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Home , Receptive field, Visual system

Visual System Advanced article

Stephen D Van Hooser, Brandeis University, Waltham, Massachusetts, USA Article Contents

. Anatomy of the Sacha B Nelson, Brandeis University, Waltham, Massachusetts, USA . Concept of a . and many other animals obtain much of their about the world . Focusing of on to the Retina through their . Patterns of light are transformed into nerve impulses in the retina and . First Stage of Information Processing: visual information is processed by nerve cells in the primary . In the Hyperpolarization of Photoreceptor Cells , about one-half of the is dedicated in some way to the processing of . Receptive Fields of Ganglion Cells visual information. . Relay of Signals from the Lateral Geniculate Nucleus to the Visual Cortex . Orientation and Directional Selectivity in Cortical Cells Anatomy of the Visual System . Double-opponent Colour Cells in the Visual Cortex . Columnar Organization of the Visual Cortex begins in the , where light passes . Beyond the Primary Visual Cortex through the and is focused on to photoreceptors in the . Summary retina. of retinal ganglion cells, the output cells of the retina, leave the eye in a bundle called the . At the , some axons cross over to the opposite doi: 10.1038/npg.els.0000230 hemisphere, so that axons representing the right half of visual space travel to the left hemisphere and axons rep- resenting the left half of visual space travel to the right number of cells in the LGN and cortex; almost half of V1, hemisphere. From the optic chiasm, the retinal ganglion for example, represents the fovea. Visual information is axons project to visual brain structures such as the gathered through active movements of the eyes to bring the lateral geniculate nucleus (LGN) of the , the su- perior colliculus in the , and the . In , over 90% of these projections are to the LGN, where the retinal ganglion axons segregate into layers based on eye of origin and other properties. LGN relay cells receive large synaptic contacts from these axons, and make projections to the primary visual cortex (V1), where LGN axons representing each eye ramify in an al- ternating fashion. The anatomy of the visual sys- Lens Retina Optic nerve Primary visual tem is shown in Figure 1. cortex (V1) There is a second major visual pathway to the neocortex Optic from the retina via the . The superior chiasm colliculus projects to the pulvinar in the thalamus, which in Lateral geniculate turn projects to specialized regions of the visual cortex lo- nucleus (LGN) cated beyond V1. In primates, the superior colliculus is known to be involved in eye movements, but it receives Optic many fewer ganglion cell axons than the LGN. In many tract other , such as carnivores and rodents, the supe- rior colliculus receives a larger percentage of retinal affer- Optic radiations ents than in primates, and it is likely that the superior colliculus plays a larger role in vision in these animals. This Figure 1 Anatomy of the visual system. Light arrives at the eye and is article will focus on the pathway from the retina to the focused by the lens on to the retina, where photoreceptors transduce the light into electrical signals that are processed by local retinal . LGN to V1, since it is much larger in primates and is better Axons of retinal ganglion cells, the output cells of the retina, leave the retina studied than the pathway via the superior colliculus. in a bundle called the optic nerve. At the optic chiasm, some axons cross Since are limited in size by developmental and over, so that axons representing the right half of visual space travel to the energy constraints, the visual system does not represent all left lateral geniculate nucleus (LGN) and axons representing the left half of parts of the visual field equally, but instead emphasizes the visual space travel to the right LGN (not shown). In the LGN, the axons segregate into layers according to eye of origin and other properties. LGN area in the centre of the eye. The centre of the retina, called relay cell axons form a band called the optic radiations and project to the the fovea, contains the highest density of photoreceptors, primary visual cortex, where LGN axons representing each eye ramify in an and the fovea is represented by a disproportionately large alternating fashion.

