| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Review
Department of Anatomy, University of Wisconsin, School of Medicine, Madison, Wisconsin 53706
Submitted 7 April 2003; accepted in final form 24 April 2003
ABSTRACT
Recent observations of single axons and review of older literature show that axons afferent to the thalamus commonly branch, sending one branch to the thalamus and another to a motor or premotor center of the brain stem. That is, the messages that the thalamus relays to the cerebral cortex can be regarded as copies of motor instructions. This pattern of axonal branching is reviewed, particularly for the somatosensory and the visual pathways. The extent to which this anatomical evidence relates to views that link action to perception is explored. Most pathways going through the thalamus to the cortex are already involved in motor mechanisms. These motor links occur before and during activity in the parallel and hierarchical corticocortical circuitry that currently forms the focus of many studies of perceptual processing.
INTRODUCTION
"If I could only move my hand about I should know what the things
were."—Patient reporting on failure to identify objects by
touch after removal of cortex limited to the precentral cortex
(Horsley 1909
).
The thalamus has for long been regarded as a "sensory relay"
passing sensory inputs to the cerebral cortex for perceptual processing along
corticocortical pathways (Fig.
1A). Evidence presented elsewhere
(Guillery and Sherman 2002a),
and briefly summarized below, shows that most axons carrying information to
the thalamus are branches of axons whose other branch innervates motor or
premotor centers (Fig.
1B). Some of these axons go to the thalamus along
ascending (sensory) pathways; others come from the cortex itself. That is, the
thalamus passes to cortex information that copies instructions being
sent concurrently to motor or premotor centers (a corollary discharge; see
Sommer and Wurtz 2002). This
pattern of branching afferents leads to a focus on the close and potentially
important link between the afferent, sensory messages, passed to the cortex
for perceptual processing on the one hand, and to motor centers for concurrent
motor action on the other. Although perceptual processing is today often
treated as though it were an independent activity, based on what Churchland et
al. (1994) for vision have
aptly described as a "Theory of Pure Vision," there have been many
earlier arguments to link perceptual processing closely to motor action. In
the following review, current knowledge of thalamocortical pathways will be
presented and related to views that link action to perception. Recent evidence
about patterns of axonal branching in afferents to the thalamus will be
summarized for the somatosensory and visual pathways. This evidence will then
be related to older evidence and to views of perceptual processing.
|
AFFERENTS TO THE THALAMUS PROVIDE KEY FUNCTIONAL INPUTS FOR CORTEX
Essentially all areas of the neocortex receive afferents from the thalamus. For some cortical areas, such as primary visual or somatosensory areas (V1, S1), this thalamic input is seen to dominate the functional properties of the cortical cells. These thalamocortical afferents pass to the cortex the main, "driving input"1 that the thalamic relay cells receive from the optic tract or medial lemniscus. The functional organization of these pathways, including cortex, has been studied in terms of the receptive field properties of their neurons. The fact, considered below, that many of the afferents to the thalamus are branches of axons that also innervate motor centers has not contributed significantly to an analysis of the message that is being passed to the cortex. The analysis has generally related to perception, not to action.
For most "higher" cortical areas, in contrast to V1 or S1, the functional role of the thalamic afferents (shown as interrupted lines in Fig. 1A) remains unexplored. However, these higher cortical areas also receive afferents from thalamic relay cells, and these relay cells are innervated from the cortex by axons that, like the lemniscal and optic pathways, also have branches to motor or premotor centers (Fig. 1B). All of these branching afferents to thalamus, both ascending and corticothalamic, can provide a new view of the messages that the thalamus passes to the cortex.
In most contemporary studies of the cortex, as illustrated in
Fig. 1A,
thalamocortical connections dominate the functional analysis of primary
cortical areas (V1, S1, A1), whereas corticocortical connections dominate the
analysis of higher cortical areas (e.g.,
Born 2001;
Mishkin et al. 1983;
Sereno et al. 2002;
Van Essen et al. 1992). At
present there are no reasons for treating the thalamic input to some cortical
areas, such as V1, S1, or A1 as having prime importance, and ignoring this
input for other cortical areas. There are only practical reasons for not
including these other thalamocortical axons: much less is known about them and
they have proved hard to study.
Recent evidence, based on filling and tracing corticothalamic axons shows
that, whereas essentially all thalamic relays receive afferents from cortical
layer 6 (not illustrated in the figure), only some receive afferents from
layer 5 (e.g., Abramson and Chalupa
1985; Bourassa and
Deschênes 1995; Bourassa
et al. 1995; Gilbert and Kelly
1975; Ojima 1994).
These two types of corticothalamic axon are distinct in their light and
electron microscopic appearance, in the pattern of their thalamic synaptic
contacts (Guillery 1995;
Guillery and Sherman 2002b;
Rouiller and Welker 2000;
Sherman and Guillery 2001;
Vidnyánsky et al. 1996), and in their known functional roles. Whereas
layer 6 axons have small terminals that contact peripheral dendritic segments
and modulate transmission in the thalamus, layer 5 axons are large, resemble
the contacts of lemniscal or retinal afferents, contact proximal dendritic
segments (Feig and Harting
1998; Guillery et al.
2001; Mathers 1972), and act as "drivers" (footnote 1,
and Guillery 1995; Sherman and
Guillery 1998,
2001, 2002). That is, where
the function of layer 5 cells has been tested by silencing their cortical
origin, they are seen to transmit receptive field properties to the thalamus
(Bender 1983;
Chalupa 1991;
Diamond et al. 1992), and in
this they differ from layer 6 afferents
(Geisert et al. 1981;
Kalil and Chase 1970;
Schmielau and Singer
1977).
CORTICOFUGAL AXONS ARISING FROM LAYER 5 PYRAMIDAL CELLS
The layer 5 axons innervate the thalamic relay cells that project to higher
cortical areas, serving to send messages through the thalamus from one
cortical area to another (Fig.
1B). More important, for understanding the messages that
reach higher cortical areas, layer 5 corticothalamic axons, like many
ascending axons to thalamus, are also branches of axons going to motor or
premotor centers in the brain stem
(Bourassa and Deschênes
1995; Bourassa et al.
1995; Guillery et al.
2001; Rockland
1998; and see figure). That is, these corticothalamic axons send
copies of motor instructions to the thalamus for transmission to other
cortical areas.
Where one or a few axons are traced from visual or somatosensory cortex to
their terminal sites in the thalamus one sees that the layer 6 axons (not
shown in the figure) never extend beyond the thalamus, whereas layer 5 axons
also have branches that continue caudally to the tectum or pons
(Bourassa and Deschênes
1995; Bourassa et al.
1995; Rockland
1998). For visual areas 17 and 18 of the cat, each corticothalamic
axon with terminals in the pulvinar also sends a branch to the midbrain.
Further, no axons go to the midbrain without first sending a branch to the
pulvinar (Guillery et al.
2001). Details of branching patterns of corticothalamic
projections for many cortical areas still remain to be defined.
