Download Neural correlates of consciousness: A definition of the dorsal and

Medical Hypotheses (2005) 65, 922–931
http://intl.elsevierhealth.com/journals/mehy
Neural correlates of consciousness:
A definition of the dorsal and ventral streams
and their relation to phenomenology
Costa Vakalopoulos
*
171 McKean Street North Fitzroy, 3068 Melbourne, Australia
Received 19 April 2005; accepted 16 May 2005
Summary The paper presents a hypothesis for a neural correlate of consciousness. A proposal is made that both the
dorsal and ventral streams must be concurrently active to generate conscious awareness and that V1 (striate cortex)
provides a serial link between them. An argument is presented against a true extrastriate communication between the
dorsal and ventral streams. Secondly, a detailed theory is developed for the structure of the visual hierarchy. Premotor
theory states that each organism–object interaction can be described by the two quantitative measures of torque and
change in joint position served by the basal ganglia and cerebellum, respectively. This leads to a component theory of
motor efference copy providing a fundamental tool for categorizing dorsal and ventral stream networks. The rationale
for this is that the dorsal stream specifies spatial coordinates of the external world, which can be coded by the
reafference of changes in joint position. The ventral stream is concerned with object recognition and is coded for by
forces exerted on the world during a developmental exploratory phase of the organism. The proposed pathways for a
component motor efference copy from both the cerebellum and basal ganglia converge on the thalamus and modulate
thalamocortical projections via the thalamic reticular nucleus. The origin of the corticopontine projections, which are
a massive pathway for cortical information to reach the cerebellum, coincides with the area typically considered as
part of the dorsal stream, whereas the entire cortex projects to the striatum. This adds empirical support for a new
conceptualization of the visual streams. The model also presents a solution to the binding problem of a neural
correlate of consciousness, that is, how a distributed neural network synchronizes its activity during a cognitive event.
It represents a reinterpretation of the current status of the visual hierarchy.
c 2005 Elsevier Ltd. All rights reserved.
Introduction
A theory of premotor relations discusses the emergence of cognitive processes and conscious awareness from the motor history of a developing
* Tel.: +61408810220.
E-mail address: [email protected].
organism [1]. It is mediated by a mechanism of motor
efference copy, which directly modulates the neural
properties of neocortical regions receiving perceptual input from the respective sensory organs. It ascribes meaning to this input determining the quality
of the experience. A notable feature of neocortical
networks is a division of processing between dorsal
and ventral streams and is best described in the pri-
0306-9877/$ - see front matter c 2005 Elsevier Ltd. All rights reserved.
doi:10.1016/j.mehy.2005.05.016
Neural correlates of consciousness
mate visual hierarchy. The dorsal stream is often described as the ‘where’ pathway serving spatial information that allows us to navigate the environment or
pick up an object. The ventral stream, on the other
hand, serves object recognition, the so-called
‘what’ pathway. This concept of brain architecture
is supported by local lesion studies. Remarkable progress has been made over the last several decades
delineating visual areas according to physiological
properties and anatomical connections. The research effort has culminated in detailed maps of
the interrelation of the various subregions within a
dorsal/ventral stream framework.The benchmark
paper is by Felleman and Van Essen [2]. However,
there are a number of contentious debates surrounding the accuracy of these maps and their exact significance for cognitive function.
The first part of this paper will deal with a
hypothesis of a neural correlate of consciousness.
The modern concept is of a widely distributed network, but the relative and critical importance of
the striate cortex and frontal lobes is in great dispute.The problem has become so intractable that
Milner and Goodale even propose a third pathway
based on lessons learned from the neglect literature. The first hypothesis of the present paper
states that concurrent activation of both dorsal
and ventral streams are required for conscious
awareness. From a theoretical point of view,this
is a prediction of premotor theory since both
streams present the totality of categorization of
motor efference copy of the exploring organism.
From the empirical stance evidence supporting this
contention is gained from direct electrical stimulation of the temporal cortex (ventral stream) and
supplemented by lesion studies of the parietal cortex (dorsal stream).
The second part of the paper deals with the fine
structure of the visual hierarchy by proposing heuristic definitions of the dorsal and ventral streams.
