Stephen D Van Hooser, Brandeis University, Waltham, Massachusetts, USA Sacha B Nelson, Brandeis University, Waltham, Massachusetts, USA Humans and many other animals obtain much of their information about the world through their eyes. Patterns of light are transformed into nerve impulses in the retina and visual information is processed by nerve cells in the primary visual cortex. In the human brain, about one-half of the cerebral cortex is dedicated in some way to the processing of visual information. Anatomy of the Visual System Visual processing begins in the eye, where light passes through the lens and is focused on to photoreceptors in the retina. Axons of retinal ganglion cells, the output cells of the retina, leave the eye in a bundle called the optic nerve. At the optic chiasm, some axons cross over to the opposite hemisphere, so that axons representing the right half of visual space travel to the left hemisphere and axons representing the left half of visual space travel to the right hemisphere. From the optic chiasm, the retinal ganglion cell axons project to visual brain structures such as the lateral geniculate nucleus (LGN) of the thalamus, the superior colliculus in the midbrain, and the suprachiasmatic nucleus. In primates, 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 alternating fashion. The anatomy of the primate visual system is shown in Figure 1. There is a second major visual pathway to the neocortex from the retina via the superior colliculus. The superior colliculus projects to the pulvinar in the thalamus, which in turn projects to specialized regions of the visual cortex located beyond V1. In primates, the superior colliculus is known to be involved in eye movements, but it receives many fewer ganglion cell axons than the LGN. In many other mammals, such as carnivores and rodents, the superior colliculus receives a larger percentage of retinal afferents than in primates, and it is likely that the superior colliculus plays a larger role in vision in these animals. This article will focus on the pathway from the retina to the LGN to V1, since it is much larger in primates and is better studied than the pathway via the superior colliculus. Since brains are limited in size by developmental and energy constraints, the visual system does not represent all parts of the visual field equally, but instead emphasizes the area in the centre of the eye. The centre of the retina, called the fovea, contains the highest density of photoreceptors, and the fovea is represented by a disproportionately large Advanced article Article Contents. Anatomy of the Visual System. Concept of a Receptive Field. Retina. Focusing of Light on to the Retina. First Stage of Information Processing: Hyperpolarization of Photoreceptor Cells. Receptive Fields of Retinal Ganglion Cells. Relayof Signalsfrom the LateralGeniculate Nucleusto the Visual Cortex. Orientation and Directional Selectivity in Cortical Cells. Double-opponent Colour Cells in the Visual Cortex. Columnar Organization of the Visual Cortex. Beyond the Primary Visual Cortex. Summary doi: 10.1038/npg.els.0000230 number of cells in the LGN and cortex; almost half of V1, for example, represents the fovea. Visual information is gathered through active movements of the eyes to bring the Cornea Lens Retina Optic nerve Optic tract Optic radiations Optic chiasm Primary visual cortex (V1) Lateral geniculate nucleus (LGN) Figure 1 Anatomy of the visual system. Light arrives at the eye and is focused by the lens on to the retina, where photoreceptors transduce the light into electrical signals that are processed by local retinal neurons. Axons of retinal ganglion cells, the output cells of the retina, leave the retina in a bundle called the optic nerve. At the optic chiasm, some axons cross over, so that axons representing the right half of visual space travel to the left lateral geniculate nucleus (LGN) and axons representing the left half of 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 relay cell axons form a band called the optic radiations and project to the primary visual cortex, where LGN axons representing each eye ramify in an alternating fashion. ENCYCLOPEDIA OF LIFE SCIENCES 2005, John Wiley & Sons, Ltd. www.els.net 1