ENCYCLOPEDIA OF LIFE SCIENCES © 2005, John Wiley & Sons, Ltd. www.els.net 1 Visual System most informative parts of a scene into focus on the centre of the retina. Humans make over 100 000 such eye move- PRL Rod ONL ments, or , in a single day, typically one or more Cone per second. By devoting large numbers of cells to a small OPL region of visual space and moving the eyes to informative Horizontal cell places in an image, the mammalian visual system affords INL Bipolar cell higher resolution than would be possible in an animal with ON fixed eyes and equal brain size. Light IPL OFF GCL Ganglion cell +– Time Concept of a Receptive Field (a) To optic nerve (b)

In each brain structure described here, an individual cell Centre light Surround light responds to images in a small part of the visual field and Inverting only responds strongly to particular image patterns. The part of the visual field to which a cell responds is called Noninverting synapse the receptive field of the cell, and the relationship between image patterns in the receptive field and the activity of the cell is referred to as the cell’s receptive field properties.

Figure 2b shows an example of the receptive field properties Stimulus on of one in the retina that is excited by light in the centre of its receptive field but inhibited by light in the Voltage excitation Inhibition/ surrounding part. Time depolarizing Hyperpolarizing/

(c)

Retina Figure 2 (a) The major cell types in the retina and their laminar organization. PRL 5 photoreceptor layer; ONL 5 ; The retina is a sheet of neurons and specialized OPL 5 ; INL 5 ; IPL 5 inner cells located in the back of the eye. As shown in Figure 2a, plexiform layer; GCL 5 . (b) A centre–surround retinal the retina consists of six layers: the photoreceptor layer ganglion cell that responds to light in the centre of its receptive field and is (PRL), the outer nuclear layer (ONL), the outer plexiform inhibited by light in the surrounding region. The stimulus is shown on the left, and action potentials in the cell relative to the onset and offset of the layer (OPL), the inner nuclear layer (INL), the inner plexi- stimulus are shown on the right. Note that the cell responds most form layer (IPL), and the ganglion cell layer (GCL). The vigorously to a light spot in the centre surrounded by a dark annulus organization of the layers is peculiar in that the photo- (second from the top), but the cell responds much less vigorously when receptors are located at the back of the retina so that light stimulated by a large white spot (third from the top) because of the passes through all of the layers before reaching them. The inhibitory surround. These properties are often denoted symbolically with the notation at bottom, with ‘+’ indicating a preference for more light photoreceptors of the retina transduce light into electrical relative to background and ‘ 2 ’ indicating less light. (c) Schematic diagram signals that are processed by the local neurons of the retina. of retinal circuitry that mediates the centre–surround cell depicted in (b). The retinal ganglion cells are the only output cells of the Light in the centre hyperpolarizes a cone, which excites a bipolar cell, which retina, so all visual information available to the brain is in turn excites the . Horizontal cells mediate the effect of transmitted by the axons of these cells. the surround, providing inhibition to the bipolar cell in the centre when there is light in the surround. This figure is adapted from Werblin and Dowling (1969), who studied the salamander Necturus maculosus, and similar circuitry has been found in other vertebrates. Focusing of Light on to the Retina First Stage of Information Processing: Light enters the eye through a transparent portion of the external membrane of the eye (the cornea), passes through Hyperpolarization of Photoreceptor the lens and the vitreous space, and forms an image on the Cells retina. Light is bent, or refracted, as it enters compartments that possess different refractive indices. This The transduction of light into electrical activity occurs in permits the formation of a focused image on the retina. The two types of photoreceptors: rods and cones. Both rods lens contributes only about 1/4 of the refractory power of and cones consist of an inner segment that contains the cell the eye (the remainder is due to the cornea), but because the body and nucleus, and an outer segment containing a stack shape of the lens can be actively adjusted, it allows objects of membranous disks specialized for phototransduction. at various distances to be brought into focus. Rods have an elongated outer segment, are specialized for