The status of the lateral connections between regions and the flow of information between the
two pathways present prescient anomalies to the
currently favoured model. Premotor theory states
that each organism–object interaction can be described by the two quantitative measures of torque
and change in joint position. This leads to a component theory of motor efference copy providing a
fundamental tool for categorizing dorsal and ventral stream networks. The second main hypothesis
then, states that a rigorous definition of the visual
hierarchy is based on the distribution of cortical
projections to the cerebellum and basal ganglia,
the former uniquely determining dorsal stream
properties and the latter a characteristic of both
streams.The aforementioned structures code for
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the parameters of change in joint position and torque conditions of an interactive history, respectively [1]. The model renders the concept of
lateral connections obsolete.
The third major hypothesis proposes a mechanism of binding of distributed neural networks.
The thalamic reticular nucleus TRN envelops the
entire thalamus and can mediate the binding by a
motor reentrant pathway through its known modulation of thalamocortical networks. It directly addresses the important philosophical issue of
embodiment of phenomenal experience in spite
of a non-focal neural correlate of consciousness.
Neuroanatomical correlates of
consciousness
Ungerleider and Mishkin [3] showed that object
recognition and spatial tasks were served by cortical pathways and that these projected differentially to the inferior temporal (IT) and posterior
parietal cortex, respectively. A practical argument
will be made that the awareness of a phenomenal
episode requires the simultaneous activation of
the dorsal and ventral streams described here as
parallel premotor levels. The reciprocal nature of
cortical networks is consistent with the paradigm
view of a non-focal localization of awareness. However,the striate cortex appears to play a unique
role in visual awareness and premotor theory proposes that it serves as a serial link between the
streams. Certainly, attention appears to modify
activity within both extrastriate and striate cortex
as shown by binocular rivalry experiments [4,5].
The significance of these studies is that they suggest that early visual cortex is not simply a passive
receptacle. The hypothesis is that true reciprocal
pathways between the dorsal and ventral streams
exist only in the region of the striate cortex. This
opinion is obviously contrary to current beliefs
and will require justification. It is in considering
the pathways for top-down generation of imagery
that the serial nature of the structure of the striate
cortex becomes apparent.
There is substantial evidence for an overlap of
networks that serve both bottom-up and top-down
processes, i.e., internal images use homologous
neural networks to those directly representing the
same external event. It is proposed that the
production of a top-down image requires the serial
activation of the dorsal stream via ventral backprojections to the striate cortex. At progressively
higher levels individual neurons exhibit greater subspecificity. The underlying structure of the visual
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Vakalopoulos
posterior parietal cortex
(dorsal stream)
striate cortex V1
inferior prefrontal
cortex
inferior temporal cortex
(ventral stream)
Thalamus
(eg MDmc)
lateral hypothalamus
Figure 1
Top-down imagery.
hierarchy is an anterior convergence of posterior
intraareal elements [6,7]. In the ventral stream,this
would facilitate the endogenous stimulation of a focal group of neurons augmenting a response within
the inferotemporal cortex and recruiting by backflow primary cortical modules. While probing the
exposed cortex of patients during neurosurgical
procedures for epilepsy in the 1940s, Wilder Penfield showed that direct stimulation of the temporal
lobes evoked explicit memories. Premotor theory
predicts that an image is evoked by linking of the
ventral to the dorsal streams at the level of the striate cortex (Fig. 1). That the dorsal stream is a critical element of conscious perception is suggested
by the syndrome of unilateral neglect, which is
associated with lesions of the inferior parietal lobule and is clinically demonstrated by a lack of
awareness of contralateral space. Critically, the
deficit can manifest itself in imagination,such as
when patients are asked to recall a familiar scene
[8]. The evidence from Penfield’s studies and patients with neglect thus, suggest top down pathways from temporal cortex (ventral stream)
recruits posterior or inferior parietal (dorsal
stream) networks in the evocation of imagery.
Lesions in striate cortex that result in blindness
also impede the resolution of cognitive imagery,
suggesting that V1 is the critical binder of parallel
streams of premotor level functions. Whether conscious vision is possible without V1 is still hotly
debated. Premotor theory does not imply that visual
awareness is localized to V1, but only that it is a critical link within a distributed neural correlate. Consistent with this view neuroimaging studies
demonstrated activation of human primary visual
cortex [9] and the lateral geniculate nucleus [10]
during visual recall.In fact, in a visual imagery task
of famous faces, cortical activation involved a distributed network including the intraparietal sulcus
and temporal cortex in addition to the striate cortex
[11]. The theory still allows that under pathological
conditions dorsal and ventral stream binding may
generate a conscious percept independent of V1
activation. For example, LSD, a 5HT2 receptor agonist, induces visual hallucinations with prominent
parietal and temporal lobe activation and relative
striate cortex inactivation [12]. A similar argument
can be made for dreaming where PET studies have
shown significant activation of the inferior parietal
lobe and inferior temporal cortices, in addition to
limbic and paralimbic areas, but relative inactivation of V1 (see review in Hobson et al. [13]).