most informative parts of a scene into focus on the centre of the retina. Humans make over 100 000 such eye movements, or saccades, in a single day, typically one or more per second. By devoting large numbers of cells to a small region of visual space and moving the eyes to informative places in an image, the mammalian visual system affords higher resolution than would be possible in an animal with fixed eyes and equal brain size. Light PRL ONL OPL INL IPL GCL Rod Cone Horizontal cell Bipolar cell Amacrine cell Ganglion cell ON Stimulus OFF + Time Concept of a Receptive Field (a) To optic nerve (b) In each brain structure described here, an individual cell responds to images in a small part of the visual field and only responds strongly to particular image patterns. The part of the visual field to which a cell responds is called 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 of one neuron in the retina that is excited by light in the centre of its receptive field but inhibited by light in the surrounding part. Voltage Inverting synapse Noninverting synapse Stimulus on Time Hyperpolarizing/ depolarizing Inhibition/ excitation Centre light Surround light Retina The retina is a sheet of neurons and specialized receptor cells located in the back of the eye. As shown in Figure 2a, the retina consists of six layers: the photoreceptor layer (PRL), the outer nuclear layer (ONL), the outer plexiform layer (OPL), the inner nuclear layer (INL), the inner plexiform layer (IPL), and the ganglion cell layer (GCL). The organization of the layers is peculiar in that the photoreceptors are located at the back of the retina so that light passes through all of the layers before reaching them. The photoreceptors of the retina transduce light into electrical signals that are processed by the local neurons of the retina. The retinal ganglion cells are the only output cells of the retina, so all visual information available to the brain is transmitted by the axons of these cells. Focusing of Light on to the Retina Light enters the eye through a transparent portion of the external membrane of the eye (the cornea), passes through the lens and the vitreous space, and forms an image on the retina. Light is bent, or refracted, as it enters compartments that possess different refractive indices. This refraction permits the formation of a focused image on the retina. The lens contributes only about 1/4 of the refractory power of the eye (the remainder is due to the cornea), but because the shape of the lens can be actively adjusted, it allows objects at various distances to be brought into focus. (c) Figure 2 (a) The major cell types in the retina and their laminar organization. PRL 5 photoreceptor layer; ONL 5 outer nuclear layer; OPL 5 outer plexiform layer; INL 5 inner nuclear layer; IPL 5 inner plexiform layer; GCL 5 ganglion cell layer. (b) A centre surround retinal ganglion cell that responds to light in the centre of its receptive field and is 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 stimulus are shown on the right. Note that the cell responds most vigorously to a light spot in the centre surrounded by a dark annulus (second from the top), but the cell responds much less vigorously when stimulated by a large white spot (third from the top) because of the inhibitory surround. These properties are often denoted symbolically with the notation at bottom, with + indicating a preference for more light relative to background and 2 indicating less light. (c) Schematic diagram of retinal circuitry that mediates the centre surround cell depicted in (b). Light in the centre hyperpolarizes a cone, which excites a bipolar cell, which in turn excites the retinal ganglion cell. Horizontal cells mediate the effect of 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. First Stage of Information Processing: Hyperpolarization of Photoreceptor Cells The transduction of light into electrical activity occurs in two types of photoreceptors: rods and cones. Both rods and cones consist of an inner segment that contains the cell body and nucleus, and an outer segment containing a stack of membranous disks specialized for phototransduction. Rods have an elongated outer segment, are specialized for 2
detection of low intensity (scotopic) light, and are homogeneous in their wavelength sensitivity. Cones have a tapering outer segment, are specialized for detection of higher intensity (photopic) light, and individually are more sensitive to long (L-cones), medium (M-cones), or shorter wavelengths of light (S-cones). Comparisons of intensity across different wavelengths are the basis of colour vision. In the human retina there are approximately 100 million rods and 5 million cones. The most sensitive portion of the retina, the fovea, contains exclusively cones and the density of cones falls off with increasing distance from the fovea. Rods are absent in the fovea but are present throughout the rest of the retina. The proportion and distribution of rods and cones varies widely across animal species. In the dark, photoreceptors have a relatively depolarized membrane potential ( 2 40 mv) and continually release glutamate from their synaptic terminals. This depolarization is caused by continual