2 Visual System detection of low intensity (scotopic) light, and are homo- to operate at different light levels. If one reads a newspaper geneous in their wavelength sensitivity. Cones have a ta- outside on a bright sunny day, the absolute amount of light pering outer segment, are specialized for detection of reflected from both the black text and the white page will be higher intensity (photopic) light, and individually are more much greater than if one reads the same newspaper in- sensitive to long (L-cones), medium (M-cones), or shorter doors. However, the between the black text and wavelengths of light (S-cones). Comparisons of intensity the white page conveys meaningful information in both across different wavelengths are the basis of colour vision. settings. In the human retina there are approximately 100 million Each retinal ganglion cell type receives input from a dif- rods and 5 million cones. The most sensitive portion of the ferent arrangement of the local retinal circuitry. The local retina, the fovea, contains exclusively cones and the density circuitry that produces the light/dark opponent retinal of cones falls off with increasing distance from the fovea. ganglion cell described above is shown in Figure 2c (Werblin Rods are absent in the fovea but are present throughout the and Dowling, 1969). Photoreceptors synapse directly on to rest of the retina. The proportion and distribution of rods bipolar neurons, which in turn provide the primary input and cones varies widely across animal . to retinal ganglion cells. In the case of a light/dark oppo- In the dark, photoreceptors have a relatively depolarized nent cell, the bipolar cell is excited by the photoreceptors. (  2 40 mV) and continually release Horizontal cells, which make inhibitory connections to bi- glutamate from their synaptic terminals. This depolariza- polar cells, provide surround inhibition to the bipolar cell, tion is caused by continual activation of mixed cation which then provides less excitation to the ganglion cell channels located in the outer segments by cytoplasmic cy- when there is light in the surround. Bipolar neurons that clic GMP. Current flow through these channels is termed respond to a dark/light contrast between the centre and the ‘dark current’. The dark current is opposed by a resting surround hyperpolarize in response to light in their centre potassium conductance that would otherwise hyperpolar- regions because they receive sign-conserving ize the photoreceptor to  2 80 mV. Absorption of light from their photoreceptor inputs. They are depolarized by activates the (rhodopsin in rod photorecep- the release of glutamate during the dark and then hyper- tors) and initiates a biochemical cascade that leads to ac- polarize back towards their resting membrane potential tivation of a phosphodiesterase, rapidly reducing when glutamate release is shut off by light. Bipolar and cytoplasmic cGMP levels and thereby closing the cGMP- ganglion cells that respond to a light/dark contrast be- sensitive cation channels. The effect of light is therefore to tween the centre and surround are called ON cells, while hyperpolarize the photoreceptor by shutting off the dark those that respond to a dark/light contrast between the current. This hyperpolarization shuts off release of gluta- centre and surround are called OFF cells. mate from the photoreceptor terminal. Retinal ganglion cells are the only output cells of the retina, so these cells must convey all information necessary for a variety of visual functions such as seeing in colour, seeing form, and detecting . Thus, it is not surpris- Receptive Fields of Retinal Ganglion ing that there is a large diversity of retinal ganglion cell Cells types (DeMonasterio and Gouras, 1975), although the precise number of these types and the exact qualities that Most mammalian retinal ganglion cells have an opposing identify each type are still a subject of debate. Ganglion centre–surround (or concentric) receptive field organiza- cells are commonly grouped on the basis of their size and tion, which means they are excited by one stimulus in the their axonal projections; cell types vary slightly from spe- centre of their receptive field and inhibited by another cies to species, and here we describe cells found in the stimulus in the area surrounding this centre (Kuffler, 1953). monkey. Small ganglion cells projecting to the An example of a centre–surround cell that responds vig- parvocellular layers of the LGN are called midget cells, orously to a light spot surrounded by a dark annulus is while the larger ganglion cells projecting to the magnocel- shown in Figure 2b. Since neurons fire action potentials and lular layers of the LGN are called parasol cells. There is a cannot signal negatively, centre–surround cells usually ex- third, less well studied class of cells that project to small ist in two polarities. For example, most vertebrates possess cells throughout the LGN called the koniocellular cells. a retinal ganglion cell type that responds to a light/dark The midget cells are primarily responsible for seeing de- contrast between its receptive field centre and surround, tail and colour. They comprise about 80% of all retinal and in addition possess another retinal ganglion cell type ganglion cells and have very small receptive fields. In hu- that responds to a dark/light contrast between the centre mans and Old World monkeys, the vast majority of midget and the surround. cells are colour-opponent, being excited by red in the centre The fact that most retinal ganglion cells, such as the and inhibited by green in the surround or vice versa. It is light/dark centre–surround cell described above, respond important to note that this type of colour opponency does to a contrast between two regions rather than absolute not correspond to a preference for a red/green contrast brightness allows the visual system to use the same circuitry between the centre and surround, as such a neuron would