Component theory of motor efference
copy
Torque and change in joint position are the two
parameters that specify all motor activity including
Neural correlates of consciousness
velocity and acceleration. Motor reentry can be
analyzed as a component theory of motor efference copy serving distinct cognitive parameters in
the organization of neocortical networks. It is not
intuitively obvious parameters of a motor action
can specify the properties of posterior cortical regions one tends to associate with object or face
recognition, for example. It is precisely this conceptual undertaking premotor theory claims. A detailed exposition of the theory of premotor
relations is to be found elsewhere [1].
Conditions of torque in a neural network may
conceivably be specified by the basal ganglia via
TRN modulation of thalamocortical projections.
Whether the role of the basal ganglia can be
entirely defined in this manner remains to be
demonstrated. However, several extrapyramidal
features of patients with Parkinson’s disease support this claim. Signs of bradykinesia are generally
considered a deficiency of dopamine regulation
within the basal ganglia. A shuffling gait is a characteristic of these patients. A step involves a
power burst by an appropriate muscle group.
Any movement has accelerating and decelerating
phases,which are directly proportional to force
exerted. Godaux et al. [14] revealed a diminution
in the rate of rise of muscle activity during rapid
arm reaching movements to a visual target, but
normal sequential activation of muscles, co-contraction of antagonist muscles, movement trajectory and accuracy. There is evidence that the
latter parameters, which may be normal in Parkinson’s disease, are served by the cerebellum
[15,16]. However, it may not be possible to entirely dissociate kinematic effects from kinetic
deficits. Overall,the evidence suggests a failure
in force generation associated with basal ganglia
pathology.
Given its role in force generation, the basal ganglia can thus, specify the torque component of motor efference copy as an organizing principle of
neocortical categorization. Majsak et al. [17]
showed an impairment in the acceleration phase
of reaching for a stationary ball. In a study by Berardelli et al. [18] patients were able to modulate
EMG activity during wrist flexion in the same way
as normals, but could not use these bursts to make
rapid movements. The authors state that: ‘‘The patients appear to underestimate what muscle activity is required for a particular movement. There is
a breakdown of the link between perceptual appreciation of what is needed and the delivery of appropriate instructions to the motor cortex ’’. These
findings are predicted by a cognitive theory of the
basal ganglia. Premotor theory states that the
judgment of the force required is an inherent prop-
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erty of the phenomenology of perception of the
object. In a study by Mollion et al. [19] PD patients
off medication were differentially impaired in a
non-spatial compared to a spatial version of a
working memory task based on reaction times.
The authors concluded that the deficit could not
be attributed to a simple motor impairment and
implicating a cognitive role for the basal ganglia.
What premotor theory attempts is a conceptual
bridge between force generation and cognitive
function so that dysfunction of the former underpins impairment of the latter in some fundamental
sense, that is it is not just an incidental association
[1].
Proprioceptive feedback is the second critical
element of premotor category function. Joint position will be served by the cerebellum.The organization of cerebellar global networks parallels
that of the basal ganglia [20]. The afferent limb
is a massive corticopontine and mossy fibre system. The efferent reentrant limb is a projection
of the deep cerebellar nuclei to the motor thalamus.This loop covaries with peripheral cerebellar
input. However, the corticopontine network has
a restricted origin, with a distinct spatial character, in contrast to the widespread input to the
striatum [21]. Its distribution of origin appears
to parallel the areas commonly attributed to the
dorsal stream, especially parietal cortex. The cerebellar loop fulfils the criteria of a spatiotemporal
relation to the organism and which can only be
specified by changes in joint position during an
interactive history. Conversely, the categorization
of a percept in the inferotemporal cortex is not
spatial, but feature-dependent. Recognition is
generally, orientation insensitive, eschewing a
proprioceptive role in the organization of ventral
stream circuits that serve it and which project
predominantly to subcortical hedonic centres
rather than dorsal prefrontal and motor areas to
which the dorsal stream projects. Receptive field
properties of the ventral stream are tolerant of
various spatial loci and orientations for an object.