Layer 5 corticothalamic axons represent the drivers to thalamic nuclei
whose driver input had for long been undefined. Specifically, for the pulvinar
of the cat (Bender 1983;
Chalupa 1991) and the
posterior nucleus of the rat (Diamond et
al. 1992) they provide the characteristic thalamic receptive field
properties. Each higher-order thalamic nucleus that receives driver afferents
from the cortex in turn relays the message to other (higher-order) cortical
areas. The pulvinar sends its axons to many different visual cortical areas
(Abramson and Chalupa 1985),
and each of these cortical areas must be seen as receiving, from the thalamus,
copies of messages from "lower" cortical areas that have already
been sent to brain stem motor or premotor centers. That is, these layer 5
cortical cells send one branch to brain stem centers for action and another
through the thalamus to higher cortical areas for perception.
THE SOMATOSENSORY PATHWAYS
Once the branching pattern of corticothalamic afferents is recognized as
providing thalamic inputs that are copies of motor instructions, it becomes of
interest to look at the branching patterns of other thalamic afferents. For
this, the relevant branching occurs in axons that terminate in prethalamic as
well as thalamic relays. For the somatosensory pathway, dorsal root axons
enter the spinal cord and branch, with an ascending branch as well as local,
spinal branches, and often a descending branch as well
(Fig. 1B)
(Brown et al. 1977;
Brown and Fyffe 1981; Cajal
1911; Lu and Willis 1999). The
common occurrence of such branching has to be seen in the light of evidence
(Lu and Willis 1999) that
false negative observations on branching are readily produced by anatomical
and physiological methods. In spite of this difficulty, it is evident that
both the dorsal column system and the anterolateral pathway are carrying
messages to the thalamus that have already had an opportunity to act at spinal
levels. Some messages, like those in the anterolateral pathway, act with a
synaptic relay involved, and others, in the dorsal columns, act through
branching of the incoming dorsal root axon.
For many years sensory losses, characteristic of Tabes dorsalis, were
taught to medical students to help them understand the function of the dorsal
columns. Romberg's sign, a loss of balance evident when such a patient stood
straight with legs together and then closed the eyes, was interpreted in
textbooks as a loss of the proprioceptive pathway in the dorsal columns
(Brodal 1969;
Nolte 1988). However, as
Brodal pointed out later
(1981), citing Vierck
(1978) and Wall and
Noordenboos (1977; see also
Brinkman and Porter 1977), the
lesion involves the dorsal roots and differs from a pure dorsal column lesion,
which spares the local, spinal branches of dorsal roots. That is, the dorsal
column lesion interrupts the branch that transmits copies of motor
instructions through the thalamus to the cortex for perceptual processing,
whereas in Tabes the branches for action and perception are both
interrupted.
Views on the pathways that transmit information about limb position to the
cortex have varied over the years and are relevant to understanding the
distinctions between pathways for action and perception. Whereas Sherrington
(1894) in describing the
muscle afferents saw these as providing information about limb position,
Mountcastle and Rose (1959) and Skoglund
(1973) saw the perception of
limb position as depending on joint receptors. They distinguished this from
the information from spindle afferents, which they regarded as not reaching
cortical levels and therefore playing no role in perception. This was a
conceptually important distinction, separating the pathway for perception from
the pathway for action. Burgess and Clark
(1969) and Burgess and Wei
(1982) subsequently
demonstrated that joint receptor responses were too limited to provide useful
information about limb position, and Matthews
(1977,
1982) showed that activity in
muscle afferents could be perceived. Further, Matthews pointed out that
artificial joint replacements did not lead to a loss of position sense: this
once more united perception and action in a single, branched pathway coming
from the muscle spindles; the false separation was reversed.
Before the medial lemniscus and the anterolateral pathways reach the
thalamus several axons are given off to intermediate stations, including the
brain stem reticular nuclei, inferior olive, hypothalamus, and superior
colliculus (summarized in Guillery and
Sherman 2002a; only the ones to the superior colliculus are shown
in Fig. 1B). Some of
these have been shown to be given off by branching axons, some may arise from
distinct cells in the dorsal column or lateral cervical nuclei
(Berkley 1975;
Berkley et al. 1980;
Bull and Berkley 1984;
Feldman and Kruger 1980), and
for some the evidence about branching is not clear. Textbooks often treat
these as intermediate stops on the way to the thalamus, presenting them as a
part of the pathway for perception. However, the connections to the inferior
olive and the hypothalamus are as readily regarded as acting on premotor
pathways,2 not leading
to the cortex but influencing cerebellar or autonomic (affective) components
of motor reactions. The superior colliculus can also be seen as a motor or
premotor center on evidence discussed in the next section.
These patterns of axonal branching show that messages passed from the thalamus to the somatosensory cortex carry more, and different, information than simply the "sensory" messages from peripheral receptors. No matter how one views the branching axons, in terms of which represents a "copy" of the other, the branch to the thalamus carries, in addition to the sensory information that has been the major or only focus for sensory physiologists, a considerable burden of information about instructions currently going to centers for action. For the ascending and the motor branches of the dorsal root axons we know that the incoming messages pass along both branches. It is possible that not every incoming impulse passes along both branches, and the postsynaptic action may well differ at the two terminal sites, depending on the nature of the receptors and on other local factors (e.g., Markham et al. 1998). However, one can expect there to be a relatively constant relationship between the messages delivered by the two branches. The message going through the thalamus to cortex will represent a concurrent motor instruction that will influence a motor act, directly or indirectly, positively or negatively, without need for any further outcome of the perceptual process, and quite possibly before the completion of the perceptual process. An issue that is largely unexplored concerns how the perceptual processes relate to these instructions for action. Are they best regarded as completely independent, as is often done, or can more be learned about perceptual processing by studying this relationship more closely?
THE VISUAL PATHWAYS
The isolation of the mechanisms for perception from those for action in
many contemporary studies of the visual system has received careful and
critical review by Churchland et al.
(1994). They look for models
of visual processing that relate more closely to the continuous interactions
between action and perception, and consider a number of psychophysical
phenomena that do not fit readily into a theory of "Pure Vision."
They report on anatomical connections that appear to argue against the pure
theory, and consider the computational advantages of what they call
"interactive vision," that is, visual perception that is not
waiting for a cortical analysis of the visual scene before
action.
Churchland et al. (1994),
having summarized much of the relevant connectional anatomy, comment:
"what is frustrating about this assembly of data, as with neuroanatomy
generally, is that we do not really know what it all
means."3 This is
a valid point about the material they summarize; many of the relevant
pathways, corticocortical, corticothalamic, and descending corticofugal, are
given no clearly assigned functions. Drivers need to be distinguished from
modulators, not only in the thalamus, where this is generally possible
(although still in need of much more detailed experimental verification), but
also in the corticocortical pathways, where this is essentially unexplored.
Comparably, descending pathways to the brain stem and cord are generally not
defined in terms of motor actions. It is important to know not only whether a
descending corticofugal pathway is a driver or a modulator, but it may prove
even more important to know the branching patterns of the axons, which, as
indicated above for the somatosensory pathways, are often undefined. Where a
branching axon sends a branch to a thalamic relay for transfer to the cortex,
knowledge about the actions of its other, motor or premotor branch may provide
additional clues about the message going to the cortex.
For retinogeniculate axons, branches for action and perception are readily
recognized. For rodents and rabbits, all retinogeniculate axons have branches
that go to the midbrain tectum or pretectum
(Chalupa and Thompson 1980;
Jhaveri et al. 1991;
Linden and Perry 1983;
Vaney et al. 1981). There is
no "pure," unbranched geniculocortical pathway exclusively for
perceptual processing in cortex. In cats the evidence for branching in the
large (Y) and the small (W) ganglion cells is clear
(Fukuda and Stone 1974;
Leventhal et al. 1985;
Wässle and Illing 1980).