activation of mixed cation channels located in the outer segments by cytoplasmic cyclic GMP. Current flow through these channels is termed the dark current. The dark current is opposed by a resting potassium conductance that would otherwise hyperpolarize the photoreceptor to 2 80 mv. Absorption of light activates the photopigment (rhodopsin in rod photoreceptors) and initiates a biochemical cascade that leads to activation of a phosphodiesterase, rapidly reducing cytoplasmic cgmp levels and thereby closing the cgmpsensitive cation channels. The effect of light is therefore to hyperpolarize the photoreceptor by shutting off the dark current. This hyperpolarization shuts off release of glutamate from the photoreceptor terminal. Receptive Fields of Retinal Ganglion Cells Most mammalian retinal ganglion cells have an opposing centre surround (or concentric) receptive field organization, which means they are excited by one stimulus in the centre of their receptive field and inhibited by another stimulus in the area surrounding this centre (Kuffler, 1953). An example of a centre surround cell that responds vigorously to a light spot surrounded by a dark annulus is shown in Figure 2b. Since neurons fire action potentials and cannot signal negatively, centre surround cells usually exist in two polarities. For example, most vertebrates possess a retinal ganglion cell type that responds to a light/dark contrast between its receptive field centre and surround, and in addition possess another retinal ganglion cell type that responds to a dark/light contrast between the centre and the surround. The fact that most retinal ganglion cells, such as the light/dark centre surround cell described above, respond to a contrast between two regions rather than absolute brightness allows the visual system to use the same circuitry to operate at different light levels. If one reads a newspaper outside on a bright sunny day, the absolute amount of light reflected from both the black text and the white page will be much greater than if one reads the same newspaper indoors. However, the contrast between the black text and the white page conveys meaningful information in both settings. Each retinal ganglion cell type receives input from a different arrangement of the local retinal circuitry. The local circuitry that produces the light/dark opponent retinal ganglion cell described above is shown in Figure 2c (Werblin and Dowling, 1969). Photoreceptors synapse directly on to bipolar neurons, which in turn provide the primary input to retinal ganglion cells. In the case of a light/dark opponent cell, the bipolar cell is excited by the photoreceptors. Horizontal cells, which make inhibitory connections to bipolar cells, provide surround inhibition to the bipolar cell, which then provides less excitation to the ganglion cell when there is light in the surround. Bipolar neurons that respond to a dark/light contrast between the centre and surround hyperpolarize in response to light in their centre regions because they receive sign-conserving synapses from their photoreceptor inputs. They are depolarized by the release of glutamate during the dark and then hyperpolarize back towards their resting membrane potential when glutamate release is shut off by light. Bipolar and ganglion cells that respond to a light/dark contrast between the centre and surround are called ON cells, while those that respond to a dark/light contrast between the centre and surround are called OFF cells. 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 motion. Thus, it is not surprising that there is a large diversity of retinal ganglion cell types (DeMonasterio and Gouras, 1975), although the precise number of these types and the exact qualities that identify each type are still a subject of debate. Ganglion cells are commonly grouped on the basis of their size and their axonal projections; cell types vary slightly from species to species, and here we describe cells found in the macaque monkey. Small ganglion cells projecting to the parvocellular layers of the LGN are called midget cells, while the larger ganglion cells projecting to the magnocellular layers of the LGN are called parasol cells. There is a third, less well studied class of cells that project to small cells throughout the LGN called the koniocellular cells. The midget cells are primarily responsible for seeing detail and colour. They comprise about 80% of all retinal ganglion cells and have very small receptive fields. In humans and Old World monkeys, the vast majority of midget cells are colour-opponent, being excited by red in the centre and inhibited by green in the surround or vice versa. It is important to note that this type of colour opponency does not correspond to a preference for a red/green contrast between the centre and surround, as such a neuron would 3