This cannot be the case for accurate visuomotor
control that is the presumed function of the dorsal stream.
A clearly stated hypothesis is that corticopontine projections as part of the cerebellar loop define a priori the dorsal stream of any modality.
This appears quite satisfying intellectually because
dorsal stream function is generally associated with
spatial localization and the cerebellum can directly
specify the neocortical neural properties that encode such knowledge. That is,the target of a visually guided movement must already have an
inherent algorithm as part of the phenomenological
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Vakalopoulos
awareness of the object for the correct movement
to be executed.
Ventral/dorsal stream boundaries
Several visual areas assigned to the dorsal stream
by most current descriptions of the visual hierarchy appear to have connections with the ventral
stream as illustrated by the middle temporal
(MT) and superior temporal polysensory (STP)
[22,23]. The projections to the ventral stream
from these classic dorsal stream areas (especially
MT) may come from a distinct ‘ventral’ subpopulation involved in the recognition of moving objects, STP possessing neurons whose activity is
specific for movements such as walking [24]. This
serves the ventral stream function of recognition
that a subject is walking,for example. It may be
misleading to consider this a true exchange between the parallel streams given the current disagreement on what areas constitute the dorsal
stream [25]. Premotor theory gives a functional
definition of the dorsal and ventral streams based
on properties of subpopulations of neurons, but
which do not necessarily correspond to an areal
distribution. An area such as MT, which is classically regarded as part of the dorsal stream will,
according to a component theory of motor efference copy, possess two subpopulations of neurons,
only one of which has properties that define the
dorsal stream. These properties are the presumed
product of the cerebellar loop. The other group
has receptive field properties specified by the basal ganglia and is a constituent of both ventral and
dorsal streams. It is only the latter neuronal type
that is proposed to have reciprocal connections
between areas that are typically regarded as
being segregated in parallel streams. In other
words, it may be more accurate to consider that
the parallel nature of the respective streams is
maintained within a particular domain or visual
area. Fig. 2 and the discussion in the next section
will make this point clearer. Current staining
techniques may not reveal the heterogeneity in
the neuronal properties of a particular visual area
with only a subpopulation being the potential
source of the corticopontine efferents.
Studying the figures of Schmanmann and Pandya
[21] one is struck by how the shaded area (origin of
the corticopontine projections) delineates a sharp
boundary in the superior temporal sulcus (STS) separating parietal cortex from the non-shaded inferotemporal cortex (ITC). The apparent homogeneity
of the shading belies the possible functional differences of subpopulations of neurons within these
Figure 2 Dorsal and ventral streams. A schematic
figure of the distribution of neuronal subpopulations
(crosses and ovals) in the ventral and dorsal streams of
the monkey visual cortex. The dashed line represents the
limits of the superior temporal sulcus. The oval figures
are a proposed category product of the cerebellar loop.
They code for spatial coordinates and are modulated by
gaze direction. Their distribution corresponds to the
shaded corticopontine projection areas of Fig. 4 in
Schmahmann and Pandya [21]. The crosses comprise
the proposed neuron population categorized by the basal
ganglia and represents the torque conditions of their
receptive field properties. These neurons are found in
PPC, STP and IT. It is only this subgroup that projects to
both dorsal and ventral streams. The dorsal and ventral
streams according to this model are defined by the
physiological properties of neurons and not any strict
anatomical demarcation. The receptive field properties
of both subpopulations ultimately combine in a motor
transformation that represents the parameters of pyramidal motoneurons. In the proposed convergence of
dorsal stream receptive fields the torque condition may
be specified by any of the red marked population [An
analogous pattern of distribution can be extrapolated for
the prefrontal cortex dorsal and ventral to the principal
sulcus].
shaded areas, as already stated. None the less,
the general correspondence of the shaded area to
the dorsal stream pathways is so striking, it gives
unequivocal support for a component premotor
definition of the visual hierarchy.
