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AMER. ZOOL., 24:717-731 (1984) Design Features in Vertebrate Sensory Systems' PHILIP S. ULINSKI Department of Anatomy and Committee on Neurobiology, University of Chicago, Chicago, Illinois 60637 SYNOPSIS. All vertebrates face the problem of analyzing events in their environments. In spite of environmental differences, there are, however, aspects of the problems of analyzing external events that are common. It can be expected that sensory systems thus have certain common design features that reflect the functional constraints placed on sensory systems as information processing networks. This article surveys the organization of vertebrate sensory systems and identifies several major design features. The nature of design features and the assumptions underlying their definition are then discussed. INTRODUCTION Like all animals, vertebrates face the problem of analyzing events in their environments. The events vary from changing patterns of colored shapes in the case of primates, to reflected acoustic signals in the case of bats, to electric currents in water in the case of electroreceptive fishes, to infrared radiation in the case of rattlesnakes. Each species lives in a particular environment and copes with a specific set of sensory stimuli, but the problem of transforming events in the environment into neural codes and interpreting them in a way that provides a coherent and relevant picture of the external world is common. It is necessary in each case to transduce energy fluxes in the environment into the ionic fluxes that are the substrate for interactions within the nervous system (Beidler and Reichardt, 1970). The result of the transduction process is that information about the external world is coded in the nervous system in terms of either graded potentials or trains of propagated action potentials (Perkel and Bullock, 1968). Finally, information about the external environment provided by each system is processed or transformed, presumably by means of synaptic interactions between pairs or groups of neurons, in ways that affect subsequent behaviors. Sensory systems should thus have properties that are 1 From the Symposium on Evolution of Neural Systems in the Vertebrates: Functional-Anatomical Approaches presented at the Annual Meeting of the American Society of Zoologists, 27-30 December 1982, at Louisville, Kentucky. constant across sensory modalities and across species. They are what an engineer would call design features and they reflect the functional constraints placed on sensory systems as information processing networks. Knowledge of these design features is important in understanding the evolution of sensory systems, and thus of the nervous system as a whole, because they are among the factors that determine how the animal responds to sensory information. Any Darwinian model of neural evolution requires that environmental selection pressures will, through natural selection, modify the behavior of organisms. The design features of the sensory systems are the fundamental determinants of the sensory aspects of behavior. They establish the way in which an organism interprets its environment so that an immediate product of neural evolution must be changes in sensory system design features. Recognition and analysis of design features is then an obligatory initial step in understanding how evolutionary processes shape nervous system structure and function. This paper attempts to identify design features characteristic of vertebrate sensory systems. To aid in this endeavor, Figure 1 provides an impression of the overall organization of a "typical" vertebrate sensory system. The obvious caveat is that there are no "typical" cases; each set of receptors and neurons involved in processing sensory information has its own, characteristic features. Still, there are aspects of sensory system organization that have some generality. The first part of the 717 718 PHILIP S. ULINSKI FIG. 1. Structure of a generalized sensory system. The major features of vertebrate sensory systems are summarized in this diagram of a "typical" sensory system. Each box represents a population of neurons. The lines show the patterns of synaptic interconnections. Receptors are indicated as R,, ganglion cells as G,, brainstem and spinal cord structures as B,, dorsal thalamic structures as D, and D2, and telencephalic structures as T, and Tj. paper analyzes the organization of systems like that diagrammed in Figure 1, pointing out what seem to be their major design features. The second part of the paper turns to a discussion of the general significance of these features. ORGANIZATION OF INFORMATION PROCESSING NETWORKS Receptors Sensory systems all have receptors that transduce energy in the environment into the ionic fluxes that form the basis for neural codes. Receptors are indicated in Figure 1 by the boxes R, to RN. In the olfactory and vomeronasal systems, a single neuron serves both as a receptor and as the first neuron in a sensory pathway. In other cases, such as some of the somatosensory receptors, a receptor consists of the peripheral process of a neuron and accessory cells. However, many receptors, such as hair cells and photoreceptors, are specialized cells that are presynaptic to the first neurons in a particular pathway. There are broad classes of receptors such as photoreceptors, mechanoreceptors, etc., but it is now clear that there are subclasses of receptors, each of which has its own adequate, or natural, stimulus. Thus, photoreceptors include rods, green cones, red cones, blue cones and double cones (Walls, 1942), each of which is sensitive to a particular range of wavelengths. Electroreceptors include a complex variety of modified hair cells (Bullock, 1982), each of which codes a particular type of information. Each of the boxes, R,, can be regarded as a different subclass of receptors. The various receptor subclasses in each sensory system are arranged in a geometric array or receptor sheet. Hair cells in the inner ears of