Evidence for the intermediate (X cells) at one time indicated that these might
send a direct, unbranched pathway to the lateral geniculate nucleus. However,
observations of some X-cell axons with fine-caliber branches heading to the
midbrain (Sur et al. 1987)
and, later, of six out of six filled X-cell axons with fine branches going to
the pretectum (Tamamaki et al.
1994) suggest that there may be no pure unbranched
retinogeniculate pathway in cats. In monkeys the evidence about the largest
and the smallest retinal ganglion cells (magnocellular and koniocellular; see
Casagrande and Norton 1991)
again shows the majority, probably all, with branching axons going to lateral
geniculate nucleus and midbrain. The evidence for the parvocellular cells was
summarized earlier (Guillery and Sherman
2002a); although it is inconclusive. However, given the difficulty
of demonstrating fine branches (see Lu and
Willis 1999) and evidence for cats that the midbrain branches of
X-cells are very fine, it is reasonable to conclude that for all species most,
possibly all, retinogeniculate axons have midbrain branches.
The branch of the optic tract to the midbrain was earlier treated as an
alternative route to the cortex (Diamond
1973; Schneider 1966; Sprague
1972) and thus as possibly another pathway for perception. This is
because there are axons going from the superior colliculus to the pulvinar
(Mathers 1971;
Partlow et al. 1977), and the
pulvinar sends its axons to several higher visual cortical areas
(Abramson and Chalupa 1985).
Two issues relate to this view of the midbrain as a visual relay to the
cortex. One is that, whether or not there is a tecto-pulvino-cortical pathway,
there is no doubt that the superior colliculus and the pretectal nuclei are
motor centers concerned with head and eye movements. Even though the
retinotectal axons go to the superficial layers of the colliculus, not to the
deep layers more closely involved in motor control mechanisms themselves, the
retinotectal axons must still be seen to provide access to tectal computations
that produce head and eye movements. The second, more critical point concerns
the nature of the messages going from the midbrain to the pulvinar. Are these
drivers or modulators? In terms of their synaptic relationships and fine
structural appearance in the pulvinar, reports vary
(Mathers 1971;
Partlow et al. 1977;
Robson and Hall 1977). Perhaps
most tellingly, pulvinar cells lose their characteristic receptive field
properties after the visual cortex is silenced but not after tectal silencing
(Bender 1983;
Chalupa et al. 1972;
Chalupa 1991), indicating that
the tectum does not provide a significant driver input to pulvinar for
perceptual processing.
Taking the visual system as a specific example, several stages are
encountered from retina to higher cortical areas, where thalamic afferents can
send one branch to the thalamus for transmission to cortex and one to motor or
premotor centers of the brain stem. The visual message goes from the retina
through the geniculocortical pathway to area 17 for early stages of perceptual
processing, and along the retinotectal branches to the superficial layers of
the superior colliculus for premotor action. From area 17, in turn, layer 5
axons go the pulvinar and also send a branch to the superficial layers of the
superior colliculus (Guillery et al. 2002;
Harting et al. 1992). Evidence
that the axons coming from area 17 to the colliculus can affect a motor or
premotor action comes from Schiller and Tehovnik
(2001) and Tehovnik et al.
(2002), who showed that
microstimulation in area 17 of a monkey can affect the target choice of a
saccadic eye movement. Thresholds for the evocation of saccades were lowest
for the deep layers of the cortex, suggesting that the layer 5 corticofugal
axons, which send branches to the thalamus and superior colliculus (see
above), were being stimulated. The layer 6 axons are less likely to act on the
saccade because they do not go beyond the thalamus, and are modulators in the
thalamus.
The pulvinar itself sends axons to several different higher cortical areas,
many of which, in turn, have layer 5 projections back to the thalamus
(Abramson and Chalupa 1985).
They also send axons to the superior colliculus, some to the superficial
layers, but many to the deeper layers, nearer to the motor output (see
Harting et al. 1992). That is,
the outputs of these higher cortical areas, again, go to the cortex for
perceptual processing and to the brain stem for action, although at present it
is not known whether these two pathways represent branches of single axons or
are two independent outputs. Currently there is no evidence about the
branching patterns of these corticothalamic axons.
The problem that arises is to define exactly how visual perception and eye
movements relate to each other, and to the pathways considered above. The
rapid searching movements that occur when a new scene is examined
(Yarbus 1967) are clearly
relevant to perception, but most of the corticotectal axons from many
different cortical areas (Harting et al.
1992) cannot yet be related to the production of these, or other,
eye movements. Nor, at present, is it known how corticofugal messages to the
tectum for action relate to messages passed through the thalamus to the cortex
for perception. More information about the anatomy of the pathways is needed,
but in addition, at each stage of corticothalamocortical processing the
relationship of the motor instructions to the messages that contribute to the
perceptual process needs to be understood.
An example is provided by the recent demonstration
(Moore and Armstrong 2003)
that changes in the visual responses of neurons in the cortical area V4 of
monkeys can be produced by subthreshold stimulation of the frontal eye fields.
Here, subthreshold motor instructions for saccade production, possibly carried
in corticotectal axons to the deep layers of the colliculus
(Harting et al. 1992), produce
a change in a "sensory" response in the cerebral cortex. Moore and
Armstrong (2003) postulate
"a common network for the control of visual and oculomotor
selection." The possibility that this involves corticotectal (motor)
axons that have branches going through a thalamic relay to the visual
(sensory) cortex, merits exploration.
For the visual pathways, as for the somatosensory pathways, there is
limited evidence about the losses produced by damage to one or another of the
branches of axons afferent to the thalamus. Lesions of the superior colliculus
in cats or tree shrews produce deficits in directed movements in response to
visual stimuli (Diamond 1973;
Sprague 1972). In primates
Mishkin et al. (1983) briefly
reported for rhesus monkeys (but with no details and no citation) that
"complete bilateral destruction of the superior colliculus" had no
effect on the performance of a visual "landmark task." Earlier,
for monkeys Pasik et al.
(1966) had reported
essentially no changes after collicular lesions, whereas Anderson and Symes
(1969) reported mild changes
(see also Schiller, 1972).
Dumont et al. (1974) reported
briefly that bilateral lesions of the superior colliculus in monkeys produced
abnormalities of eye movements, but found no evidence for loss of brightness,
color, or pattern discrimination. Heywood and Ratcliff (1975) reported mild
oculomotor abnormalities in humans after lesions of the superior colliculus.
Pierrot-Deseilligny et al.
(1991) described a patient
with a lesion in the superior and inferior colliculi with abnormal saccades,
and diplopia, but no other visual losses. Comparably Girkin et al.
(1998) reported on a patient
with a lesion in the brachium of the superior colliculus who had diplopia and
pupillary defects, but no other visual sensory losses.
These are brief reports with little detail. It may prove important to explore the perceptual capacities more fully. Visual perceptions depend on extensive exploratory eye movements. On the basis of current evidence it appears that lesions of the midbrain branches of cortico- and retinogeniculate axons affect mechanisms of action, leaving those concerned with perception essentially intact.
