Our eyes send different 'images' of the outside world to the brain - an image of contours (line drawing), a colour image (watercolour painting) or an image of moving objects (movie). This is commonly referred to as parallel processing, and starts as early as the first synapse of the retina, the cone pedicle. Here, the molecular composition of the transmitter receptors of the postsynaptic neurons defines which images are transferred to the inner retina. Within the second synaptic layer - the inner plexiform layer - circuits that involve complex inhibitory and excitatory interactions represent filters that select 'what the eye tells the brain'.

Parallel processing in the mammalian retina.

https://www.cell.com/trends/neurosciences/pdf/S0166-2236(00)01922-6.pdf

The thalamic matrix and thalamocortical synchrony.

Calcium entry through voltage-gated calcium channels can activate either large- (BK) or small- (SK) conductance calcium-activated potassium channels. In hippocampal neurons, activation of BK channels underlies the falling phase of an action potential and generation of the fast afterhyperpolarization (AHP). In contrast, SK channel activation underlies generation of the slow AHP after a burst of action potentials. The source of calcium for BK channel activation is unknown, but the slow AHP is blocked by dihydropyridine antagonists, indicating that L-type calcium channels provide the calcium for activation of SK channels. It is not understood how this specialized coupling between calcium and potassium channels is achieved. Here we study channel activity in cell-attached patches from hippocampal neurons and report a unique specificity of coupling. L-type channels activate SK channels only, without activating BK channels present in the same patch. The delay between the opening of L-type channels and SK channels indicates that these channels are 50-150 nm apart. In contrast, N-type calcium channels activate BK channels only, with opening of the two channel types being nearly coincident. This temporal association indicates that N and BK channels are very close. Finally, P/Q-type calcium channels do not couple to either SK or BK channels. These data indicate an absolute segregation of coupling between channels, and illustrate the functional importance of submembrane calcium microdomains.

Selective activation of Ca2+ : activated K+ channels by co-localized Ca2+ channels in hippocampal neurons

The superior colliculus is a laminated midbrain structure that acts as one of the centers organizing gaze movements. This review will concentrate on sensory and motor inputs to the superior colliculus, on its internal circuitry, and on its connections with other brainstem gaze centers, as well as its extensive outputs to those structures with which it is reciprocally connected. This will be done in the context of its laminar arrangement. Specifically, the superficial layers receive direct retinal input, and are primarily visual sensory in nature. They project upon the visual thalamus and pretectum to influence visual perception. These visual layers also project upon the deeper layers, which are both multimodal, and premotor in nature. Thus, the deep layers receive input from both somatosensory and auditory sources, as well as from the basal ganglia and cerebellum. Sensory, association, and motor areas of cerebral cortex provide another major source of collicular input, particularly in more encephalized species. For example, visual sensory cortex terminates superficially, while the eye fields target the deeper layers. The deeper layers are themselves the source of a major projection by way of the predorsal bundle which contributes collicular target information to the brainstem structures containing gaze-related burst neurons, and the spinal cord and medullary reticular formation regions that produce head turning.

The mammalian superior colliculus: laminar structure and connections.

A neurochemically distinct population of koniocellular (K) neurons makes up a third functional channel in primate lateral geniculate nucleus. As part of a general pattern, K neurons form robust layers through the full representation of the visual hemifield. Similar in physiology and connectivity to W cells in cat lateral geniculate nucleus, K cells form three pairs of layers in macaques. The middle pair relays input from short-wavelength cones to the cytochrome-oxidase blobs of primay visual cortex (V1), the dorsal-most pair relays low-acuity visual information to layer I of V1, and the ventral-most pair appears closely tied to the function of the superior colliculus. Throughout each K layer are neurons that innervate extrastriate cortex and that are likely to sustain some visual behaviors in the absence of V1. These data show that several pathways exist from retina to V1 that are likely to process different aspects of the visual scene along lines that may remain parallel well into V1.

/pdf/the-koniocellular-pathway-in-primate-vision-r8a3ulbfua.pdf

The koniocellular pathway in primate vision.