teleost fishes, for example, are arranged with their stereocilia and kinocilia oriented in particular patterns (Fay and Popper, 1980). These arrays appear to play a role in coding auditory parameters such as the locations of stimuli in auditory space. Somatosensory receptors are distributed in specific patterns over the body surface and within muscles, joints and fasciae. They often form complex arrays such as those present along the shafts of vibrissae (Andres, 1966), in Eimer's organs on the noses of moles (Andres and von During, 1973) or beneath the scales of lizards (von During and Miller, 1979). Different types of electroreceptors are distributed in the skin of electric fish in particular patterns (Carr et al., 1982). Photoreceptors in teleost fishes sometimes have very orderly, almost crystal-like, mosaic arrays (Hibbard, 1971). The structure of the receptor sheet has functional consequences because it is the array of receptors that samples information from the environment. For example, the environment is represented upon the retinal surface as a continuous function of light intensity and wavelength. The photoreceptors, however, have finite dimensions and numbers, so that the representation of the environment that reaches the brain is based on a finite sample from the continuous representation. The physical dimensions of the photoreceptor outer segments and the details of their distribution in the receptor sheet partially determine the properties of a transfer function SENSORY SYSTEMS that specifies the transformation of the light distribution function into the electrical activity of the total set of photoreceptors. The character of the receptor sheet varies throughout its spatial extent. There are regional specializations consisting of preferential accumulations of particular subclasses of receptors in specific regions of the receptor sheet. This occurs in the retina where cones accumulate in the foveas of primates or specific subclasses of cones accumulate in the red and yellow retinal fields of birds (Blough, 1979). It also occurs in the somatosensory system where there is an elevated density of mechanoreceptors on the palms of ground squirrels (Brenowitz, 1980). Regional specializations are exploited behaviorally when an animal orients towards a region of the environment that is of special interest, as when primates use directed eye movements to center a visual stimulus on the fovea or when rodents use their whiskers to sample physical objects in the environment. There are in some cases feedback projections from the central nervous system to receptors (Fig. 1). This occurs, for example, in many hair cells in the auditory, vestibular and ordinary lateral line systems (Warr, 1978; Goldberg and Fernandez, 1980). The efferent control exerted by gamma motoneurons on muscle spindles are a second example of a feedback system to receptors (Matthews, 1981). It is unlikely that such feedback systems have a single function, but it is clear that they provide a mechanism whereby the sensitivity of receptors can be adjusted to match the intensity of stimuli currently in the environment. Ganglion cells Receptors are generally contacted by the ganglion cells that carry sensory information into the central nervous system (CNS). An exception occurs in the retina where one or more neurons are interposed between the photoreceptors and ganglion cells. However, the entire retina is an outpocketing of the diencephalon, so that the retinal ganglion cells are actually CNS neurons and differ from cells in the dorsal root, trigeminal and lateral line ganglia, etc., 719 which develop from the neural crest or sensory placodes. From a functional viewpoint, retinal ganglion cells can be lumped with the other ganglion cell populations. Ganglion cells are indicated by the boxes G, to GN in Figure 1. Neurons in each of the ganglia vary in size and sometimes in morphology and transmitter substance. It is then possible to recognize subpopulations of ganglion cells, each of which is designated by a box G, in Figure 1. Each distinct population of ganglion cells has a particular set of physiological properties. This point has been best demonstrated in the case of cat retinal ganglion cells which are divided into morphologically distinct populations based on soma size, dendritic morphology and axon size and conduction velocity (Rodieck, 1979). Neurons in each population have specific physiological properties. The large neurons designated Y-cells, for example, have non-linear summation properties and respond well to phasic or transient stimuli while the smaller X-cells have linear summation properties and respond to tonic stimuli. The W-cells are smaller still and have a complex range of properties. The properties of different classes of ganglion cells, both in the retina and elsewhere, reflect in part the biophysical properties of the cells themselves (Koch et ah, 1982). However, each population of ganglion cells has a characteristic set of inputs so their functional properties are determined in large part by the receptor subclasses that they contact. The structure of the receptive fields of retinal ganglion cells in cats is determined by the classes of photoreceptor, bipolar and amacrine cells that contact them (Nelson et ai, 1978). Specific connections are made possible by the very precise spatial relationships that hold between retinal cells in the outer and inner plexiform layers. Retinal ganglion cells have axons resembling those of other CNS neurons. Neurons in the olfactory and vomeronasal epithelia and in the various ganglia are bipolar with one peripherally directed process and a second, centrally directed process. The central process bifurcates into ascending and descending branches, each of which 720 PHILIP S. ULINSKI issues many second order branches. These nuclear complex (Brugge and Geisler, collaterals result in information from a sin- 1978; Warr, 1982). This is a precisely orgagle ganglion cell being distributed to sev- nized array of many different types of neueral structures in the