Lesions in the visual cortex (area 17) in primates produce blindness
(Holmes and Lister 1916;
Polyak 1957;
Walsh and Hoyt 1957), showing
again that visual perception depends on the geniculate branches, not on the
midbrain branches. The phenomenon called "blindsight"
(Weiskrantz 1986), which
allows a patient to respond with some degree of discrimination to a stimulus
presented in the blind visual field, again demonstrates this separation of
action from perception. Details of pathways underlying the action component of
blindsight remain unexplored, although pathways through pulvinar or amygdaloid
nuclei have been proposed (e.g., Hamm et
al. 2003; Weiskrantz
2003). If the pulvinar were involved, it would probably not be a
driver pathway transmitting receptive field properties to the cortical areas,
given that these cortical areas are concerned with perceptual processing. It
would more likely involve tectothalamic modulators that alter the response
properties of pulvinar cells, with some visuotopic (localizing) organization.
However, since "blindsight" is demonstrable after a
hemidecortication (Perenin and Jeannerod, 1978) it seems more probable that
subcortical mechanisms are involved. They are capable of the topographical
sophistication needed to account for the responses recorded in blindsight.
Frogs can catch flies, a cat without visual cortex can turn accurately to a
visual stimulus, and even a spinal dog can accurately scratch a local stimulus
on the flank.
OTHER BRANCHED AFFERENTS TO THE THALAMUS
Although, as indicated above, evidence about branching axons is difficult
to obtain, there are observations, summarized by Guillery and Sherman
(2002a), that many afferents
serving as drivers to one or another thalamic nucleus have branches that
innervate lower brain stem centers. The evidence for the auditory pathways is
weakest, perhaps because the branching has been of no interest, or possibly
because lower levels of the auditory system are less closely linked to motor
actions. There is good evidence that cerebellothalamic and mamillothalamic
axons both have brain stem branches (Cajal 1911; and see Guillery and Sherman
2002). From the evidence available currently it is possible to entertain the
hypothesis that all driver axons to the thalamus, ascending and
cortical, have motor or premotor brain stem branches. The hypothesis is worth
testing not only because it suggests an interesting new generalization about
the organization of the thalamus, but also because, provided more reliable
methods can be developed for demonstrating branches, then, if the hypothesis
can be proved wrong, an important functional question will arise: how do the
branched pathways differ functionally from the unbranched pathways?
INTERACTIONS BETWEEN ACTION AND PERCEPTION
Although the idea that perceptual processing involves more than the passive
transmittal of messages from receptors to cerebral cortex is not new, it
merits a new focus that relates to the anatomy summarized above. Helmholtz
(Warren and Warren 1968)
wrote:
"The correspondence, therefore between the external world and the perceptions of sight rests, either in whole or in part, on the same foundation as all our knowledge of the actual world— on experience, and on constant verification of its accuracy by experiments which we perform with every movement of our body" (stress in the original).
and,
"[N]o perceptions obtained by the senses are merely sensations impressed on our nervous systems. A peculiar intellectual activity is required to pass from a nervous sensation to the conception of an external object which the sensation has aroused" (stress added).
Sperry (1952) has
stated:
"An analysis of our current thinking will show that it tends to suffer generally from a failure to view activities in their proper relation, or even in any relation, to motor behavior. The remedy lies in further insight into the relationship between the sensori-associative functions of the brain on the one hand and its motor activity on the other."
The brain stem branches of afferents to the thalamus provide an important anatomical clue for reevaluating perceptual processing in accord with the views of Helmholtz; they may provide the "remedy" sought by Sperry. These branches show that few if any messages transmitted to the cerebral cortex do not concurrently influence the motor apparatus, in some way or another, directly or indirectly, to increase or decrease a motor response. The relationship between Sperry's "sensori-associative" functions and motor activity can be sought in the motor links of thalamic afferents. The search need not be limited, as in Sperry's proposed "remedy," to links of higher cortical areas. The motor links are there for primary ascending afferents to the thalamus. For these, the motor message must accompany, and generally precede, perceptual processing in cortex. That is, the anatomy shows that, where this branching occurs, the sensory input will inevitably initiate both action and perception. The motor message is a necessary accompaniment of the perceptual process.
There is a serious question about the messages that are passed along any of
these branching thalamic afferents. Are they to be seen as a mechanism
producing motor effects, or as sensory messages? Because the axons branch, the
answer for the experimentalist must be "both" when the whole live
organism is considered. However, it will inevitably be seen as a sensory
mechanism where an animal is anesthetized, perhaps paralyzed as well. This is
an important limitation for many early studies of perceptual processing in
cortical cells. The role of a particular pattern of neural activity in
perceptual processing has been based on the fact that the neural activity
occurred in the cortex, and that there was a conceivable link between this and
known perceptual processes. There could be no direct evidence linking the
neural activity to particular perceptual processes, or more importantly for
the present discussion, to motor actions. It is of interest to compare studies
of cortex in cats or monkeys (e.g., Hubel
and Wiesel 1977) with those on the tectum of frogs
(Maturana et al. 1960), where
considerations about perception were never in the forefront. Rather, for the
frog (and for the investigators) the important issue, in relation to tectal
activity recorded, was the likely motor reaction to a visual stimulus: if it
is large, retreat; if it is small, eat it.
Studies of visual processing in the cerebral cortex of cats and monkeys,
which dominate much contemporary thinking about perceptual processing, start
at visual area V1 (area 17), progressing through simple, and complex cells,
and then continuing through several hierarchical stages of cortical
processing, with specializations for color, movement, and with putative
"where" and "what" pathways (e.g.,
Kandel et al. 2000). This type
of analysis of sensory circuitry has deep roots in studies of anesthetized
preparations and still relies to a significant extent on such studies. Recent
studies using fMRI or recordings from awake animals are beginning to change
the picture, but the interpretations of the cortical records (e.g.,
Luppino et al. 2001;
Nakamura et al. 2001;
Rizzolatti and Luppino 2001;
Sereno et al. 2002;
Tolias et al. 2001) are still
commonly expressed in terms of a relatively passive chain of messages
transferred from one cortical area to another, toward a motor cortical
"outlet," with no attention paid to thalamic inputs that any one
of the cortical areas receives, or to any of the outputs that each of the
cortical areas sends to lower motor centers.
To explore how sensory mechanisms relate to motor outputs, consider an organism that develops a new set of sensors. It can be a primitive organism first developing light- or sound-sensitive receptors, or a higher mammal, conceptually human, developing new sensors, such as mystacial vibrissae, an echo-locating system, or electro-receptors for use, perhaps, in aquatic recreations. When these receptors first appear they will be of no use, except insofar as they lead to motor responses. It is not likely that they could lead to perceptual functions until after some motor reactions had been produced. These motor reactions in themselves are likely to produce further, positive or negative, experiences, although these experiences will be of limited use unless they are stored in memory. This record of the sensory–motor experience can then provide the first trace of what can later form the basis of perceptual processes, after more experiences of similar stimuli and various motor responses. In terms of the acquisition of new sensory mechanisms, sensory machinery that connects to higher levels of processing, without first connecting to the motor pathways will bring to those higher levels a puzzling set of messages that can be given empirical sense only by reference first to lower-level motor, exploratory mechanisms.
