responses are mediated by motion mechanisms rather than being an unspecific preference for fast rate of flicker. The results show that the visual cortex responds to very fast motion, at speeds generated when we move our eyes rapidly, or when moving objects pass by closely.

Adaptive Surround Modulation in Cortical Area MT

1. Luis H. Ospina, MD* 1. *Assistant Professor, Pediatric Ophthalmology and Neuro-ophthalmology, Ste-Justine Hospital, University de Montreal, Montreal, Quebec, Canada After completing this article, readers should be able to: 1. Recognize cortical visual impairment (CVI) as an important cause of pediatric visual loss. 2. Identify the most frequent causes of pediatric CVI and, more specifically, understand the role of hypoxia as a cause of central visual damage. 3. Describe the different patterns and implications for future vision of hypoxic central visual damage occurring in preterm compared with term babies. 4. Know the clinical signs suggestive of CVI in children. 5. Discuss the involvement of visual functions other than visual acuity (ie, cognitive visual aspects) in CVI and correlate them with the likely affected neuroanatomic substrates. 6. Explain the value of using a multidisciplinary approach in rehabilitating children who have CVI early in their development. Vision loss caused by central nervous system damage often is referred to as CVI but also may be referred to as cerebral visual impairment or neurologic visual impairment. These terms refer to the fact that the primary defect may not necessarily be limited to the striate (primary visual) cortex and may affect other areas subserving vision, such as the visual associative cortex, optic radiations, and visual attention pathways. Although it is not yet certain which of these three terms best describes the visual deficit, it is clear that use of the label cortical blindness must be abandoned. That term not only evokes negative connotations for the child and the family but is inaccurate because in almost every instance, some degree of residual vision remains, and visual improvement can occur. CVI has become the greatest cause of pediatric visual impairment in developed countries (1)(2)(3)(4)(5) and is becoming increasingly prevalent in developing nations. CVI is a problem of increasing frequency for two primary reasons. First, the progress in neonatal care has resulted in improved survival of …