3 Visual System be excited by red in the centre and also be excited by green in the surround or vice versa; such ‘double opponent’ cells K6 are first seen in the primary visual cortex. Midget cells tend 6 to respond to stimuli in a sustained manner, which means K5 that they fire constantly to a constant stimulus. 5 Parasol cells, by contrast, primarily mediate seeing mo- 4 K4 tion and change. They make up about 10% of retinal gan- glion cells, and have larger receptive fields than midget 3 cells. There are few parasol cells in the fovea, but the ratio K3 of parasol to midget cells increases with eccentricity. Par- 2 asol cells are insensitive to colour and instead are lumi- 1 K2 nance-opponent. Unlike midget cells, parasol cells respond transiently to stimuli, which means they fire a few action K1 potentials when a stimulus appears but do not fire con- stantly to a constant stimulus. Parasol cells can, however, respond to more rapid changes in a stimulus pattern than can midget cells. The function of the koniocellular cells is much less well understood than that of the midget and parasol cells (Hen- dry and Reid, 2000). Koniocellular cells are a heterogene- ous class of neurons, some of which have large receptive fields (158), low firing rates, and slow-conducting axons. Only one specific type of receptive field properties, previ- ously to be associated with a class of midget neu- rons, has been conclusively identified as koniocellular. Figure 3 The lateral geniculate nucleus of the rhesus monkey. Midget Cells of this type are colour-opponent neurons excited by cells of the retina innervate layers 3–6, and the parasol cells innervate layers blue in the centre and inhibited by red or green in the cen- 1 and 2. Koniocellular cells innervate K1–K6 but are also diffusely present tre. These cells have larger receptive field centre sizes than throughout the entire LGN. the midget cells and they lack a surround. referred to as a relay station between the retina and visual cortex, and LGN cells that receive retinal input and project to cortex are called relay cells. Axons from these relay cells Relay of Signals from the Lateral form a band called the optic radiations and travel to the Geniculate Nucleus to the Visual Cortex primary visual cortex (see Figure 1). The LGN also receives massive direct and indirect connections from primary vis- After leaving the retina, midget, parasol and koniocellular ual cortex, that can modulate signals from the retina in cell axons enter the optic chiasm and travel to the LGN, various ways. However, the functional role of these ‘feed- where they segregate into layers based on eye of origin and back’ connections and their modulation of the retinal input cell properties. The layers of the LGN are shown in Figure 3. are incompletely understood. Layers 3–6 are the parvocellular layers, which receive input Upon arriving in the primary visual cortex (V1), axons from midget cells, and layers 1 and 2 are the magnocellular from each of the three LGN neuron classes make synaptic layers, which receive input from parasol cells. Layers 1, 4, contacts in different cortical layers. V1 is a six-layered and 6 receive input from the contralateral eye, whereas structure, and a simplified wiring diagram of its connec- layers 2, 3, 5 receive input from the ipsilateral eye. The tions is shown in Figure 6. The majority of input from the koniocellular axons project to layers K1–K6, which are parvocellular cells arrives at a subdivision of layer 4 called intercalated among the parvocellular and magnocellular layer 4B, while the magnocellular cells largely project to layers, and koniocellular cells are also found diffusely another layer called 4A. Cells in layers 4B and 4A primarily throughout the entire LGN. Each layer of the LGN is or- exhibit receptive field properties similar to the parvocellu- ganized topographically, which means there is a one-to- lar and magnocellular neurons that provide their input. one relationship between receptive field locations in the The koniocellular cells project to small bands of cells retina and those in the LGN, and that adjacent cells also spanning layers 1–3 called ‘blobs’ that will be discussed have adjacent receptive field locations. further below. Within the cortex, cells in layer 4 project to Retinal ganglion cells make powerful synapses on to layers 2 and 3 throughout the cortex, and layers 2 and 3 LGN cells, and measurements of LGN cell properties have cells in turn project to layers 5 and 6 in V1 and also project shown them to be similar to those of the retinal ganglion to adjacent cortical areas. Cells in layer 5 project to adja- cells that drive them. For this , the LGN is often cent cortical areas and also to subcortical structures such as