A more direct approach to the acquisition of new sensors can be based on
the experience of providing a prosthesis to individuals who lack a particular
sense. In a probably unrepeatable study, Button and Putman
(1962) implanted into the
occipital cortex of a blind subject wires attached to a light-controlled
stimulator. They report that "with a few moments' practice, she learned
to point the photocell at a light in the room." Bach-y-Rita (2003) has
written about blind subjects provided with a TV camera that delivered
information about the visual scene to skin receptors, indicating that the
subjects' ability to appreciate the visual scene depended on their ability to
control the camera, including zooming, aperture, and focus. "After
sufficient training (stress added), our subjects reported experiencing
the image in space, instead of on the skin. They learn to make perceptual
judgments, using visual means of analysis." It is not clear from
accounts I have seen what perceptual abilities can be developed in the
complete absence of any motor control of the sensor. This information is not
of obvious interest for developing or using a prosthesis but it may prove of
considerable interest for understanding the development of new perceptual
capacities.
Helmholtz (Warren and Warren
1968) addressed the appearance of new sensory systems by
considering an infant, developing a perceptual apparatus. He wrote of the
infant exploring objects by handling them, putting them into its mouth,
regarding them from different angles, to make judgments about the causes of
the sensations: "It is only by voluntarily bringing our organs of sense
in various relations to the objects that we learn to be sure as to our
judgments of the causes of our sensations."
Here the importance of the motor exploration confirms the above discussion, but the "voluntary" nature of the exploration merits separate consideration. Helmholtz stresses the importance of the exploration of the sensory environment that allows us, through motor actions, to make judgments about our environment, that is, to establish perceptual structures. He wrote:
"If we ask whether there exists some common characteristic distinguishable by direct sensation through which each perception related to objects in space is characterized for us, then we actually find such a characteristic in the circumstance that bodily movement places us in different spatial positions relative to the perceived objects, and in doing so also changes the impressions which these objects make on us. The impulse to movement, however, which we give through the innervation of our motor nerves, is something which can be perceived directly. We feel we are doing something when we give such an impulse. But what it is we are doing we do not know directly."
For the last statement it is worth comparing the first with the second half. In the first half the movement might represent an involuntary act, perhaps even the action of a motor branch of a sensory axon, but then he makes clear that this is not his intention; he has the observer as initiating the movement, even though there is some mystery about the basis of that initiation; and he ascribes a perceptual experience to the motor act.
Two points arise clearly from what Helmholtz has written. One is that our perceptions depend on and are in part generated by our movements. The other is that the observer makes these movements (voluntarily) in order to explore the environment. The second point is quite explicit when he says:
"Finally, the tests we employ by voluntary movements of the body are of the greatest importance in strengthening our conviction of the correctness of the perceptions of our senses."
This is as extreme as he gets; it is easy to sense the history of a life devoted to testing the correctness of the perceptions of the senses, although that is not how most people operate most of the time. We do not feel a need to test the correctness of the perceptions of our senses. Our daily lives, which consist predominantly of motor reactions to changing sensory inputs, provide us with a store of corollary discharges, each associated with a particular sensory event and passed, as such, to the next, higher cortical level as yet another corollary discharge.
In general, impulses generated in sensory nerves can be said to vary the conditions under which the "structure" of the sensory environment is perceived. That is, these impulses produce the movements that vary the conditions. One can ask: who actually is in control? Are we initiators of the movements, as Helmholtz suggests, or does the environment initiate the movements, which then allow us to develop our perceptual categories? Which of our movements are a direct response to sensory stimuli bombarding us continuously; which are "voluntary," "exploratory" movements that we have initiated to explore the environment; and how much of the circuitry may actually be concerned with the suppression of movements that might otherwise be produced by the incoming messages?
The anatomy is clear about an early involvement of motor connections in perceptual mechanisms. Where these connections are branches of axons that also serve perception, the mechanisms are not "voluntary," they are parts of the machinery committed to particular motor outputs. This applies to the incoming (e.g., retinofugal or dorsal column) axons and also applies to corticothalamic axons from cortical layer 5 that pass copies of motor instructions to higher cortical areas.
Although the anatomy shows close links between pathways for perception and
action, this does not imply that perception cannot occur without action. There
may be sensory systems that pass straight to the cortex, without any lower
motor connections. Once, in the course of evolution, a sensory system is
established with close links to motor systems, then it could, perhaps, develop
direct connections into a previously established "perceptual"
center that has no prethalamic links into motor systems. This would fit
closely to a model of "Pure Sensation," parallel to the system of
"Pure Vision" (Churchland et
al. 1994). It would be a pathway where cortical analysis of
perceptual structures could be independent of movement. In principle this
seems feasible and could be studied experimentally. However, it has been shown
that with current techniques, negative evidence about axonal branching cannot
be interpreted as evidence for the absence of branching. The possibility that
there are pathways, perhaps the parvocellular part of the visual pathway in
primates (see above), or parts of the auditory pathway (for listening to
Bach), that go straight to the cortex with no subcortical branches, may prove
hard to demonstrate until methods of studying fine axonal branches are more
sensitive.
A telling dissociation of action and perception is seen in the
"locked-in" syndrome (Allain et
al. 1998; Plum and Posner
1966), since patients demonstrate a virtual absence of movement
but a good survival of perceptual functions. However, in these patients the
perceptual skills were established at a time when the motor actions produced
by the nonthalamic branches were still effective, and action and perception
could be related. After the brain stem (or other) injury the action of the
motor branches is no longer effective, but many of the sensory messages passed
to the thalamus are likely to be unchanged and can be interpreted in terms of
past experience. That is, in these patients, the ascending afferents carry
copies of messages to motor cells (e.g., ascending branches from spindle
afferents), but are carrying messages that cannot be obeyed. Nonetheless,
these copies will be transmitted to the cortex through the thalamus.
Similarly, afferents that send copies of messages to premotor (or
pre-premotor) centers are sending copies of messages that can still play a
significant role in central processing even if there can be no final motor
outcome. The corticothalamic axons will be intact and will be sending copies
of "intended" motor instruction from one cortical area to another;
these are messages that were previously used in perceptual processing in
higher cortical areas, and can still be used. Transthalamic messages from
cortex will represent intended movements in a way that the direct
corticocortical messages probably would not. The higher-order circuits can
then be seen to represent a complex of instructional messages that relate to
perceptual processing even when the final execution of the motor instructions
is no longer possible.
GENERAL CONCLUSIONS
The citation at the beginning of this review refers to a sense where the interaction of action and perception is striking. I have argued that the anatomy of sensory pathways provides strong evidence for close interactions of this nature in many other sensory systems, possibly all that traverse the thalamus. Not only is there evidence of interactions in many ascending pathways to the thalamus, but in addition there is the interaction that must occur whenever a corticocortical pathway linking one sensory cortical area to another relays in the thalamus and sends a descending branch to the brain stem or beyond.
The pathways considered here provide the cortex with an ongoing record of
motor instructions. That record provides the input for perceptual processing.
It can be regarded as providing the machinery of perceptual processing. Sperry
(1952) wrote: "In so far
as an organism perceives a given object, it is prepared to respond with
reference to it," which suggests the model of an incoming sensory train
discharging its perceptual load for the initiation of a motor response; yet he
continues: "That the preparation for response is (his italics)
the perception is suggested by further considerations." This view of
perception as the preparation for response can be seen in terms of the
anatomy, which shows perceptual processing as built up from the ongoing motor
instructions.