be excited by red in the centre and also be excited by green in the surround or vice versa; such double opponent cells are first seen in the primary visual cortex. Midget cells tend to respond to stimuli in a sustained manner, which means that they fire constantly to a constant stimulus. Parasol cells, by contrast, primarily mediate seeing motion and change. They make up about 10% of retinal ganglion cells, and have larger receptive fields than midget cells. There are few parasol cells in the fovea, but the ratio of parasol to midget cells increases with eccentricity. Parasol cells are insensitive to colour and instead are luminance-opponent. Unlike midget cells, parasol cells respond transiently to stimuli, which means they fire a few action potentials when a stimulus appears but do not fire constantly 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 (Hendry and Reid, 2000). Koniocellular cells are a heterogeneous 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, previously thought to be associated with a class of midget neurons, has been conclusively identified as koniocellular. Cells of this type are colour-opponent neurons excited by blue in the centre and inhibited by red or green in the centre. These cells have larger receptive field centre sizes than the midget cells and they lack a surround. Relay of Signals from the Lateral Geniculate Nucleus to the Visual Cortex After leaving the retina, midget, parasol and koniocellular cell axons enter the optic chiasm and travel to the LGN, where they segregate into layers based on eye of origin and cell properties. The layers of the LGN are shown in Figure 3. Layers 3 6 are the parvocellular layers, which receive input from midget cells, and layers 1 and 2 are the magnocellular layers, which receive input from parasol cells. Layers 1, 4, and 6 receive input from the contralateral eye, whereas layers 2, 3, 5 receive input from the ipsilateral eye. The koniocellular axons project to layers K1 K6, which are intercalated among the parvocellular and magnocellular layers, and koniocellular cells are also found diffusely throughout the entire LGN. Each layer of the LGN is organized topographically, which means there is a one-toone relationship between receptive field locations in the retina and those in the LGN, and that adjacent cells also have adjacent receptive field locations. Retinal ganglion cells make powerful synapses on to LGN cells, and measurements of LGN cell properties have shown them to be similar to those of the retinal ganglion cells that drive them. For this reason, the LGN is often 6 5 4 K6 K5 3 K4 K3 2 1 Figure 3 The lateral geniculate nucleus of the rhesus monkey. Midget cells of the retina innervate layers 3 6, and the parasol cells innervate layers 1 and 2. Koniocellular cells innervate K1 K6 but are also diffusely present throughout the entire LGN. 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 form a band called the optic radiations and travel to the primary visual cortex (see Figure 1). The LGN also receives massive direct and indirect connections from primary visual cortex, that can modulate signals from the retina in various ways. However, the functional role of these feedback connections and their modulation of the retinal input are incompletely understood. Upon arriving in the primary visual cortex (V1), axons from each of the three LGN neuron classes make synaptic contacts in different cortical layers. V1 is a six-layered structure, and a simplified wiring diagram of its connections is shown in Figure 6. The majority of input from the parvocellular cells arrives at a subdivision of layer 4 called layer 4B, while the magnocellular cells largely project to another layer called 4A. Cells in layers 4B and 4A primarily exhibit receptive field properties similar to the parvocellular and magnocellular neurons that provide their input. The koniocellular cells project to small bands of cells spanning layers 1 3 called blobs that will be discussed further below. Within the cortex, cells in layer 4 project to layers 2 and 3 throughout the cortex, and layers 2 and 3 cells in turn project to layers 5 and 6 in V1 and also project to adjacent cortical areas. Cells in layer 5 project to adjacent cortical areas and also to subcortical structures such as K2 K1 4