4 Visual System the superior colliculus. Finally, cells in layer 6 project back respond to the presence of a bar located anywhere within to the LGN. (Note that we have followed Casagrande and their receptive fields, and thus do not have specific regions Kaas (1994) in using Hassler’s labelling of V1 layers.) that can be stimulated by spots of light (see Figure 4c). Many complex cells respond most vigorously to bars or edges that are moving, and some simple and complex cells only re- spond to movement in one particular direction, as shown in Orientation and Directional Selectivity Figure 4d. The synaptic connections and cellular mechanisms that in Cortical Cells underlie orientation selectivity are still a subject of debate. The investigators who first characterized simple and com- With the exception of cells in the input layers 4A and 4B, plex cells, David Hubel and , proposed a luminance-sensitive neurons in V1 have very different re- theory describing how simple and complex receptive field ceptive field properties from cells in the LGN. These cells properties could arise from input from LGN cells (or V1 respond best to edges or bars at a particular orientation layer 4A/4B cells) and other cortical cells. They suggested (see Figure 4a), and these orientated edges are an important that responses could arise from feed-forward feature for the because they frequently de- input from centre–surround cells with co-linear receptive fine the boundaries of objects. V1 has two types of orien- field centres of like signs as shown in Figure 5a. Such an tation-sensitive neurons, simple cells and complex cells arrangement would produce a cell with excitatory and in- (Hubel and Wiesel, 1962). Receptive fields of simple cells hibitory regions and orientation selectivity. The complex have separate regions that respond to light increments or cell properties of orientation selectivity but indifference to light decrements, so simple cells respond to bars or edges at precise positioning could arise from input from multiple one particular position in space with a maintained re- adjacent simple cells with similar orientation preferences, sponse, as shown in Figure 4b. Complex cells, by contrast, as shown in Figure 5b. The simplest and strongest evidence for Hubel and + – + Wiesel’s idea comes from anatomical and physiological studies of cat primary visual cortex. In the cat, unlike in the + – + monkey, cells in the input layer 4 of V1 show orientation selectivity. Almost all layer 4 cells in the cat are simple cells, +– + while many cells in layers 2 and 3 and 5 and 6 are complex +– + cells, consistent with the notion that simple cells can be

ON ON produced directly with synaptic input from centre–sur- Bar Bar OFF OFF round neurons, but that complex cells require an addi- (a) (b) tional layer of intervening neurons. In addition, simultaneous recordings of connected neurons in cat