The arrangement of projections from the basilar
pontine nuclei to the cerebellum implies that a focal cerebral cortical area is distributed to numerous discrete sites in the cerebellum and
conversely, that many cerebral areas communicate
with a single folium [21]. The basilar pons distributes its mossy fibre terminals predominantly to
the lateral cerebellar hemispheres [26]. The interaction of mossy fibre input to the cerebellum with
the ‘patchy’ mosaic pattern of climbing fibre input
evoked by peripheral somatosensory input sub-
Neural correlates of consciousness
serves the putative cognitive function of dorsal
stream-type networks. The inferior olive is the origin of climbing fibres to the cerebellum and each
purkinje cell has input from both systems (mossy
and climbing fibres). Thus, the peripheral sensory
input to the olive is in a unique position to modulate the activity of the cerebropontine projection
system. This will not be a simple facilitation of
mossy fibre activity, but an imposed specification
of cortical network properties by association of
perceptual information with a history of component motor efference copy. The contextual interactions between these two systems were
originally proposed in an instruction-selection theory of cerebellar learning [27], but the cognitive
role of the cerebellum has only more recently been
the focus of speculation. One might expect the
neocerebellum (much expanded in primates) to
play a dominant cognitive role in spatial
awareness!
A detailed structure of the visual
hierarchy
For a particular premotor act and its corresponding
premotor levels, the cortical pathways through
various visual areas are bound by a specific motor
history and its motor efference copy through a
common node of reentry, the thalamus. The theory
proposes that the ‘perpendicular’ thalamocortical
circuits are categorizing and the parallel cortical
domains, the substrate categorized. Pallidal projections to thalamocortical circuits are the proposed pathways for the categorization of the
visual hierarchy. The complex cells of the striate
cortex are already exhibiting some of the receptive
field properties of neurons at more anterior levels
of the visual hierarchy. Binocular V2 neurons respond to illusory contours. MT (V5) detects motion.
V4 is the colour area. Lesions in these two areas
cause deficits in perceiving motion and colour,
respectively. Within each domain of a sensory hierarchy neurons display category specific properties
which are a unique,although not an exclusive, innovation for that domain. What is the neuroanatomical basis for the introduction of category specific
function? The associative visual cortices project
to the striatum with a variable degree of segregation. The topography of specific regions of the thalamic nuclei, such as the pulvinar has largely
segregated corticothalamic projections [28]. Thus,
the parallel anatomical arrangement allows the
process of motor reentry (motor efference copy)
to functionally differentiate the corticostriatal,
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thalamocortical loops that project to and from
the various visual areas V2,V3,V4, MT, etc. This is
proposed to be the origin of the characteristic
properties of individual areas within the visual hierarchy as one progresses from posterior to anterior
cortex. The properties of neurons in the visual hierarchy become progressively more complex, even
abstract, yet are the outcome of a reductive process of a thalamocortical axis of reentry.
In addition, contrasting sequences of motor
activity, for example, may categorize the neural
assemblies that are conscious of an object,or of facial features in both specific spatiotemporal coordinates (posterior parietal cortex) and non-spatial
recognition circuits (inferotemporal cortex) via
corticopontine and corticostriatal loops, respectively. A component motor theory of reentry provides torque as a sole condition for ventral
stream networks as is the case for the posterior
inferotemporal cortex. In other words, the role of
the ventral stream in object and facial recognition
is developmentally linked to the basal ganglia only.
The cerebellar loop, on the other hand, provides a
spatiotemporal history. In summary, the mechanism of motor reentrant function may characterize
both the properties of individually defined areas as
one ascends the visual hierarchy and the division of
visual processing into dorsal and ventral streams.
Neuroanatomical evidence supports the role of
the thalamocortical projection in the categorization cortical neuronal properties. Ascending intercortical connections is associated with the
convergence of receptive field properties. Neurons
in more anterior locations of the visual cortex have
larger even bilateral fields suggesting a cumulative
response. Convergence of neuronal types is postulated and has been demonstrated anatomically by
the lateral connections of supragranular and, to a
lesser extent, infragranular clusters of interdigitating columns or modules of a visual area [29]. Pulvinocortical connections with extrastriate visual
areas project predominantly to layer 3 with axon
collaterals to other depths which are often not in
register with the typical columnar organization
[30]. Clustered terminal arbors distributed within
a visual area may form a mechanism for the conjoint effects of motor efference copy on disparate
intraareal elements. This demonstrates how motor
reentry can bind the properties of distinct intraareal neuron clusters. The final section will deal
with how non-contiguous visual areas can form a
distributed neural network, functionally coupled
into a single cognitive domain or event. This has
been coined the binding problem, i.e., how a distributed networks that serves conscious awareness
can be bound into a functional unit. But first, a
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demonstration of how premotor theory can resolve
several key problems in the current scheme of the
visual hierarchy is discussed. The currently accepted map of visual areas will be described as
the old model to distinguish it from a new paradigm
presented here.