the superior colliculus. Finally, cells in layer 6 project back to the LGN. (Note that we have followed Casagrande and Kaas (1994) in using Hassler s labelling of V1 layers.) Orientation and Directional Selectivity in Cortical Cells With the exception of cells in the input layers 4A and 4B, luminance-sensitive neurons in V1 have very different receptive field properties from cells in the LGN. These cells respond best to edges or bars at a particular orientation (see Figure 4a), and these orientated edges are an important feature for the nervous system because they frequently define the boundaries of objects. V1 has two types of orientation-sensitive neurons, simple cells and complex cells (Hubel and Wiesel, 1962). Receptive fields of simple cells have separate regions that respond to light increments or light decrements, so simple cells respond to bars or edges at one particular position in space with a maintained response, as shown in Figure 4b. Complex cells, by contrast, Bar (a) ON OFF + + + + + + + + Bar (b) ON OFF respond to the presence of a bar located anywhere within their receptive fields, and thus do not have specific regions 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 respond to movement in one particular direction, as shown in Figure 4d. The synaptic connections and cellular mechanisms that underlie orientation selectivity are still a subject of debate. The investigators who first characterized simple and complex cells, David Hubel and Torsten Wiesel, proposed a theory describing how simple and complex receptive field properties could arise from input from LGN cells (or V1 layer 4A/4B cells) and other cortical cells. They suggested that simple cell responses could arise from feed-forward input from centre surround cells with co-linear receptive field centres of like signs as shown in Figure 5a. Such an arrangement would produce a cell with excitatory and inhibitory regions and orientation selectivity. The complex cell properties of orientation selectivity but indifference to precise positioning could arise from input from multiple adjacent simple cells with similar orientation preferences, 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 produced directly with synaptic input from centre surround neurons, but that complex cells require an additional layer of intervening neurons. In addition, simultaneous recordings of connected neurons in cat Bar (c) ON OFF 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 clockwise from vertical, but responds poorly to bars with other orientations. (b) Simple cells have separate regions of their receptive fields that respond to light increments and light decrements and thus respond to bars at specific locations. One example of such a receptive field pattern is shown. (c) In contrast to simple cells, complex cells respond to a properly oriented bar anywhere in their receptive fields. (d) Many cells in V1 respond to moving oriented bars. The arrows in the stimulus (left) indicate direction of bar movement. Most cells in V1 are orientation-selective and not directionselective, responding to movement in both directions (upper), but some cells are direction-selective and only respond to bars moving in a particular direction (lower). (d) + + + + + + + + + ++ (a) (b) Figure 5 Hubel and Wiesel s model for the formation of simple and complex receptive field properties. (a) A simple cell (at right) that responds to a dark, oriented bar on a light background could receive input from several adjacent centre surround cells that respond to light decrements in their receptive field centres. (b) A complex cell (at right) could obtain its indifference to bar position by receiving input from several adjacent simple cells (at left) sharing one orientation preference. The complex cell s receptive field properties cannot be represented in the same form as the schematics for the LGN cells and simple cell in (a) and the simple cells in (b). It responds to a properly oriented bar at any position in its receptive field. 5
LGN and V1 by Reid and Alonso show that an LGN neuron is much more likely to contact a V1 simple cell with an overlapping receptive field if the LGN neuron s receptive field centre has the same sign as the overlapping region in the simple cell s receptive field than if the two signs do not agree (Reid and Alonso, 1995). Another idea for generation of orientation selectivity posits that this selectivity arises from an interaction of synaptic input from centre surround cells and recurrent synaptic connections with other V1 neurons (Sompolinsky and Shapley, 1997). In this view, orientation-selective cells receive centre surround input that has a small orientation bias (not as strong as pictured in Figure 5a), and receive strong excitatory input from nearby V1 neurons with similar orientation preferences and inhibitory input from nearby cells with many different orientation preferences. When an oriented edge is observed, many V1 cells with an orientation preference close to that of the stimulus fire weakly initially, but over time the recurrent input from other V1 