central nervous sys- rons. The ganglion cell axons effect syntem. The central processes of specific apses with several types of neurons, each classes of ganglion cells can now be visu- via an axon terminal that is morphologialized by using microelectrodes to deter- cally distinct and differs in its physiological mine the physiological properties of indi- effect. The various populations of cochlear vidual processes and then injecting them neurons have highly organized and varying with HRP. This procedure has been used projections to auditory structures, such as extensively to study the central processes the superior olivary nuclei, nuclei of the of cat dorsal root ganglion cells (Brown, trapezoid body, etc., deeper in the brain1981). It shows that the terminal arbors of stem. Similarly, the various populations of ganglion cells associated with receptor types dorsal root ganglion cells project in specific such as primary muscle spindles, Golgi ten- patterns to different populations of neudon organs and hair follicle afferents are rons in the gray matter of the spinal cord each morphologically distinct and termi- (Brown, 1981). These, in turn, effect spenate in specific regions of the spinal cord. cific connections with structures in the Similarly, the W-, X-, and Y-cell popula- brainstem. In spite of the complexity of tions of cat retinal ganglion cells each col- connections, the rule seems to be that there lateralize and terminate in specific regions are parallel pathways or channels that are of the brainstem (Giolli and Towns, 1980). established by the presence of different receptor types and different ganglion cell types and maintained to a greater or lesser Spinal cord and brainstem The central processes of ganglion cells extent as information flows from the carry sensory information into the spinal periphery into the central nervous system. A second property of sensory structures cord and brain. The central processes of is a consequence of these parallel pathways. neurons in the olfactory and vomeronasal It is a tendency for information from the epithelia terminate in the telencephalon. various receptor subclasses or ganglion cell The retinal ganglion cells terminate in the populations to be segregated within the diencephalon and mesencephalon. The brainstem structures. This property is best central processes of all other ganglion cells studied by systematically moving a microare presynaptic to neurons in metencephaelectrode through a given neural structure lon, myelencephalon or spinal cord. For while subjecting the animal to appropriate the sake of simplicity, the ganglion cell stimuli. Experiments of this sort typically populations in Figure 1 are shown termishow that information from each submonating in three structures, B, to B3, in the dality is represented in a specific subregion brainstem or spinal cord. There is a treof the nucleus or area under study. Hismendous variation in the organization of tological studies generally demonstrate that the structures that receive sensory inforeach of the subregions or areas is cytoarmation from ganglion cells, but there are chitectonically distinct. For example, the some trends. lateral line nerves in electric fishes carry First, ganglion cells associated with each information from ordinary lateral line of the major sensory systems project to receptors which are activated by mechanmultiple central targets. Neurons in each ical stimuli in the water and from several of the primary targets project in turn to different types of electroreceptors (Bulseveral secondary targets. An individual lock, 1982). Electrophysiological studies of neuron projects to only a single target in the posterior lateral line lobes, which some instances, but there are many cases receive information from the central proin which one neuron is known to project cesses of ganglion cells in the lateral line to several targets. For example, each neu- ganglia, show that information from each ron in the spiral ganglion within the inner receptor type is localized within a cytoarears of cats sends an axon into the cochlear SENSORY SYSTEMS 721 chitectonically distinct region of the lobe. such as color, position in auditory space, Similarly, the torus semicircularis in the velocity of visual targets, etc. that are not midbrain of catfish contains two represen- coded by position on any receptor sheet. tations of the lateral line receptor sheet, Central representations of variables of this one each for ordinary lateral line receptors sort would have to differ from the examples discussed in the previous section: they and electroreceptors (Knudsen, 1977). A third property of sensory structures is would have to be constructed in some way that there is often an orderly representa- by the central nervous system. This occurs tion of the receptor sheet. The most famil- in a representation of position in auditory iar arrangement involves a point-to-point space that is present in the nucleus mesor topological map between the receptor encephalicus lateralis pars dorsalis (MLD) sheet and neurons in a central nucleus or of the torus semicircularis of owls (Knudarea. The representations within topologi- sen, 1980). Part of MLD contains a repcal maps are orderly, but are generally resentation of auditory frequency. This is deformed to some extent. For example, a familiar topological representation of the the facial lobes in the medulla of catfish hair cell receptor sheet. An adjacent part contain a topologically organized repre- of the MLD lacks an orderly representasentation of the gustatory receptor sheet tion of auditory frequency. It is instead in which the representation of the head "space mapped" in that there is an orderly and barbels is disproportionately large representation of position in the auditory (Finger, 1978). The optic tectum of pigeons space that surrounds the owl. It is imporcontains a topologically organized repre- tant to understand that position in auditory sentation of the retinal receptor sheet in space is not coded in the hair cell receptor which the red