Anomalies of the visual hierarchy
In a detailed analysis of the relationship between
visual areas based on the origins and terminations
of laminar cortical projections, Felleman and Van
Essen [2] placed areas at the same level if the projection was columnar and ascending if predominantly to layer 4. Furthermore, a commonly held
belief is that the dorsal and ventral streams communicate in prestriate cortex. This certainly fits
the dominant view of a compartmentalization of
parvocellular and magnocellular pathways as the
predominant inputs to ventral and dorsalstreams,
respectively. However, functionally there is evidence for mixing of these signals [31]. The latter
findings are consistent with the alternative interpretation offered here that a typically parvocellular feature such as colour contrast must be
processed in both a spatial (posterior parietal)
and an object (inferotemporal) sense.
The treatment of visual areas in this manner
may help resolve the potential anomalies of the visual hierarchy. This is exemplified by the reciprocal
relationship of cortical areas such as the dorsal
medial superior temporal (MSTd) and 7a and the
ambiguity inherent in the projections from MT to
V4 [2,32] MSTd projects to area 7a as a columnar
pattern (C). The projection from posterior parietal
7a to MSTd is a multilayered pattern (M) typical of a
backprojection, (Fig. 3). Under the old model a
columnar pattern is a lateral projection (same level
in the hierarchy) and the expectation would be a
columnar pattern for the reciprocal projection.
But, this is multilayered (projections to supragranular and infragranular layers), which is typical of
backprojections, directly contradicting the lateral
connection model. The basic premise of the new
model is that columnar patterns are part of the
anterior projection crossing various domains in a
hierarchical model, without the need to invoke lateral connectivity.
Visual areas need not be assigned exclusively to a
dorsal and ventral pathway, but may have elements
inclusive of both. Similar to the above interpretation, the V4 to MT columnar projection is destined
for a dorsal category stream and thus an apparent
change in stream from a ventral to dorsal premotor
level. However,MT has two patterns of reciprocal
projections with V4. One is columnar as the same
level hypothesis predicts (old model), but the other
is multilayered, typical of a backprojection, an
untenable finding for the old model. The most parsimonious explanation is to regard these connections as part of two parallel networks within the
ventral and dorsal streams, respectively (Fig. 4).
This requires a change in point of view that neither
MT nor V4 are entirely defined by a single stream.
Thus, there is no requirement for a communication
between the parallel streams. According to the old
model, the ascending pathway is defined by a prominent layer 4 input. The new model maintains this,
but considers uniform columnar interdigitation a
variation on the same theme, without invoking the
problematic view of lateral connections.
By admission of the authors themselves [2], most
suggested lateral connections are problematic at
Parietal
Temporal
Anterior
C
V4
MT
M
M
7a
MSTd
C
Striate Cortex
Posterior
Figure 3
Lateral connection between MSTd and 7a.
Figure 4
Lateral connections between V4 and MT.
Neural correlates of consciousness
some level of description, but the acceptance of
their existence as can be discerned from the scientific literature contradicts this irresolute ambiguity. In the case of V4 and MT, laterality is
suggestive of a complete and reciprocal transfer
of information between both the dorsal and ventral
streams. An alternative paradigm proposes that
only neuronal populations that are the category
products of the basal ganglia and hence, the torque
component of motor efference copy, will be represented in either stream. A particular area, such as
MT or MST will have a population of neurons with
properties specified only by the basal ganglia and
these will be distributed in parallel. Conversely,
neuronal populations that are the category products of the cerebellar loop and hence, the change
in joint position component of motor efference
copy, are exclusive of the dorsal stream by definition and do not project to the ventral stream
(Fig. 2). The inference that can be drawn from this
model is that although, there is an obvious exchange of information between extrastriate areas
such as V4 and MT,this does not necessarily assume
a communication between streams. An individual
domain may contribute to the neural processing
of both ventral and dorsal streams in a parallel
fashion. The existence of only a subpopulation
within the parieto-occipital cortex that is responsive to changes in the direction of gaze is compatible with this view. In extrastriate area V3A, for
example, the responsiveness to visual stimulation
of only about half of the studied units was modulated by the angle of the experimental animal’s
gaze [33]. These neurons are presumably involved
in the coding of spatial coordinates. Furthermore,
gaze dependent neurons appear to be segregated
from non-gaze dependent cells in the same cortical
area. Similar proportions of gaze and non-gaze
dependent neurons are found in area V6 [34],
where they are more uniformly distributed, and
area 7a [35]. The hypothesis is that the differential
modulation of receptive field properties may be
attributed to their respective projections to either
the striatum or basilar pons representing the pathways for the categorization by the two respective
components of motor efference copy, torque or
force and joint position.