For Helmholtz (Warren and Warren
1968) our perceptions are a "symbol" for the source of
the stimulation. They are not an "image," standing in some
particular relation to an object; the symbol is arbitrary, comparable to
writing, which is a symbol of words but not an image of words. Helmholtz
wrote: "Thus even if our sensory perceptions in their quality are only
symbols, whose special nature depends entirely on our organization, they must
not be discarded as empty appearances; rather they are symbols for something,
either existing or happening—and what is most important—they can
represent the laws governing this event for us."
These symbols are created from the copies of motor and premotor (and pre-premotor) instructions from a great range of sources. Some come almost directly from the environment, for instance, pain fibers that innervate spinal reflex mechanisms and send ascending messages to the thalamus. Others come from higher cortical areas, representing thalamocortical circuits that are recording motor instructions that have already been sent out by other, lower cortical centers. Anatomy shows action and perception inexorably linked at all levels, from the peripheral input to the higher cortical areas.
Finally one should ask why all of these pathways go through the thalamus.
This opens another chapter, a subject for another review. Briefly, as an end
note, it is important to recognize that all of the copies of motor
instructions that pass through the thalamus are there exposed to rich
modulatory influences that come from the cortex, the thalamic reticular
nucleus, and the brain stem. This modulation (see
Guillery and Sherman 2002b;
Sherman and Guillery 1996,
2001) represents an important
function of the thalamic relay, allowing it to modulate transmission to the
cortex in accord with current attentional needs. The modulation can be global
or it can be highly localized and specific; it can allow for changing
interactions between one circuit (or part of one circuit) and another in a
complex pattern of interactions that are currently almost entirely unexplored.
This characteristic action of the thalamic relay will be able to modify all of
the messages passing through the thalamus for perceptual processing, but will
leave the motor branches for action unaffected.
DISCLOSURES
This work was supported by National Eye Institute Grant EY-12936.
ACKNOWLEDGMENTS
My thanks to Drs. S. M. Sherman, L. C. Populin, and H. J. Ralston III who provided helpful comments on an earlier draft.
FOOTNOTES
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
1 The "driving input" can be defined as the input that determines
the receptive field properties that are passed on to cortex by the thalamic
relay cells. (More details in Sherman and
Guillery 1998.) 
2 Sperry (1952), writing
about motor aspects of perceptual processing has said: "The core of the
perceptual process in the higher centers is more premotor or better
pre-premotor in nature, owing to the hierarchical plan of neural
organization." The important point here is that the sensory pathways
have actions that, although they may be far removed from a motor neuron, are
not on any of the classical sensory pathways, and they must be evaluated in
terms of their eventual motor actions.
3 It is worth pointing out that interpreting evidence from psychophysical
studies or from computer models in terms of what they mean for the neural
circuitry underlying particular perceptual processes is equally frustrating.
The ways in which these different approaches to perception can be interrelated
are but poorly defined as yet.
Address reprint requests to R. W. Guillery (E-mail: rguiller{at}wisc.edu).
REFERENCES
Abramson BP and Chalupa LM. The laminar distribution of cortical connections with the tecto- and cortico-recipient zones in the cat's lateral posterior nucleus. Neuroscience 15: 81–95, 1985.[Web of Science][Medline]
Allain P, Joseph PA, Isambert JL, Le Gall D, and Emile J. Cognitive functions in chronic locked-in syndrome: a report of two cases. Cortex 34: 629–634, 1998.[Web of Science][Medline]
Anderson KV, and Symmes D. The superior colliculus and higher visual functions in the monkey. Brain Res 13: 37–52, 1969.[Web of Science][Medline]
Bach-y-Rita P. Late post-acute neurologic rehabilitation: neuroscience, engineering and clinical programs. Arch Phys Med Rehab In press.
Bender DB. Visual activation of neurons in the primate pulvinar depends on cortex but not colliculus. Brain Res 279: 258–261, 1983.[Web of Science][Medline]
Berkley KJ. Different targets of different neurons in nucleus gracilis of the cat. J Comp Neurol 163: 285–303, 1975.[Web of Science][Medline]
Berkley KJ, Blomquist A, Pelt A, and Fink R. Differences in the collateralization of neural projections from dorsal column nuclei and lateral cervical nucleus to the thalamus and tectum in the cat: an anatomical study using two different double labeling techniques. Brain Res 202: 273–290, 1980.[Web of Science][Medline]
Born RT. Visual processing: parallel-er and parallel-er. Curr Biol 11: R566–R568, 2001.[Web of Science][Medline]
Bourassa J and Deschênes M. Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 66: 253–263, 1995.[Web of Science][Medline]
Bourassa J, Pinault D, and Deschênes M. Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fiber study using biocytin as an anterograde tracer. Eur J Neurosci 7: 19–30, 1995.[Web of Science][Medline]
Brinkman J and Porter J. Movement performance and afferent projections to the sensorimotor cortex in monkeys with dorsal column lesions. In: Active Touch, the Mechansim of Recognition of Objects by Manipulation: A Multidisciplinary Approach, edited by Gordon G. Oxford, UK: Pergamon Press, 1977, p. 119–137.
Brodal A. Neurological Anatomy in Relation to Clinical Medicine (2nd ed.). Oxford, UK: Oxford University Press, 1969, p. 108.
Brodal A. Neurological Anatomy in Relation to Clinical Medicine (3rd ed.). New York: Oxford University Press, 1981, p. 140.
Brown AG and
Fyffe RE. Direct observations on the contacts made between IA afferent
fibres and alpha motoneurons in the cat's lumbosacral spinal cord.
J Physiol 313:
121–140, 1981.
Brown AG, Rose
PK, and Snow PJ. The morphology of hair follicle afferent fibre
collaterals in the spinal cord of the cat. J Physiol
272: 779–797,
1977.
Bull MS and Berkley KJ. Differences in the neurones that project from the dorsal column nuclei to the diencephalon, pretectum and tectum in the cat. Somatosens Res 1: 281–300, 1984.[Web of Science][Medline]
Burgess PR and
Clark FJ. Characteristics of knee joint receptors in the cat. J
Physiol 203:
317–335, 1969.
Burgess PR and Wei JY. Signaling of kinesthetic information by peripheral sensory receptors. Annu Rev Neurosci 5: 171–187, 1982.[Web of Science][Medline]
Button J and Putman T. Visual responses to cortical stimulation in the blind. J Iowa State Med Soc 52: 17–21, 1962.
Cajal S and Ramón Y. Histologie du Système Nerveux De l'Homme et des Vertébrés, translated by Azoulay L. Paris: Maloine, 1911.
Casagrande VA and Norton TT. Lateral geniculate nucleus: a review of its physiology and function. In: Vision and Visual Dysfunction, edited by Leventhal AG. London, UK: MacMillian Press, 1991, p. 41–84.
Chalupa LM. Visual function of the pulvinar. In: The Neural Basis of Visual Function, edited by Leventhal AG. Boca Raton, FL: CRC Press, 1991, p. 140–159.
Chalupa LM, Anchel H, and Lindsley DB. Visual input to the pulvinar via lateral geniculate, superior colliculus and visual cortex in the cat. Exp Neurol 36: 449–462, 1972.[Web of Science][Medline]
Chalupa LM and Thompson I. Retinal ganglion cell projections to the superior colliculus of the hamster demonstrated by the horseradish peroxidase technique. Neurosci Lett 19: 13–19, 1980.[Web of Science][Medline]
Churchland PS, Ramachandran VS, and Sejnowski TJ. A critique of pure vision. In: Large-Scale Neuronal Theories of the Brain, edited by Koch C and Davis JL. Boston, MA: MIT Press, 1994, p. 23–65.