and yellow fields are dispro- sheet and is not explicitly represented in portionately large (Clarke and Whitter- lower brainstem auditory structures. idge, 1976). The rules that determine such Rather, the connections that reach MLD differential magnifications of the receptor in some as yet unknown way construct a sheet are only partially known. However, representation of auditory space. The there is often a relationship between the neural mechanisms that underly such conmagnification factor in a given part of the structed representations are not known, but map and the density of receptors in the it seems clear that they must involve somecorresponding part of the receptor sheet thing more than simple point-to-point pro(Tusa et al., 1978). Thus, regions of the jections. They must involve non-topological receptor sheet that contain a high density maps. of receptors command a greater proporThese three properties can be summation of the central map. rized by saying that the sensory structures The truth of the matter is that we do of the spinal cord and brainstem tend to not really know the functional significance have multiple representations of each of topological maps. It is possible, of course, receptor sheet. These representations are that they lack any functional significance a reflection of the existence of parallel and reflect, instead, some underlying pathways or channels that can be traced developmental process or tend to facilitate from the receptor sheet, through the ganthe establishment of orderly connections glion cells and into the central nervous syswithin a structure. However, it is easy to tem. Some of the representations are see the potential behavioral value of orga- topological, but deformed, maps of the nized neural representations of variables receptor sheet, each representing inforsuch as position in visual space, sound fre- mation from a specific subclass of recepquency and body surface. It may be, then, tors. Other representations are non-topothat topological maps of receptor sheets logical or constructed representations. provide organized representations of Their significance is not yet clear, but they may be representations of parameters of behaviorally significant variables. sensory stimuli that are not encoded by An extension of this idea is that there position on the receptor sheet. should also be representations of variables 722 PHILIP S. ULINSKI Dorsal thalamus and telencephalon The retina and the sensory structures of the brainstem and spinal cord project to the dorsal thalamus, a major component of the diencephalon. It was clearly established by the first quarter of this century that the dorsal thalamus contains several cytoarchitecturally distinct nuclei in mammals and that some of these contain topologically organized maps of the visual, auditory and somatosensory receptor sheets. These thalamic sensory nuclei project in turn to discrete, sensory areas of the cerebral cortex (Jones, 1981a). Thus, the sensory pathways or channels that we have been following from the receptor sheet into the central nervous system extend through the dorsal thalamus and to the cerebral cortex in mammals. The situation in non-mammalian vertebrates has been less clear. One influential theory held that the establishment of discrete dorsal thalamic nuclei with projections to the telencephalon was a major step in the evolution of the mammalian pattern of forebrain organization (see Diamond and Hall, 1969). However, the application of modern axonal tracing techniques to nonmammals, beginning in the mid 1960s, demonstrated that there are discrete sensory representations in both the dorsal thalamus and telencephalon of vertebrates in each of the major groups (Ebbesson et al., 1972). This holds for the visual, auditory and somatosensory systems as well as the lateral line systems of fishes. The existence of discrete pathways from the receptor sheet through the dorsal thalamus and to the telencephalon is thus a basic vertebrate characteristic and is indicated in Figure 1 by connections involving two thalamic (D, and D2) and two telencephalic (T, and T2) structures. Significant variations related to the subsequent embryology of the telencephalon occur among the major groups of vertebrates (Northcutt, 1981). The telencephalon evaginates during development to produce paired cerebral hemispheres that contain lateral ventricles in amniotes, elasmobranches, agnathans and lungfishes. However, the telencephalon undergoes a developmental process in which it everts to produce hemispheres that lack lateral ventricles in actinopterygian fishes. There are significant variations among groups within each of these two basic patterns. So far, we have detailed information on thalamic and telencephalic organization only in reptiles, birds and mammals. Reptiles and birds share one basic pattern of forebrain organization while all three subclasses of Recent mammals share a second pattern. The situation in mammals is better understood and can be discussed first. (1) Dorsal thalamus in mammals. The dorsal thalamus in mammals contains discrete nuclei associated with the sensory systems (Jones, 1981a). The ventrobasal complex receives somatosensory information from the spinal cord, trigeminal nuclei and the dorsal column nuclei of the brainstem. The posterior nuclear group lies adjacent to the ventrobasal complex and also receives somatosensory inputs. The medial geniculate complex receives auditory information from the inferior colliculi of the caudal midbrain. Two nuclear complexes receive visual information. The dorsal lateral geniculate complex receives visual information primarily from the retina and secondarily from the superior colliculi in the rostral midbrain. The pulvinar and lateral posterior nuclei form a second complex that receives visual information from the superior colliculus, the pretectum and visual cortex. These nuclei share several organizational principles. Each receives one or more topologically organized maps of the appropriate receptor sheet. The dorsal lateral geniculate