Saccadic eye movements are extremely rapid and jerk-like shifts of the eyes (up to 900 deg s−1) with which we explore our environment between periods of fixation, and other oculomotor tasks. We perform about 20 000–25 000 of such highly accurate eye movements per day to bring visual targets of interest onto our foveae. To achieve such precision, eye movements in general, and saccades in particular, need to be space–time coordinated. An article by Cromer & Waitzman (2006) in this issue of The Journal of Physiology suggests one mechanism of how space–time coordination of saccadic eye movements in the horizontal plane could be achieved by a little known and little studied area in the brainstem, the central mesencephalic reticular formation (cMRF). Although discovered years ago by the Cohen group (Cohen & Büttner-Ennever, 1984; Cohen et al. 1985, 1986), its existence had been largely neglected until the Waitzman group recently unearthed it. The classically defined cMRF is located lateral to the oculomotor nucleus (Fig. 1), dorsal to the caudal pole of the red nucleus and ventral to the posterior commissure. Different cMRF regions receive projections from small and large saccade areas of the superior colliculus (Cohen & Büttner-Ennever, 1984; Cohen et al. 1986). Stimulation of the dorsal cMRF induces fixed vector saccades (‘retinocentric’), i.e. of constant amplitude and direction regardless of the initial eye position, whereas in the ventral cMRF saccade amplitude varies depending on eye position (Cohen et al. 1985). Summary of connections of the central mesencephalic reticular formation (cMRF) The cMRF receives input from the frontal eye fields (FEFs), supplementary eye fields (SEFs) and superior colliculus (SC). Reciprocal ‘feed-back’ projections reach the SC from the cMRF. ‘Feed-forward’ projections from the cMRF target populations involved in head movements (brainstem head movement centres and cervical spinal cord) and eye movements (e.g. horizontal saccade generator network containing excitatory burst neurones (EBNs) in the paramedian pontine reticular formation (PPRF), inhibitory burst neurones (IBNs) and omnipause neurones (OPNs). Bilateral monosynaptic projections exist both to medial rectus (MR) motoneurones in the oculomotor nucleus (III) and to ‘slow’ and ‘fast’ abducens (VI) motoneurones (MNs), which innervate the lateral rectus muscle (LR). While feed-back projections from the cMRF to the SC and feed-forward projections (e.g. to PPRF) are mediated by separate neurone populations, it is unknown whether the same applies to the various other efferent projections from the cMRF. Direct projections from the cMRF to fast LR and MR MNs represent another pathway for horizontal saccade generation, in addition to traditional saccade generation pathways (involving projections from the FEFs via the SC to the PPRF, and from the PPRF to ipsilateral LR MNs and abducens internuclear neurones, AIN, and subsequently contralateral MR MNs for the production of horizontal conjugate eye movements). In addition, the cMRF plays a role in the coordination of eye and head movements, i.e. in gaze control. INC, interstitial nucleus of Cajal. The important role the cMRF is playing for space–time coordinated rapid eye movements, as shown in the article by Cromer & Waitzman (2006), has to be seen in the following context. While we may be looking anywhere at a given moment in time when an object of interest appears in our visual field, we are able to capture such a target immediately with a saccadic eye movement. The superior colliculus provides a spatial map of the visual environment of interest. The spatial code for target-selecting saccadic eye movements exists in the form of a vector representation of a given target location that allows us to shift gaze from one place to any other place in the visual field. However, up to now, it has been unclear which neuronal circuits are actually involved in performing such a movement vector calculation, since the superior colliculus only offers a spatial map but not the temporal aspect of the required eye movement. Cromer & Waitzman (2006) now offer the suggestion that various feed-back and feed-forward loops between the cMRF, the superior colliculus and the premotor saccade generator network (Fig. 1), including neurones within the cMRF, constitute a network that allows the space–time coordination of target-selecting rapid eye movements. They have identified eight different neurone types within the cMRF related to one or more saccade metric parameters and combinations thereof, e.g. velocity, duration, amplitude, etc. They argue that these different neurone types indicate different processing stages of spatial–temporal transformations via multiple anatomical pathways and physiological mechanisms. Projections from the cMRF to the premotor saccade generator network (EBNs, IBNs, OPNs) would serve as the feed-forward signals of the now time-coordinated and space-coded collicular outflow, whereas the projections from the cMRF to the superior colliculus would provide the necessary feed-back flow. Neuroanatomical tract tracing results with a retrograde transneuronal marker have shown that the cMRF also innervates directly, i.e. monosynaptically, lateral rectus (Graf et al. 2000; Ugolini et al. 2001, and submitted) and medial rectus motoneurones (Graf et al. 2002). These direct projections may be part of the network involved in generation of combined eye and head movements, i.e. gaze control, since the cMRF also innervates the cervical spinal cord (Robinson et al. 1994; Scudder et al. 1996) and brainstem head movement centres (May et al. 2005; Perkins et al. 2005). Furthermore, the cMRF, like the superior colliculus, receives direct projections from the cortical frontal eye fields (FEFs) (Huerta et al. 1986; Stanton et al. 1988) and the supplementary eye fields (SEFs) (Huerta & Kaas, 1990; Shook et al. 1990) (Fig. 1). This makes the cMRF also a potential relay to transmit information related to saccade metrics from the FEFs and SEFs to horizontal extraocular motoneurones. Finally, the cMRF may even play a role in maintaining eye position, gaze holding and fixation. Monosynaptic projections from the caudal (horizontal) cMRF to lateral rectus and medial rectus motoneurones support such an idea of participation in stabilizing eye position and fixation, particularly as such projections also target the so-called ‘slow’ lateral rectus motoneurones (Ugolini et al. 2001, and submitted), and bilateral stimulation of the cMRF promotes fixation (Cohen et al. 1985). The bilateral monosynaptic projections from the cMRF to lateral rectus motoneurones are also a potential substrate for the transmission to these motoneurones of vergence signals (Mays & Gamlin, 1995). To summarize, the cMRF is embedded in an interconnected and complex network of eye movement circuits for the production of saccades, fixation, gaze holding and vergence (Fig. 1). It receives direct input from the cortical eye movement centres, the FEFs and SEFs, and it projects directly to horizontal, i.e. lateral and medial rectus, motoneurones. There it contacts both ‘fast’ and ‘slow’ motoneurones. Besides ocular motoneurones, the cMRF also contacts the horizontal saccade generator network (EBNs, IBNs, OPNs) and head movement related brainstem centres, and maintains reciprocal connections with the superior colliculus.

Stimulation of the optic chiasm (OX) or visual cortex (VC) elicited a burst of impulses from visual cells in the superficial layers of the hamster's superior colliculus which was followed by a period of response suppression which lasted from 50-200 ms. During this period responses to normally suprathreshold OX and VC shocks, spontaneous activity and even injury discharges were markedly attenuated. For approximately 50% of the visual cells tested VC stimulation also reduced responses to visual stimuli. No correlations between receptive field properties and whether or not VC shocks diminished a given cell's visual responses were noted. Stimulation of either the cervical spinal cord (SC) or somatic sensory cortex (SMCTX) evoked action potentials from somatosensory neurons in the deep tectal laminae. These responses were followed by a period of suppression identical to that seen in the superficial layers after OX or VC shocks. SMCTX stimulation attenuated responses to tactile stimuli for 30% of the cells tested in the deep layers. Again, no correlation was observed between somatosensory response characteristics and whether or not a given cell exhibited response suppression.