Diamond IT. The evolution of the tectal-pulvinar system in mammals: structural and behavioral studies of the visual system. Symp Zool Soc Lond 33: 205–233, 1973.
Diamond ME, Armstrong-James M, Budway MJ, and Ebner FF. Somatic sensory responses in the rostral sector of the posterior group (POm) and in the ventral posterior medial nucleus (VPM) of the rat thalamus: dependence on the barrel field cortex. J Comp Neurol 319: 66–84, 1992.[Web of Science][Medline]
Dumont M, Ptito M, Cardu B, and Lepore F. Collicular system as oculomotor coordination or visual perception centers. Trans Am Neurol Assoc 99: 23–27, 1974.[Medline]
Feig S and Harting JK. Corticocortical communication via the thalamus: ultrastructural studies of corticothalamic projections from area 17 to the lateral posterior nucleus of the cat and inferior pulvinar nucleus of the owl monkey. J Comp Neurol 395: 281–295, 1998.[Web of Science][Medline]
Feldman SG and Kruger L. An axonal transport study of the ascending projection of medial lemniscal neurons in the rat. J Comp Neurol 192: 427–454, 1980.[Web of Science][Medline]
Fukuda Y and
Stone J. Retinal distribution and central projections of Y-, X-, and
W-cells of the cat's retina. J Neurophysiol
37: 749–772,
1974.
Geisert EE, Langsetmo A, and Spear PD. Influence of the cortico-geniculate pathway on response properties of cat lateral geniculate neurons. Brain Res 208: 409–415, 1981.[Web of Science][Medline]
Gilbert CD and Kelly JP. The projections of cells in the different layers of the cat's visual cortex. J Comp Neurol 163: 81–105, 1975.[Web of Science][Medline]
Girkin CA,
Perry JD, and Miller NR. A relative afferent pupillary defect without any
visual sensory deficit. Arch Ophthalmol
116: 1544–1545,
1998.
Grant G, Boivie J, and Silfvenius H. Course and termination of fibres from the nucleus Z of the medulla oblongata. An experimental light microscopical study in the cat. Brain Res 55: 55–70, 1973.[Web of Science][Medline]
Guillery RW. Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. J Anat 187: 583–592, 1995.[Web of Science][Medline]
Guillery RW, Feig SL, and Van Lieshout DP. Connections of higher order visual relays in the thalamus: a study of corticothalamic pathways in cats. J Comp Neurol 438: 66–85, 2001.[Web of Science][Medline]
Guillery RW and
Sherman SM. The thalamus as a monitor of motor outputs. Phil
Trans R Soc Lond B 357:
1809–1821, 2002a.
Guillery RW and Sherman SM. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33: 163–175, 2002b.[Web of Science][Medline]
Hamm AO, Weike
A, Schupp HT, Treig T, Dressel A, and Kessler C. Affective blindsight:
intact fear conditioning to a visual cue in a cortically blind patient.
Brain 126:
267–275, 2003.
Harting JK, Updyke BV, and Van Lieshout DP. Corticotectal projections in the cat: anterograde transport studies of twenty-five cortical areas. J Comp Neurol 324: 379–414, 1992.[Web of Science][Medline]
Heywood S and Ratcliff G. Long term oculomotor consequences of unilateral colliculectomy in man. In: Basic Mechanisms of Ocular Motility and Their Clinical Implication, edited by Lennerstrand D, Bach Y Rita P. Oxford: Pergamon, p. 561–564.
Holmes G and
Lister WT. Disturbances of vision from cerebral lesions with special
reference to the cortical representation of the retina.
Brain 39:
34–73, 1916.
Horsley V. The function of the so-called motor area of the brain. Br Med J 2: 125–132, 1909.
Hubel DH and Wiesel TN. Functional architecture of macaque monkey visual cortex. Proc R Soc Lond B Biol Sci 198: 1–59, 1977.[Medline]
Jhaveri S, Edwards MA, and Schneider GE. Initial stages of retinofugal axon development in the hamster: evidence for two distinct modes of growth. Exp Brain Res 87: 371–382, 1991.[Web of Science][Medline]
Johansson H and
Silfvenius H. Input from ipsilateral proprio- and exteroceptive hind limb
afferents to nucleus Z of the cat medulla oblongata. J
Physiol 265:
371–393, 1977.
Kalil RE and
Chase R. Corticofugal influence on activity of lateral geniculate neurons
in the cat. J Neurophysiol 33:
459–474, 1970.
Kandel ER, Schwartz JH, and Jessel TM. Principles of Neural Science (4th ed.). New York: McGraw-Hill, 2000.
Leventhal AG, Rodieck RW, and Dreher B. Central projections of cat retinal ganglion cells. J Comp Neurol 237: 216–226, 1985.[Web of Science][Medline]
Linden R and Perry VH. Massive retinotectal projection in rats. Brain Res 272: 145–149, 1983.[Web of Science][Medline]
Lu GW and Willis WD. Branching and/or collateral projections of spinal dorsal horn neurons. Brain Res Rev 29: 50–82, 1999.[Medline]
Luppino G, Calzavara R, Rozzi S, and Matelli M. Projections from the superior temporal sulcus to the agranular frontal cortex in the macaque. Eur J Neurosci 14: 1035–1040, 2001.[Web of Science][Medline]
Markram H, Wang
Y, and Tsodyks M. Differential signaling via the same axon of neocortical
pyramidal neurons. Proc Natl Acad Sci USA
95: 5323–5328,
1998.
Mathers LH. Tectal projections to the posterior thalamus of the squirrel monkey. Brain Res 35: 295–298, 1971.[Web of Science][Medline]
Matthews PB. Where does Sherrington's "muscular sense" originate? Muscles, joints, corollary discharges? Annu Rev Neurosci 5: 189–218, 1982.[Web of Science][Medline]
Matthews PBC. Muscle afferents and kinesthesia.
Br Med Bull 33:
137–142, 1977.
Maturana HR,
Lettvin JY, and Pitts WH. Anatomy and physiology of vision in the frog
(Rana Pipiens). J Gen Physiol
43: 129–175,
1960.
Mishkin M, Ungerleider LG, and Macko KA. Object vision and spatial vision: two cortical pathways. Trends Neurosci 6: 414–417, 1983.[Web of Science]
Moore T and Armstrong KM. Selective gating of visual signals by microstimulation of frontal cortex. Nature 421: 370–373, 2003.[Medline]
Nakamura H,
Kuroda T, Wakita M, Kusunoki M, Kato A, Mikami A, Sakata H, and Itoh K.
From three-dimensional space vision to prehensile hand movements: the lateral
intraparietal area links the area V3A and the anterior intraparietal area in
macaques. J Neurosci 21:
8174–8187, 2001.
Nolte J. The Human Brain. St. Louis, MO: CV Mosby, 1988.
Ojima H.
Terminal morphology and distribution of corticothalamic fibers originating
from layers 5 and 6 of cat primary auditory cortex. Cereb
Cortex 4:
646–663, 1994.