complex, for example, receives a topologically organized representation of the retina (Guillery et al, 1980) and the ventrobasal complex receives a topologically organized representation of the body surface (Welker, 1973). A second principle is that each individual region of the receptor sheet is represented as a column of tissue that extends perpendicular to the representation of the receptor sheet. Thus, an electrode that advances through the dorsal lateral geniculate complex perpendicular to the representation of the retinal surface will encounter units that respond to stimuli SENSORY SYSTEMS in the same region of visual space (Kaas et al., 1972). Similarly, there are isofrequency lamellae in the medial geniculate complex and columnar representations of the body surface in the ventrobasal complex (Jones et al., 1982). A third principle is that each dorsal thalamic sensory nucleus contains several morphologically distinct types of neurons. It was classically held that the largest were relay neurons that project to the cerebral cortex while the smaller were interneurons that affected synaptic interactions only within the given thalamic nucleus (Jones, 1981a). However, it is now apparent that at least some of the smaller thalamic neurons are also involved in projections to the cerebral cortex (Friedlander et al., 1981). They are thus not true interneurons, but the possibility exists that they also participate in local interactions within the thalamus remains. A fourth principle is that all of the dorsal thalamic sensory nuclei contain glomeruli or complex arrays of synapses in which the dendrites of some neurons are presynaptic to the dendrites of other neurons (Jones, 1981&). The functional significance of glomeruli remains obscure. Finally, each sensory nucleus receives topologically organized corticothalamic projections whose function, again, is not certain (Frigyesi et al., 1972). There is some evidence for modality segregation within dorsal thalamic sensory nuclei. The dorsal lateral geniculate complex in many mammals is divided into layers or laminae (Kaas et al., 1972). The number and character of these layers varies substantially between species. The rules that underlie the variation are not entirely clear, but there is no evident correlation between degree of lamination and phylogenetic position. Thus, distinct laminae are seen in carnivores, some rodents, primates, tree shrews, and some marsupials. There are indications that each layer receives a particular subset of visual information. For example, different classes of retinal ganglion cells terminate in different geniculate layers in cats, primates and tree shrews (Rodieck, 1979). In mink, some of the layers are divided into two leaflets; one leaflet contains neurons with on-center receptive fields and the other leaflet contains neu- 723 rons with off-center receptive fields (LeVay and McConnell, 1982). Some degree of modality segregation is also present in the ventrobasal complex of macaque monkeys in that the central core of the nucleus receives information from cutaneous mechanoreceptors whereas the outer shell of the nucleus receives information from muscle spindles (Jones etal., 1982). Finally, the medial geniculate nucleus contains a series of binaural interaction bands within its isofrequency lamellae (Middlebrooks and Zook, 1983; Moore, 1983). (2) Telencephalon in mammals. T h e iso- cortex forms the dorsolateral surface of the cerebral hemispheres in mammals and contains representations of the various sensory receptor sheets (Merzenich and Kaas, 1980;Woolsey, 1981a,*, 1982; Kaas, 1982). The number of these representations varies. Monotremes such as the echidna and duckbilled platypus (Lende, 1969; Bohringer and Rowe, 1977) have only a single representation of the visual, auditory and somatosensory receptor sheets while other mammals have two or as many as a dozen representations of each receptor sheet. Some of the representations are topologically organized. It used to be thought that each topological map was a deformed but intact representation of the receptor sheet. This is sometimes true, but in many cases there are splits or discontinuities in the maps. Thus, there are discontinuities in the representation of visual space in several of the cortical visual areas in primates (Allman, 1977). The representations of the body surface in squirrels, prosimian primates and monkeys seems to be broken up into a series of blocks, each of which contains a continuous representation of part of the body surface (Kaas et al., 1981). Kaas and his co-workers have hypothesized that the presence of these "blocks" represent solutions to the problem of packing a highly deformed representation into the smallest possible area. When two representations of a receptor sheet lie next to each other, they tend to be mirror images of each other (Kaas, 1982). The representations thus meet along a common border. The significance of such common borders is not known, but it is 724 PHILIP S. ULINSKI possible that they reflect the developmental properties of the system rather than any property with behavioral significance. In cases where adequate information is available, it appears that each map within a set of multiple maps carries information from a different subclass of receptors or ganglion cells. Those maps that are not topologically organized either have units with large receptive fields and lack any discernable organization, or contain constructed representations. A constructed representation occurs in the auditory cortex of bats (Suga, 1982). Some of the auditory areas of bats contain topological representations of the hair cell receptor sheet. However, there are additional areas that lack representations of frequency. There are instead representations of several of the variables used by the bat in echolocation. The simplest is an orderly representation of the temporal delay between the time the bat emits an echolocating pulse and the time the echo returns to the bat. This is of course a measure of the distance between