cells to V1 neurons with the proper orientation preference is amplified. This model is consistent with the experimental observations that orientation selectivity is sharpened over time and that orientation selectivity in one region of V1 can be disrupted by inactivation of cells in a V1 region hundreds of micrometres away. Double-opponent Colour Cells in the Visual Cortex Humans are able to perceive relationships between colours over a wide range of lighting conditions, which means they must be able to detect colour contrasts. In the LGN, the majority of neurons are colour-selective, being excited by one colour in one region of their receptive fields and inhibited by another colour in another region, but they do 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 opponency with a centre surround organization. They are excited by one colour in the centre of their receptive field and inhibited by another colour, and they are excited by this second colour in the surround region and inhibited by the first colour. For example, a double-opponent cell might be excited by red and inhibited by green in its centre, and be excited by green and inhibited by red in the surround (denoted r+g 2 /r 2 g+). These cells seem to only exist in four types: r+g 2 /r 2 g+, r 2 g+/r+g 2, b+y2 / y+b 2,b2 y+/y 2 b+, where b is blue and y is red and green together. Double opponent cells are found in regions of layers 2 and 3 that show increased staining for cytochrome oxidase, a mitochondrial enzyme shown to exist more densely in cells with generally higher activity since such cells require 1 2 3 4A V1 4B 5 6 Contralateral Ipsilateral Contralateral LGN To MT, V2 To superior colliculus more energy and thus have more mitochondria. These regions, called blobs for their appearance in tangential cortical sections stained for cytochrome oxidase are depicted in the wiring diagram in Figure 6. The blobs receive input from the koniocellular layers of the LGN, so it is possible that double-opponent cells get their receptive field properties only from input from koniocellular neurons; alternatively, they might receive input from the neurons in cortical layer 4B that receive input from the parvocellular LGN layers. Columnar Organization of the Visual Cortex To V2 Parvocellular contralateral Parvocellular ipsilateral Magnocellular contralateral Magnocellular ipsilateral Koniocellular contralateral Koniocellular ipsilateral Figure 6 Selected synaptic connections in the primary visual cortex. In each ocular dominance band, parvocellular LGN neurons from one eye project to cortical layer 4B, magnocellular LGN neurons project to layer 4A, and koniocellular LGN neurons project to the cytochrome oxidase blobs in layers 1 3. Neurons in layer 4 make connections with neurons in layers 2 and 3, both in the blobs and between the blobs, and these cells in turn project to layers 5 and 6. Cells in layers 2, 3 and 5 make connections with adjacent cortical areas, and cells in layer 5 also make connections with subcortical structures such as the superior colliculus. Finally, cells in layer 6 project back to the lateral geniculate nucleus. Adapted from Casagrande and Kaas (1994). In addition to the laminar organization described above, V1 has a considerable degree of horizontal organization at many scales. Like the LGN, V1 has a topographic representation of visual space, so that each position on the V1 sheet of cells corresponds to a particular point in visual space, and adjacent points on the sheet correspond to adjacent points in visual space (see Figure 7a). Within this topographic organization is a segregation of the input from the two eyes. Axons from the LGN relay cells mediating each eye ramify in layer 4 and in the blobs in an alternating fashion, as shown in Figure 6 and Figure 7b. Each of these ocular dominance bands is about 450 mm 6
Beyond the Primary Visual Cortex Figure 7 Horizontal organization of the visual cortex. (a) The topographic projection of visual space in the right visual hemifield on to an idealized, unfolded primary visual cortex (adapted from Hubel 1995). Note the large representation of the central region in V1, and the relatively small 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, 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 that the eyes are being stimulated with bars of different orientation. Each pixel in the image is colour-coded according to the bar orientation that evoked the largest response (see scale at right). For example, red regions in the image showed greatest activation by horizontal bars. (b) and (c) are reproduced with permission from Blasdel and Salama (1986). wide. All of the cells in layer 4 strictly respond to input from one of the two eyes, but in layers 2, 3, 5 