Partlow GD, Colonnier M, and Szabo J. Thalamic projections of the superior colliculus in the rhesus monkey, Macaca mulatta. A light and electron microscopic study. J Comp Neurol 72: 285–318, 1977.[Medline]
Pasik T, Pasik
P and Bender MB. The superior colliculus and eye movements. An
experimental study in the monkey. Arch Neurol
15: 420–436,
1966. Perenin MT and Jeannerod M. Visual functions within
the hemi-anopic field following early cerebral hemidecortication in man: I
Spatial localization. Neuropsychologia 16: 1–13.
Pierrot-Deseilligny C, Rosa A, Masmoudi K, Rivaud S, and Gaymard B.
Saccade deficits after a unilateral lesion affecting the superior colliculus.
J Neurol Neurosurg Psychiatry
54: 1106–1109,
1991.
Plum F and Posner JB. The Diagnosis of Stupor and Coma. Philadelphia, PA: FA Davies, 1966.
Polyak S. The Vertebrate Visual System. Chicago, IL: University of Chicago Press, 1957.
Rizzolatti G and Luppino G. The cortical motor system. Neuron 31: 889–901, 2001.[Web of Science][Medline]
Robson JA and Hall WC. The organization of the pulvinar in the grey squirrel (Sciurus carolinensis). II. Synaptic organization and comparisons with the dorsal lateral geniculate nucleus. J Comp Neurol 173: 389–416, 1977.[Web of Science][Medline]
Rockland KS. Convergence and branching patterns of round type 2 cortico-pulvinar axons. J Comp Neurol 390: 515–536, 1998.[Web of Science][Medline]
Rose JE and Mouncastle VB. Touch and kinesthesis. In: Handbook of Physiology. Neurophysiology. Washington, DC: Am. Physiol. Soc., 1959, sect. 1, vol. 1, p. 387–429.
Rouiller EM and Welker E. A comparative analysis of the morphology of corticothalamic projections in mammals. Brain Res Bull 53: 727–741, 2000.[Web of Science][Medline]
Schiller PH. Some functional characteristics of the superior colliculus of the rhesus monkey. Bibl Ophthalmol 82: 122–129, 1972.[Medline]
Schiller PH and Tehovnik EJ. Look and see: how the brain moves your eyes about. Prog Brain Res 134: 127–142, 2001.[Web of Science][Medline]
Schmielau F and Singer W. The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Res 120: 354–361, 1977.[Web of Science][Medline]
Schneider GE. Two visual systems.
Science 163:
895–902, 1969.
Sereno M, Trinath T, Augath M, and Logothetis NK. Three-dimensional shape representation in monkey cortex. Neuron 33: 635–652, 2002.[Web of Science][Medline]
Sherman SM and
Guillery RW. Functional organization of thalamocortical relays.
J Neurophysiol 76:
1367–1395, 1996.
Sherman SM and
Guillery RW. On the actions that one nerve cell can have on another:
distinguishing "drivers" from "modulators."
Proc Natl Acad Sci USA 95:
7121–7126, 1998.
Sherman SM and Guillery RW. Exploring the Thalamus. San Diego, CA: Academic Press, 2001.
Sherrington CS. On the anatomical constitution of nerves of skeletal muscles; with remarks on recurrent fibres in the ventral spinal root. J Physiol 17: 211–258, 1894.
Skoglund S. Joint receptors and kinesthesis. In: Handbook of Sensory Physiology, edited by Iggo A. Berlin: Springer-Verlag, 1973, vol. II, p. 111–136.
Sommer MA and
Wurtz RH. A pathway in primate brain for internal monitoring of movements.
Science 296:
1480–1482, 2002.
Sperry RW. Neurology and the mind–brain problem. Am Scientist 40: 291–312, 1952.
Sprague JM.
The superior colliculus and pretectum in visual behavior [review].
Invest Ophthalmol Visual Sci
11: 473–482,
1972.
Sur M, Esguerra
M, Garraghty PE, Kritzer MF, and Sherman SM. Morphology of physiologically
identified retinogeniculate X- and Y-axons in the cat. J
Neurophysiol 58:
1–32, 1987.
Tamamaki N, Uhlrich DJ, and Sherman SM. Morphology of physiologically identified X and Y axons in the cat's thalamus and midbrain as revealed by intra-axonal injection of biocytin. J Comp Neurol 354: 583–607, 1994.[Web of Science]
Tehovnik EJ, Slocum WM, and Schiller PH. Differential effects of laminar stimulation of V1 cortex on target selection by macaque monkeys. Eur J Neurosci 16: 751–760, 2002.[Web of Science][Medline]
Tolias AS,
Smirnakis SM, Augath MA, Trinath T, and Logothetis NK. Motion processing
in the macaque: revisited with functional magnetic resonance imaging.
J Neurosci 21:
8594–8601, 2001.
Van Essen DC,
Anderson CH, and Felleman DJ. Information processing in the primate visual
system: an integrated systems perspective. Science
255: 419–423,
1992.
Vaney DI, Peichl L, Wässle H, and Illing RB. Almost all ganglion cells in the rabbit retina project to the superior colliculus. Brain Res 212: 447–453, 1981.[Web of Science][Medline]
Vidnyánszky Z, Borostyánkoi Z, Gõrcs TJ, and Hámori J. Light and electron microscopic analysis of synaptic input from cortical area 17 to the lateral posterior nucleus in cats. Exp Brain Res 109: 63–70, 1996.[Web of Science][Medline]
Vierck CJ Jr. Comparison of forelimb and hindlimb motor deficits following dorsal column section in monkeys. Brain Res 146: 279–294, 1978.[Web of Science][Medline]
Wall PD and
Noordenbos W. Sensory functions which remain in man after complete
transection of dorsal columns. Brain
100: 641–653,
1977.
Walsh FB and Hoyt WF. Clinical Neuroophthalmology. Baltimore, MD: Williams & Wilkins; 1957, p. 77–84.
Warren RM and Warren RP. Helmholtz on Perception: Its Physiology and Development. New York: Wiley, 1968.
Wässle H and Illing RB. The retinal projection to the superior colliculus in the cat: a quantitative study with HRP. J Comp Neurol 190: 333–356, 1980.[Web of Science][Medline]
Weiskrantz L. Blindsight: A Case Study and Implications. Oxford, UK: Clarendon Press, 1986.
Weiskrantz L. Mind—the gap, after 65 years: visual
conditioning in cortical blindness. Brain
126: 265–266,
2003.
Yarbus AL. Eye Movements and Vision. New York: Plenum, 1967.
This article has been cited by other articles:
|
|
 |
|
  P. Bartho, A. Slezia, V. Varga, H. Bokor, D. Pinault, G. Buzsaki, and L. Acsady Cortical Control of Zona Incerta J. Neurosci., February 14, 2007; 27(7): 1670 - 1681. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. A. Berman, L. M. Heiser, R. C. Saunders, and C. L. Colby Dynamic Circuitry for Updating Spatial Representations. I. Behavioral Evidence for Interhemispheric Transfer in the Split-Brain Macaque J Neurophysiol, November 1, 2005; 94(5): 3228 - 3248. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. G. Sirota, H. A. Swadlow, and I. N. Beloozerova Three Channels of Corticothalamic Communication during Locomotion J. Neurosci., June 22, 2005; 25(25): 5915 - 5925. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| Visit Other APS Journals Online |