the bat and an external object. Other variables, such as the Doppler shift of the echolocating pulse, are more complex; but in all cases they are variables not encoded in the hair cell receptor sheet. Regardless of the number of sensory areas, the entire isocortex has a common histological structure in monotreme, marsupial and placental mammals (Lorente De No, 1938). There are two layers that have large populations of pyramidal neurons whose apical dendrites extend perpendicular to the pial surface. These are the major sources of efferents from the cortex. The smaller pyramidal neurons in the second and third layers give rise to the commissural and association projections that link together the two sides of the brain and the various cortical areas on each side of the brain, respectively (Jones and Wise, 1977). Larger pyramidal neurons in layerfivegive rise to projections to the basal ganglia and to the brainstem and spinal cord (Wise and Jones, 1977). Finally, pyramidal neurons in the sixth layer are the origin of the corticothalamic projections and efferents to the claustrum (LeVay and Sherk, 1981). The remaining layers contain a range of non-pyramidal neurons (Jones, 19816; Lund, 1981). These include neurons with stellate-shaped dendritic fields that are particularly common in the fourth layer. The projections from the thalamus to the cortex are extensive and complex, so that each particular area of the isocortex receives its own particular pattern of thalamocortical projections. Diamond (1979) has recently discussed some aspects of thalamocortical organization. He points out that each of the major sensory modalities is represented by a field of cortical areas, each of which contains a representation of at least part of the receptor sheet. Each field receives projections from a cluster of dorsal thalamic nuclei. One nucleus usually projects exclusively, or predominantly, to a single area within the field. Thus, the dorsal lateral geniculate nucleus in primates projects predominately to the primary visual area of the cortex. Similarly, the central core of the ventrobasal nucleus projects predominately to area 3b of the somatosensory field. The other components of the thalamic complex project more extensively to the cortical field, with a single thalamic neuron often projecting to two or more areas via collaterals. The pulvinar in primates projects extensively to the socalled extrastriate visual areas of the cortex. The more caudal part of the ventrobasal complex and the posterior nuclear complex in cats projects widely to areas in the somatosensory field. We are still cataloging the substantial interspecific variation that occurs in thalamocortical projections in mammals so it is not yet clear what rules, if any, prevail. Each of various thalamocortical projections terminates in a specific layer or layers of the appropriate cortical field, as well as within a particular area. It is now clear that thalamic projections reach essentially all of the cortical layers and synapse upon at least most of the neuronal types present in isocortex (White, 1979). However, a particularly extensive projection from the thalamus terminates in the fourth layer and synapses heavily on the stellate neurons prevalent in that layer. These projections arise to a large extent from larger thalamic SENSORY SYSTEMS neurons in each nucleus and terminate in axonal arbors that are relatively restricted in size (Penny et al., 1982). By contrast, projections to the upper layers originate from smaller thalamic neurons and terminate in arbors that branch extensively. A consequence of the projections that interconnect the thalamus and cortex is that each population of cortical neurons receives its own particular mix of thalamic inputs. There is evidence, particularly in the visual projections to the cortex, that the various parallel pathways or channels that we have traced from the periphery to the thalamus are maintained to the cortical level (Stone et al., 1979; Lennie, 1980). Thus, each of the laminae of the lateral geniculate nucleus projects to a particular pattern of cortical layers. Since there is a segregation of inputs to the geniculate laminae, there is also a segregation of pathways to the cortex. The segregation becomes less clear at this juncture by virtue of the connections effected within the cortex by the axons of cortical cells. Thus, there are neurons in the visual cortex that receive convergent information from both the Y-cell and X-cell channels that have been maintained distinct up to this point. A second consequence of the pattern of thalamocortical projections is that the isocortex can be divided into a series of vertical units (Mountcastle, 1979). These were originally called columns, but it is now clear that they have the form of irregularly shaped bands. Each column contains units that code information about a particular aspect of a sensory stimulus and is determined in part by the spatial organization of thalamic afferents. There are ocular dominance columns in visual cortex (Hubel and Wiesel, 1977). These are alternating bands that receive information from either the ipsilateral or contralateral eye. There are submodality columns in the sensory cortex that receive information from rapidly or slowly adapting cutaneous receptors (Sur et al., 1981). There are binaural interaction columns in the auditory cortex of cats (Imig and Adrian, 1977). These columns all bear some resemblance to constructed representations or non-topological maps because they are representations 725 of variables that are not encoded by position on the receptor sheets. (3) Dorsal thalamus in reptiles and birds. One of the significant contributions in comparative neurology during the last few decades was the demonstration that both reptiles and birds, like mammals, have discrete dorsal thalamic nuclei associated with each of the sensory systems (Ebbesson et al., 1972). The pattern is the same across species and can be illustrated in the case of crocodilian reptiles. There is a nucleus situated in the rostrolateral