ON Bar OFF (c) (d) – + Figure 4 (a) Many neurons in the primary visual cortex respond to bars or – + – + – + – + + – + – + – + edges at a particular orientation. The stimulus is shown at the left, and – + action potentials in the cell relative to the onset and offset of the stimulus are shown at the right. The neuron in (a) responds to a bar rotated 458 (a) (b) clockwise from vertical, but responds poorly to bars with other orientations. (b) Simple cells have separate regions of their receptive fields that respond Figure 5 Hubel and Wiesel’s model for the formation of simple and to light increments and light decrements and thus respond to bars at complex receptive field properties. (a) A simple cell (at right) that responds specific locations. One example of such a receptive field pattern is shown. to a dark, oriented bar on a light background could receive input from (c) In contrast to simple cells, complex cells respond to a properly oriented several adjacent centre–surround cells that respond to light decrements in bar anywhere in their receptive fields. (d) Many cells in V1 respond to their receptive field centres. (b) A (at right) could obtain its moving oriented bars. The arrows in the stimulus (left) indicate direction of indifference to bar position by receiving input from several adjacent simple bar movement. Most cells in V1 are orientation-selective and not direction- cells (at left) sharing one orientation preference. The complex cell’s selective, responding to movement in both directions (upper), but some receptive field properties cannot be represented in the same form as the cells are direction-selective and only respond to bars moving in a particular schematics for the LGN cells and simple cell in (a) and the simple cells in (b). direction (lower). It responds to a properly oriented bar at any position in its receptive field.

5 Visual System

LGN and V1 by Reid and Alonso show that an LGN neu- Contralateral Ipsilateral Contralateral ron is much more likely to contact a V1 simple cell with an 1 overlapping receptive field if the LGN neuron’s receptive 2 To V2 field centre has the same sign as the overlapping region in 3 the simple cell’s receptive field than if the two signs do not 4A To MT, V2 V1 agree (Reid and Alonso, 1995). 4B Another idea for generation of orientation selectivity posits that this selectivity arises from an interaction of 5 synaptic input from centre–surround cells and recurrent 6 To superior synaptic connections with other V1 neurons (Sompolinsky colliculus and Shapley, 1997). In this view, orientation-selective cells receive centre–surround input that has a small orientation Parvocellular – contralateral bias (not as strong as pictured in Figure 5a), and receive Parvocellular – ipsilateral strong excitatory input from nearby V1 neurons with sim- Magnocellular – contralateral LGN Magnocellular – ipsilateral ilar orientation preferences and inhibitory input from Koniocellular – contralateral nearby cells with many different orientation preferences. Koniocellular – ipsilateral When an oriented edge is observed, many V1 cells with an orientation preference close to that of the stimulus fire Figure 6 Selected synaptic connections in the primary visual cortex. In weakly initially, but over time the recurrent input from each ocular dominance band, parvocellular LGN neurons from one eye project to cortical layer 4B, magnocellular LGN neurons project to layer 4A, other V1 cells to V1 neurons with the proper orientation and koniocellular LGN neurons project to the cytochrome oxidase blobs in preference is amplified. This model is consistent with the layers 1–3. Neurons in layer 4 make connections with neurons in layers 2 experimental observations that orientation selectivity is and 3, both in the blobs and between the blobs, and these cells in turn sharpened over time and that orientation selectivity in one project to layers 5 and 6. Cells in layers 2, 3 and 5 make connections with region of V1 can be disrupted by inactivation of cells in a adjacent cortical areas, and cells in layer 5 also make connections with subcortical structures such as the superior colliculus. Finally, cells in layer 6 V1 region hundreds of micrometres away. project back to the lateral geniculate nucleus. Adapted from Casagrande and Kaas (1994).