The neurophysiology of the rodent visual system has mainly been investigated by invasive and ex-vivo techniques providing fragmented data. This area of research has been deprived of functional MRI studies based on blood oxygenation level dependent (BOLD) contrast, which allows a whole brain approach with a high spatial and temporal resolution. In the present study, we looked at the neurovascular response properties of the visual system of the pigmented rat, focusing on the visual cortex (VC), the superior colliculus (SC) and the flocculus-paraflocculus of the cerebellum (FL-PFL), using BOLD fMRI under domitor anesthesia. Visual stimulation was performed monocularly or binocularly while flashing light from a strobe unit was presented. For each structure, we assessed the flashing frequency that evoked the optimal BOLD response: Neither the VC nor the FL-PFL displayed frequency dependence during monocular visual stimulation, but were most sensitive to low frequencies (1-5 Hz) when flashing light was provided binocularly. The SC responded optimally to high flashing rates (8-12 Hz) during both monocular and binocular stimulation. The signal intensity changes in the VC and FL-PFL were locked to the stimulation period, whereas the BOLD response in the SC showed a similar onset but a very slow recovery at offset. The VC and FL-PFL, but not the SC, showed signs of binocular competition. The observed correlation between frequency-dependent responses of different visual areas during binocular visual presentation suggests a functional relationship between the VC and FL-PFL rather than between the SC and FL-PFL.

PROJECTION OF THE RETINA ON SUPERIOR COLLICULUS OF CATS

Visual response properties were examined in the superficial layers of the superior colliculus (SC) of anesthetized, paralyzed cats before and after i.v. administration of d-amphetamine. Receptive fields (RFs) of single SC units were plotted using small spots of light presented to the contralateral eye. Within the first hour following d-amphetamine injections, RF size gradually increased, reaching a maximum 86 min post-injection. On average, the area of the RF increased by 5.6 times and RF expansion was observed in all single units examined in the superficial layers. Over the subsequent 4-8 h following the injection, RF area gradually decreased and returned to control dimensions. Most RFs displayed asymmetrical patterns of expansion, showing relatively more horizontal than vertical growth. As RF expansion developed, responses to stimuli flashed "on" and "off" at various locations both inside and outside the borders of the control RF became progressively more vigorous. In contrast, no significant changes were noted in direction-selective responses at any time after d-amphetamine injections. Using an array of light bar stimuli of different lengths, the strength of surround suppression was found to be significantly diminished by d-amphetamine. The reduction in surround suppression was especially clear for bar lengths which exceeded the diameter of the control RF. No RF expansion was observed in the superficial layers of the SC when d-amphetamine was injected intravitreally. Furthermore, d-amphetamine had no discernable effect on the RF sizes of cells in the visual cortex. These results suggest that the RF changes in the SC were not of either retinal or cortical origin. We conclude that the mean retinal area which can potentially influence the activity of RFs in the superficial layers of the SC may be on average over 5 times greater than the RF area determined using conventional methods and criteria. These findings raise the interesting possibility that the relatively small size and sharp borders characteristic of RFs in the superficial layers arise from local inhibitory networks which delimit a broader field of excitatory activity supplied by retinal and cortical afferent terminals. Thus, in order to generate the RF changes observed here, either these local inhibitory circuits are amphetamine sensitive, or more likely, these inhibitory networks are dynamically modulated by an, as yet unidentified, amphetamine-sensitive input affecting visual RFs in the superficial layers.

Both the frontal eye field (FEF) in the prefrontal cortex and the superior colliculus (SC) on the roof of the midbrain participate in the generation of rapid or saccadic eye movements and both have projections to the premotor circuits of the brain stem where saccades are ultimately generated. In the present experiments, we tested the contributions of the pathway from the FEF to the premotor circuitry in the brain stem that bypasses the SC. We assayed the contribution of the FEF to saccade generation by evoking saccades with direct electrical stimulation of the FEF. To test the role of the SC in conveying information to the brain stem, we inactivated the SC, thereby removing the circuit through the SC to the brain stem, and leaving only the direct FEF-brain stem pathway. If the contributions of the direct pathway were substantial, removal of the SC should have minimal effect on the FEF stimulation, whereas if the FEF stimulation were dependent on the SC, removal of the SC should alter the effect of FEF stimulation. By acutely inactivating the SC, instead of ablating it, we were able to test the efficiency of the direct FEF-brain stem pathway before substantial compensatory mechanisms could mask the effect of removing the SC. We found two striking effects of SC inactivation. In the first, we stimulated the FEF at a site that evoked saccades with vectors that were very close to those evoked at the site of the SC inactivation, and with such optimal alignment, we found that SC inactivation eliminated the saccades evoked by FEF stimulation. The second effect was evident when the FEF evoked saccades were disparate from those evoked in the SC, and in this case we observed a shift in the direction of the evoked saccade that was consistent with the SC inactivation removing a component of a vector average. Together these observations lead to the conclusion that in the nonablated monkey the direct FEF-brain stem pathway is not functionally sufficient to generate accurate saccades in the absence of the indirect pathway that courses from the FEF through the SC to the brain stem circuitry. We suggest that the recovery of function following SC ablation that has been seen in previous studies must result not from the use of an already functioning parallel pathway but from neural plasticity within the saccadic system.