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many parts of the brain may be physiologically
coupled in a neurobiological correlate of consciousness. Essentially, the hypothesis is based on
a principle of self-organizing behaviour of thalamocortical assemblies. Premotor theory takes a further step in proposing that the organization of
cortical networks is a type of embodiment that
does not require the statistically improbable state
of strictly synchronized activity to provide a sense
of unity.
Each neocortical category domain of a sensory
(visual) hierarchy projects reciprocally to a subsequent category domain or visual area. The primary
architecture is epigenetically determined. Contiguity of cortical areas ultimately bears on shared
physiological roles, but prolific reciprocal connections are shared by areas that are quite distant
from each other, such as the prefrontal region dorsal to the principal sulcus and the posterior parietal
cortex. Areas that are reciprocally bound may be
considered as nodal points in a proposed triad of
motor reentry. The model of triangulation purports
the hierarchical binding of specific networks within
the visual cortex by non-overlapping motor relations. The third nodal point is subcortical within
the structure of the thalamus (Fig. 5). Cortical
nodes have widely distributed reciprocal networks
creating a 3-dimensional lattice. There is apposition of the largely segregated cortical prefrontal
and posterior parietal domains in the medial pulvinar and their extension across the mediodorsal thalamic border [37]. The corticothalamic projection
zones of some areas with reciprocal inputs such as
MT and V4 do not overlap at all [7]. Critically, the
corticothalamic projections have a topographic order, with scant evidence of intrinsic interthalamic
Parietal
Prefrontal
TRN
Model of triangulation
Recent theoretical interest in the synchronization
of neuronal firing patterns has been advocated as
a solution to the binding problem of consciousness
[36]. That is, how neural networks distributed over
Motor
Feedback
Pulvinar
Figure 5
Binding model of triangulation.
930
connections. This poses the main problem as I see
it for a binding mechanism of different neuronal
populations, which is solved by a model of reentry
that proposes the mediation of pallidal afferents
within and across thalamic borders. Small biocytin
injections in GPe resulted in profuse anterograde
labeling of fibres within the entire rostrocaudal
extent of the TRN [38]. The labeled fibres were
long and gave off numerous short collaterals that
terminated in clusters of large varicosities. Thus,
this projection is ideally placed for the ‘synchronous’ modulation of segregated thalamocortical
groups.
Conclusion
The application of premotor theory to brain structure and function could prove a useful tool for
establishing a rigorous definition of the visual hierarchy. The theory provides a fundamental mechanism of binding and how a distributed network
can still have a sense of embodiment of the phenomenal experience without invoking a regressive
homonculus. The dorsal and ventral streams can
be modeled on the reentrant input from cerebellar
and pallidal projections to thalamocortical circuits, respectively. If correct, it will lead to a radical change in thinking about the functional
underpinnings of the neocortex and the significance of the basal ganglia and cerebellum in the
cognitive domain. It will require a reappraisal of
the currently published maps of the visual hierarchy. It will also lead to a better understanding of
the cognitive and psychiatric dysfunction associated with disorders of these structures, such as
Huntington’s and Parkinson’s disease.
Further empirical support for the theory can be
gained by animal studies using reversible inactivations of these structures and observing consequences of cognitive function. Non-invasive
studies on humans using new TMS technology could
achieve similar results. Further descriptions of the
intrinsic properties of visual cortical neurons by
intracellular recording techniques along the lines
of the motor parameters torque and proprioception
suggests a novel experimental paradigm.
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