part of the dorsal thalamus (the dorsal lateral geniculate complex) that receives visual information directly from the retina. A second visual nucleus (nucleus rotundus) lies centrally in the dorsal thalamus. It receives visual information indirectly, via the optic tectum. An auditory nucleus (nucleus reuniens) lies in the caudomedial part of the dorsal thalamus. It receives auditory information from the torus semicircularis in the midbrain. Finally, a somatosensory nucleus (nucleus medialis posterior) lies caudal to nucleus rotundus. It receives ascending projections from the spinal cord and dorsal column nuclei. We know a great deal less about the organization of dorsal thalamic nuclei in reptiles and birds than we do in mammals. It is known for both the turtle Pseudemys scripta (Ulinski, 1980) and the owl (Pettigrew, 1979) that retinal projections to the geniculate complex are topologically organized. However, the projections from the optic tectum to nucleus rotundus appear non-topologically organized in both reptiles (Rainey and Ulinski, 19826) and birds (Benowitz and Karten, 1976). The organization of these projections has been studied using the orthograde transport of HRP. The optic tectum of both turtles and snakes receives a topologically organized representation of the retinal receptor sheet. The optic tectum projects to nucleus rotundus in the dorsal thalamus. However, restricted lesions of the tectum produce degeneration that is scattered throughout nucleus rotundus, suggesting the absence of a pointto-point projection from the tectum to rotundus. We have demonstrated this point explicitly by using the orthograde trans- 726 PHILIP S. ULINSKI port of HRP to visualize the tectorotundal rior dorsal ventricular ridge (ADVR), and axons in Pseudemys scripta (Rainey and to a structure situated between ADVR and Ulinski, 19826) and Thamnophis sirtalis the cortex that has usually been called the (Dacey and Ulinski, 1983). These experi- pallial thickening in reptiles. The pattern ments show that each tectorotundal axon of the thalamotelencephalic projections is extends through rotundus issuing wide- constant across species (Ulinski, 1983). The spread collaterals so that a given neuron auditory thalamic nucleus projects to an in nucleus rotundus can potentially receive area in the caudomedial aspect of ADVR. information from neurons throughout the Somatosensory projections appear to teroptic tectum and, consequently, from all minate in the central part of ADVR, but points in visual space. This is consistent this point has been established for only a with physiological experiments showing few species. Nucleus rotundus projects to that units in nucleus rotundus of pigeons a rostrolateral area in ADVR. The genichave widefield receptive fields and respond ulate complex projects to the pallial thickto stimuli throughout much of visual space ening (and perhaps part of the dorsal edge (Revzin, 1979). The functional significance of the cortex) in reptiles (Bruce, 1982). This of this non-topological map is not known, projection appears quite different in birds. but Revzin has suggested that nucleus The geniculate complex projects bilaterrotundus may contain a constructed rep- ally to a region on the dorsal surface of the resentation of visual parameters such as hemisphere (Miceli etal., 1975) that is called directional preference or target velocity. the Wulst (which is German for a "swellThe intrinsic organization of dorsal tha- ing" or "bump"). However, embryological lamic nuclei in reptiles or birds has been studies of the telencephalon in chicks show studied only in the case of nucleus rotun- that the neurons that are destined to condus (Rainey and Ulinski, 1982a) and the tribute to the Wulst are initially situated lateral geniculate complex in Pseudemys adjacent to ADVR—in exactly the position (Ulinski, 1982). All of the neurons in these occupied by the pallial thickening in repnuclei appear to project to the telencepha- tiles (Tsai et al., 1981a, b). They are sublon and there is no evidence for classical sequently shifted dorsomedially during the interneurons. Nucleus rotundus contains development to gain their adult position. aggregations of axon terminals around the The histological structure of ADVR difcomplex appendages that are common on fers fundamentally from that of isocortex rotundal neurons; there is no indication of in that it lacks pyramidal neurons (Ulinski, presynaptic dendrites. However, glomeruli 1983). Most of its neurons have stellate similar to those in mammals do occur in dendritic fields with dendrites that are covthe dorsal lateral geniculate complex of ered to a varying extent by spines. A domPseudemys. Reciprocal dendrodendritic inant feature of ADVR neurons is their synapses occur between the principal neu- tendency to form clusters of neurons with rons in that portion of the geniculate com- apposed somata. In some species there are plex that receives retinal synapses. They gap junctions between apposed neurons. are found in glomeruli that involve den- The function of such clusters is not known, drites and retinal terminals. but they may form a substrate for complex (4) Telencephalon in reptiles and birds. Thesynaptic interactions. The distribution of telencephalon in reptiles and birds lacks a the clusters varies between species. In all region that is structurally similar to the reptiles except crocodilians, there is a tenisocortex of mammals. It is dominated dency for clusters to be particularly prominstead by the dorsal ventricular ridge inent in a zone located near the ventricular (DVR) that protrudes into the lateral ven- surface of ADVR. In crocodilians and birds, tricle (Ulinski, 1983). The cortex that lies clusters are spread evenly throughout above the lateral ventricle represents the ADVR and there is little tendency for a cortical component of the limbic system. cell cluster zone. The dorsal thalamic sensory nuclei proLittle is known about the internal orgaject to the anterior part of DVR, the ante- nization of ADVR. The auditory area