and 6, the cell input is mixed. Neurons in layers 2, 3, 5 and 6 that lie in the centre of an ocular dominance band show a strong preference for that eye, but cells close to the ocular dominance band borders show relatively mixed input. Finally, woven into the topographic map and ocular dominance bands of V1 is a semi-regular arrangement of neurons according to orientation preference. If one drives a recording electrode into the cortex obliquely and records the orientation preferences of many neurons, one sees that nearby neurons tend to have the same orientation 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 shapes of areas containing neurons that share orientation preferences loosely resemble the leaves of a pinwheel (see Figure 7c). A complete discussion of other visual cortical areas is beyond 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 receptive 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 properties for sensitivity to motion or colour and form in the retina and LGN seems to be somewhat maintained in projections 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 magnocellular cells largely project to areas mediating the perception of motion; and cells in the blobs largely project to areas mediating perception of colour. These and intervening visual areas send many feedback connections to the visual cortex, and, as with the feedback connections to the LGN, the role of these connections is not well understood. Summary In the human visual system, signals travel from the retina to the lateral geniculate nucleus to the primary visual cortex. In the retina, photoreceptors transduce light into electrical signals that are processed by the local neurons of the retina, which in turn provide input to the retinal ganglion cells, the 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 have receptive fields with a centre surround organization. The lateral geniculate nucleus acts as a relay station between the retina and primary visual cortex. In the cortex, the luminance-sensitive simple and complex cells respond to oriented bars or edges. Simple cells respond to properly oriented bars of light at particular locations, while complex cells respond to properly oriented bars at any location within their receptive fields. Double-opponent cells in the primary visual cortex allow the visual system to sense colour contrasts. The primary visual cortex has a complex horizontal organization with overlapping maps of visual topography, ocular dominance and orientation tuning. References Blasdel GG and Salama G (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321: 579 585. 7
Casagrande VA and Kaas JH (1994) The afferent, intrinsic, and efferent connections of primary visual cortex in primates. In: Peters A and Rockland K (eds) Cerebral Cortex, vol. 10, Primary Visual Cortex of Primates, pp. 201 259. New York: Plenum Press. DeMonasterio FM and Gouras P (1975) Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology 251: 167 195. Hendry SH and Reid RC (2000) The koniocellular pathway in primate vision. Annual Review of Neuroscience 23: 127 153. HubelDH (1995) Eye, Brain, and Vision. New York: Scientific American Library. Hubel DH and Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat s visual cortex. Journal of Physiology 160: 106 154. Kuffler SW (1953) Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16: 37 68. Livingstone MS and Hubel DH (1984) Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4: 309 356. Reid RC and Alonso JM (1995) Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378: 281 284. Sompolinsky H and Shapley R (1997) New perspectives on mechanisms for orientation selectivity. Current Opinion in Neurobiology 7: 514 522. Werblin FS and Dowling JE (1969) Organization of the retina of the mudpuppy,necturus maculosus. II. Intracellular recording. Journal of Neurophysiology 32: 339 355. Further Reading Burns ME and Baylor DA (2001) Activation, deactivation, and adaptation in vertebrate photoreceptor cells. Annual Review of Neuroscience 24: 779 805. Dowling JE (1987) The Retina: An Approachable Part of the Brain. Cambridge, MA: Harvard University Press. Ferster D and Miller KD (2000) Neural mechanisms of orientation selectivity in the visual cortex. Annual Reviews of Neuroscience 23:441 471. Hassler R (1966) Comparative anatomy of the central visual systems in day- and night-active primates. In: Hassler R and Stephen H (eds) Evolution of the Forebrain, pp. 419 434. Stuttgart: Thieme. Leventhal AG (1991) The Neural Basis of Visual Function. London: Macmillan Press Ltd. McIlwain JT (1996) An Introduction to the Biology of Vision. Cambridge: Cambridge University Press. Wandell BA (1995) Foundations of Vision. Sunderland MA: Sinauer Associates. 8