Colour vision in primates is mediated by cone opponent ganglion cells in the retina, whose axons project to the dorsal lateral geniculate nucleus in the visual thalamus. It has long been assumed that cone opponent ganglion cells project to the parvocellular layers of the geniculate. Here, we examine the role of a third subdivision of the geniculocortical pathway: the interlaminar or koniocellular geniculate relay cells. We made extracellular recordings in the dorsal lateral geniculate nucleus of the common marmoset Callithrix jacchus, a New World monkey in which the interlaminar cells are well segregated from the parvocellular layers. We found that one group of colour opponent cells, the blue-on cells, was largely segregated to the interlaminar zone. This segregation was common to dichromatic (‘red-green colour-blind’) and trichromatic marmosets. The result calls into question the traditional notion that all colour information passes through the parvocellular division of the retino-geniculo-cortical pathway in primates.

Evidence that Blue‐on Cells are Part of the Third Geniculocortical Pathway in Primates

We studied the anatomical substrates of spatial vision in a New World monkey, the marmoset Callithrix jacchus. This species has good visual acuity and a foveal specialization which is qualitatively similar to that of humans and other Old World primates. We measured the spatial density of retinal ganglion cells and photoreceptors, and calculated the relative numbers of these cell populations. We find that ganglion cells outnumber photoreceptors by between 2.4 :1 and 4.2 :1 in the fovea. The peak sampling density of ganglion cells is close to 550,000 cells/mm 2 . This value falls by almost 1000-fold between the fovea and peripheral retina ; a value which approaches recent estimates of the centroperipheral ganglion cell gradient for human and macaque monkey retina and primary visual cortex. The marmoset shows a sex-linked polymorphism of color vision : all male and some female marmosets are dichromats. Six of the retinas used in the present study came from animals whose chromatic phenotype was identified in electrophysiological experiments and confirmed by polymerase chain reaction (PCR) amplification of cone opsin encoding genes. One animal was a trichromat and the others were dichromats. Antibodies against short wavelength-sensitive (SWS) cones labeled close to 8% of all cones near the fovea of one dichromat animal, consistent with electrophysiological evidence that the SWS system is present in all marmosets. The topography and spatial density of cone photoreceptors and ganglion cells was similar to that reported for macaque retina, and we found no obvious difference between dichromatic and trichromatic marmoset retinas. These results reinforce the view that the main determinate of primate foveal topography is the requirement for maximal spatial resolution.

Topography of ganglion cells and photoreceptors in the retina of a New World monkey: the marmoset Callithrix jacchus.

The lateral geniculate nucleus (LGN) in humans and Old-World monkeys is dominated by the representation of the fovea in the parvocellular (PC) layers, and most PC cells in the foveal representation have red-green cone opponent receptive field properties. It is not known whether these features are both unique to trichromatic primates. Here we measured receptive field properties and the visuotopic organization of cells in the LGN of a New-World monkey, the marmoset Callithrix jacchus. The marmoset displays a polymorphism of cone opsins in the medium-long wavelength (ML) range, which allows the LGN of dichromatic ("red-green color blind") and trichromatic individuals to be compared. Furthermore, the koniocellular-interlaminar layers are segregated from the main PC layers in marmoset, allowing the functional role of this subdivision of the LGN to be assessed. We show that the representation of the visual field in the LGN is quantitatively similar in dichromatic and trichromatic marmosets and is similar to that reported for macaque; the vast majority of LGN volume is devoted to the central visual field. ON- and OFF-type responses are partially segregated in the PC layers so that responses are more commonly encountered near the external border of each layer. The red-green (ML) opponent cells in trichromatic animals were all located in the PC layers, and their receptive fields were within 16 degrees of the fovea. The koniocellular zone between the PC and magnocellular layers contained cells that receive excitatory input from short wavelength sensitive cones ("blue- cells") as well as other nonopponent cells. These results suggest that the basic organization of the LGN is common to dichromatic and trichromatic primates and provide further evidence that ML and SWS opponent signals are carried in distinct subdivisions of the retinogeniculocortical pathway.

Heath D. Wilder

Papers

Evidence that Blue‐on Cells are Part of the Third Geniculocortical Pathway in Primates

Topography of ganglion cells and photoreceptors in the retina of a New World monkey: the marmoset Callithrix jacchus.

Segregation of Receptive Field Properties in the Lateral Geniculate Nucleus of a New-World Monkey, the Marmoset Callithrix jacchus

Blue-on cells are part of the third geniculocortical pathway in a new world monkey, the marmoset caluthrix jacchus