Double-opponent Colour Cells in the more energy and thus have more mitochondria. These re- gions, called ‘blobs’ for their appearance in tangential cor- Visual Cortex tical sections stained for cytochrome oxidase are depicted in the wiring diagram in Figure 6. The blobs receive input Humans are able to perceive relationships between colours from the koniocellular layers of the LGN, so it is possible over a wide range of lighting conditions, which means they that double-opponent cells get their receptive field prop- must be able to detect colour contrasts. In the LGN, the erties only from input from koniocellular neurons; alter- majority of neurons are colour-selective, being excited by natively, they might receive input from the neurons in one colour in one region of their receptive fields and in- cortical layer 4B that receive input from the parvocellular hibited by another colour in another region, but they do LGN layers. not respond to colour contrasts. The cortex contains a class of cells, called ‘double-opponent cells’, that performs this function (Livingstone and Hubel, 1984). Double-opponent cells show two types of colour op- ponency with a centre–surround organization. They are Columnar Organization of the Visual excited by one colour in the centre of their receptive field Cortex and inhibited by another colour, and they are excited by this second colour in the surround region and inhibited by In addition to the laminar organization described above, the first colour. For example, a double-opponent cell might V1 has a considerable degree of horizontal organization at be excited by red and inhibited by green in its centre, and be many scales. Like the LGN, V1 has a topographic repre- excited by green and inhibited by red in the surround (de- sentation of visual space, so that each position on the V1 noted r+g 2 /r 2 g+). These cells seem to only exist in sheet of cells corresponds to a particular point in visual four types: r+g 2 /r 2 g+, r 2 g+/r+g 2 ,b+y2 / space, and adjacent points on the sheet correspond to ad- y+b 2 ,b2 y+/y 2 b+, where b is blue and y is red and jacent points in visual space (see Figure 7a). green together. Within this topographic organization is a segregation of Double opponent cells are found in regions of layers 2 the input from the two eyes. Axons from the LGN relay and 3 that show increased staining for cytochrome oxidase, cells mediating each eye ramify in layer 4 and in the blobs in a mitochondrial enzyme shown to exist more densely in an alternating fashion, as shown in Figure 6 and Figure 7b. cells with generally higher activity since such cells require Each of these ocular dominance bands is about 450 mm

6 Visual System

Beyond the Primary Visual Cortex

A complete discussion of other visual cortical areas is be- yond the scope of this article, but it is important to note that neurons in the primary visual cortex make connections with cells in other visual cortical areas, and many of these areas respond to even more specific stimuli than does V1. For example, while direction-selective cells in V1 respond to motion of local image features within their small recep- tive fields, direction-selective cells in middle temporal (MT) cortex respond to motion of a complete object or texture. Some cells in the inferior temporal (IT) cortex respond to stimuli as specific as faces. The segregation of cell prop- erties for sensitivity to motion or colour and form in the retina and LGN seems to be somewhat maintained in pro- jections to the second visual cortex (V2) and higher cortical areas like MT and IT. V1 cells receiving indirect input from the LGN parvocellular cells largely project to visual areas mediating form; cells receiving indirect input from the ma- gnocellular cells largely project to areas mediating the per- ception of motion; and cells in the blobs largely project to areas mediating of colour. These and interven- Figure 7 Horizontal organization of the visual cortex. (a) The topographic ing visual areas send many feedback connections to projection of visual space in the right visual hemifield on to an idealized, the visual cortex, and, as with the feedback connections unfolded primary visual cortex (adapted from Hubel 1995). Note the large to the LGN, the role of these connections is not well representation of the central region in V1, and the relatively small understood. representation of the periphery. Within this topographic map is an alternating map of input from the two eyes. (b) A small section of V1 imaged optically using voltage-sensitive dyes by Blasdel and colleagues. Regions that respond to visual stimulation of the left eye are coloured black, Summary while regions that respond to stimulation of the right eye are white. Woven into the topographic map and ocular dominance bands is a semi-regular map of orientation preference. (c) The same area of cortex as (b), except In the human visual system, signals travel from the retina to that the eyes are being stimulated with bars of different orientation. Each the lateral geniculate nucleus to the primary visual cortex. In pixel in the image is colour-coded according to the bar orientation that the retina, photoreceptors transduce light into electrical sig- evoked the largest response (see scale at right). For example, red regions in nals that are processed by the local neurons of the retina, the image showed greatest activation by horizontal bars. (b) and (c) are which in turn provide input to the retinal ganglion cells, the reproduced with permission from Blasdel and Salama (1986). output neurons of the retina. There are many types of retinal ganglion cells, including those sensitive to colour and form and motion and change, and retinal ganglion cells generally wide. All of the cells in layer 4 strictly respond to input from have receptive fields with a centre–surround organization. one of the two eyes, but in layers 2, 3, 5 and 6, the cell input The lateral geniculate nucleus acts as a relay station between is mixed. Neurons in layers 2, 3, 5 and 6 that lie in the centre the retina and primary visual cortex. In the cortex, the lu- of an ocular dominance band show a strong preference for minance-sensitive simple and complex cells respond to ori- that eye, but cells close to the ocular dominance band bor- ented bars or edges. Simple cells respond to properly ders show relatively mixed input. oriented bars of light at particular locations, while complex Finally, woven into the topographic map and ocular cells respond to properly oriented bars at any location with- dominance bands of V1 is a semi-regular arrangement in their receptive fields. Double-opponent cells in the pri- of neurons according to orientation preference. If one mary visual cortex allow the visual system to colour drives a recording electrode into the cortex obliquely and contrasts. The primary visual cortex has a complex hori- records the orientation preferences of many neurons, one zontal organization with overlapping maps of visual topog- sees that nearby neurons tend to have the same orientation raphy, ocular dominance and orientation tuning. and that the orientation preference of cells changes slowly as one moves tangentially through the cortex. These ‘orientation maps’ have been imaged optically, and the References shapes of areas containing neurons that share orientation Blasdel GG and Salama G (1986) Voltage-sensitive dyes reveal a preferences loosely resemble the leaves of a pinwheel modular organization in monkey striate cortex. Nature 321: (see Figure 7c). 579–585.