in SENSORY SYSTEMS birds (Bonke et ai, 1979) and crocodilians (Weisbach and Schwartzkopf, 1967) contains a topological representation of the hair cell receptor sheet. There is some indication of a vertical organization in that electrode penetrations that pass perpendicularly through the area encounter units with the same best frequency. There is also evidence for a topological representation of the surface of the bill in ADVR in ducks and pigeons (Berkhoudt^ ai, 1981). However, the projection of nucleus rotundus to the visual area in ADVR appears to be nontopological (Balaban and Ulinski, 19816). DESIGN FEATURES AS HYPOTHESES The preceding paragraphs have provided the briefest possible overview of our current understanding of the organization of vertebrate sensory systems. In spite of the substantial interspecific variation that is seen in the brains of vertebrates, there are some aspects of the design of sensory systems that emerge as common if not general features. These include: the existence of multiple populations of receptors distributed over a receptor sheet; the existence of multiple populations of ganglion cells each with specific properties and inputoutput relationships; the existence of multiple representations in the brain stem, spinal cord and forebrain; the existence of parallel pathways; the existence of topological and non-topological maps; and the presence of feedback connections at many sites in the system. I wish to discuss two issues in this section. The first is how these particular properties can be singled out from all others and designated as design features. The answer, I think, requires some preconception about the overall function of the system being discussed. In the case of sensory systems, the working assumption is that there are systems in the brain that are transforming or processing sensory information in ways that lead ultimately to the formation of what humans would call "perceptions" i.e., representations of the external world that form a basis for the various behaviors present in the organism's repertoire. The problem of understanding the 727 genesis of perceptions is, of course, a longstanding one, but contemporary neurobiologists have converged over the past four decades on the idea that neurons or groups of neurons can perform computations or calculations in a way that is roughly analogous to those performed by computers. When we look at the design of sensory systems, we are then searching for analogues to features that are known or believed to be important in the construction of humanmade information processing systems. Design features in sensory systems are those that can reasonably be supposed to be of significance to the overall functions of the system, based on our knowledge of other information processing devices. This strategy of comparing biological and human designed systems that subserve similar functions is a common one in functional morphology. Biologists interested in musculoskeletal systems commonly borrow concepts of stress, strain, force, etc. from mechanical engineering. Biologists interested in fluid flow borrow concepts of Reynolds numbers, laminar flow, turbulence, etc. from hydraulic engineers. Auditory physiologists borrow concepts from acoustic engineering, and so forth. Analyses of sensory systems are coming in a similar way to rely more and more extensively upon ideas borrowed from computer and systems science. This began in the 1940s with the work of McCulloch and Pitts (McCulloch, 1965) which viewed groups of neurons as performing logical computations. Wiener (1948) developed the idea of control or cybernetic systems as applicable to the nervous system. By the 1960s, Eccles et al. (1967) summarized the organization of the cerebellum in a book entitled The Cerebellum as a Neuronal Machine. T h e r e has been an increasing tendency for neurobiologists to develop theories of neural function using concepts from systems or computer science. These include control system models of the vestibulo-ocular system (Robinson, 1981), network theories of cerebellar function (Pellionisz and Llinas, 1982) and computation theories of vision (Marr, 1982). The nervous system is approached in each case by searching for the design features that are believed to be 728 PHILIP S. ULINSKI important in a particular type of information processing system. A second issue is what to do after design features have been designated. It is important to stress that the recognition of design features per se is only a first step. For example, there is now ample evidence that vertically organized columns or bands are a general feature of mammalian sensory cortex and increasing evidence that similar structures exist in non-mammals. Such columns can be legitimately designated as design features that are analogous to modular elements in human designed information processing machines. Research on cortical columns has proceeded by attempting to determine their anatomical and physiological properties. The questions have been: What are the anatomical substrates for columns? What kinds of columns are there? How are columns distributed in the cortex? Although we now know something about the properties of columns, we know almost nothing about their biological role or how they are related to the behavior of the animal. The same situation holds for other design features such as topological and non-topological maps, parallel pathways, etc. The next, and more difficult, step must be to relate design features in the brain of a given species to the animal's behavior. The best progress seems to be made when a specific and well-defined behavior is the focus of study. There have been, for example, recent advances in understanding how the visual system perceives three-dimensional objects (Marr, 1982), how electric fish alter the frequency of their electric organ discharge to avoid jamming the signals sent by their neighbors (Bullock, 1982) and how bats use echolocation to localize objects in space (Suga, 1982). 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