Download Design Features in Vertebrate Sensory Systems

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
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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.,
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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
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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
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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
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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
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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). These are all
cases in which there is a preconception
about the overall function that the sensory
system is performing, so that the anatomical and physiological properties of the system can be related to a particular biological
role. It seems likely that future progress in
understanding the design of sensory systems will rely heavily upon a convergence
of behavioral and neuroanatomical and
neurophysiological approaches.
ACKNOWLEDGMENTS
The author's work is supported by PHS
Grant NS 12518. Maryellen Kurek provided photographic assistance. Debra
Hawkins typed the manuscript.
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