7 Visual System

Casagrande VA and Kaas JH (1994) The afferent, intrinsic, and efferent Werblin FS and Dowling JE (1969) Organization of the retina of the connections of primary visual cortex in primates. In: Peters A and mudpuppy, Necturus maculosus. II. Intracellular recording. Journal of Rockland K (eds) Cerebral Cortex, vol. 10, Primary Visual Cortex of Neurophysiology 32: 339–355. Primates, pp. 201–259. New York: Plenum Press. DeMonasterio FM and Gouras P (1975) Functional properties of gan- glion cells of the rhesus monkey retina. Journal of Physiology 251: 167– Further Reading 195. Hendry SH and Reid RC (2000) The koniocellular pathway in primate Burns ME and Baylor DA (2001) Activation, deactivation, and adap- vision. Annual Review of 23: 127–153. tation in vertebrate photoreceptor cells. Annual Review of Neurosci- Hubel DH (1995) Eye, Brain, and Vision. New York: Scientific American ence 24: 779–805. Library. Dowling JE (1987) The Retina: An Approachable Part of the Brain. Hubel DH and Wiesel TN (1962) Receptive fields, binocular interaction Cambridge, MA: Harvard University Press. and functional architecture in the cat’s visual cortex. Journal of Phys- Ferster D and Miller KD (2000) Neural mechanisms of orientation se- iology 160: 106–154. lectivity in the visual cortex. Annual Reviews of Neuroscience 23: 441– Kuffler SW (1953) Discharge patterns and functional organization of 471. mammalian retina. Journal of Neurophysiology 16: 37–68. Hassler R (1966) Comparative anatomy of the central visual systems in Livingstone MS and Hubel DH (1984) Anatomy and physiology of a day- and night-active primates. In: Hassler R and Stephen H (eds) system in the primate visual cortex. Journal of Neuroscience 4: Evolution of the Forebrain, pp. 419–434. Stuttgart: Thieme. 309–356. Leventhal AG (1991) The Neural Basis of Visual Function. London: Reid RC and Alonso JM (1995) Specificity of monosynaptic connections Macmillan Press Ltd. from thalamus to visual cortex. Nature 378: 281–284. McIlwain JT (1996) An Introduction to the Biology of Vision. Cambridge: Sompolinsky H and Shapley R (1997) New perspectives on mecha- Cambridge University Press. nisms for orientation selectivity. Current Opinion in Neurobiology 7: Wandell BA (1995) Foundations of Vision. Sunderland MA: Sinauer As- 514–522. sociates.

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