Consciousness and the Brain
The Thalamocortical Dialogue in Health and Disease
RODOLFO LLINÁS AND URS RIBARY
Department of Physiology and Neuroscience, New York University School of Medicine,
New York, New York 10016, USA
ABSTRACT: The goal of this paper is to explore the basic assumption that large-
scale, temporal coincidence of specific and nonspecific thalamic activity gener-
ates the functional states that characterize human cognition.
KEYWORDS: Thalamocortical; Gamma-band activity; Cognition; Functional
I will confine my presentation to experimental data concerning human conscious-
ness, à la Cajal. To me this is clearly the most parsimonious manner in which to
approach the issue.
In the type of wonderful meeting such as we have had, most of us [and most cer-
tainly the speaker] remain awake throughout the presentation, although we under-
stand why, given the complexity of the subject and the nature of jet lag, some of us
might fall asleep. If a person falls asleep, especially in a non-REM condition, we
may regard that person, during that time, as having ceased to exist as an entity capa-
ble of consciousness. The lyric of a well-known old tango tune entitled “Silencio en
la Noche” describes the condition in succinct poetic fashion: “el músculo duerme, la
ambición descansa [the muscle sleeps, ambition rests].” Indeed, a person does not
exist as a cognitive being during dreamless sleep. So, what does this mean? We will
rightly infer that consciousness is but one functional state of the brain. The converse
is also true: the brain has other equally costly metabolically active states in which
cognition is not generated.
The next question to ask, agreeing that a prerequisite for cognition is either wake-
fulness or dreaming, would be to describe the absolute minimal neuronal machinery
required for the support of such functional condition. We can easily agree that in ad-
dition to the brain stem and the associated basal ganglia/amygdalar nucleus, we need
the brain cortical mantle and the thalamus. Indeed if we lack the thalamus, all that
beautiful cortex is useless, and, in the absence of cortex, the thalamus on its own is
quite impotent. I have personally seen patients in Dr. Plum’s neurology clinic at Cor-
nell Medical School with an intact cortex, but with medial thalamic lesions, in a state
close to total coma—in agreement with previous papers on this subject. On the basis
Address for correspondence: Rodolfo Llinás, M.D., Ph.D., New York University School of
Medicine, Department of Physiology and Neuroscience, 550 First Avenue, New York, NY 10016.
167 LLINÁS AND RIBARY: CONSCIOUSNESS AND THE BRAIN
of such cases, as well as on magnetoencephalographic data in humans, I proposed a
decade ago that consciousness arises from a continuous “dialogue” between the thal-
amus and the cortex.
THE BASIC NEURONAL CIRCUIT IN HUMAN CONSCIOUSNESS
Given that sensory inputs generate but a fractured representation of universals,
the issue of perceptual unity concerns the mechanisms that allow these different sen-
sory components to be gathered into one global image. In recent years, this has been
described as “binding,” to be implemented by temporal conjunction.1–4
Because the number of possible categories of perceptions is so extensive, their
implementation via purely hierarchical connectivity is very unlikely, where a single
“grandmother” neuron or a small group of such neurons would represent specific el-
ements of a category. A second problem with the hierarchical proposal is sampling
size, that is, a very large number of specific elements in a very large number of cat-
egories would make the retrieval problem immense. Thus, even considering that neu-
ronal elements transduce and transmit signals at millisecond rate from the onset of
sensory primitives, exhausting all sequential combinations would be awkwardly
time-intensive. But at a more familiar level, it takes roughly the same amount of time
to recognize that a face is familiar than that it is not. As in any sequential strategy, it
takes much longer to conclude nonfamiliarity—as it would require comparing it with
“all known faces”—than familiarity, as in the latter the search will proceed for only
as long as necessary to match. From a different perspective the grandmother-neuron
hypothesis fails to explain how their unique “perceptual insights” (the specific ele-
ments in a given category) are communicated to the rest of the nervous system; that
is, how do grandmother cells tell the rest of their neurons what they know, given their
unique position at the top of a hierarchy?
Alternatively, since categorizations are generated by spatial mapping of the pri-
mary sensory cortex and its associated cortical structures, a more dynamic interac-
tion, based on temporal coherence, may generate dissipative functional structures5
capable of as rapid a change as the perception they generate. Thus, a simultaneity
mapping may be envisioned that takes advantage of the parallel and synchronous or-
ganization of the brain networks in order to generate perception.
The hypotheses to be discussed below are derived from two areas of research, the
first from the investigation of single neuronal elements studied in vitro and in vivo
and the second from measurements made via noninvasive magnetoencephalography
in humans. The principal issue to be discussed is the assumption that the intrinsic
electrical properties of neurons, and the dynamic events resulting from their connec-
tivity, result in global resonant states which we know as cognition.
INTROSPECTION AND REALITY EMULATION
Several lines of research suggest that the brain is essentially a closed system5 ca-
pable of self-generated activity based on the intrinsic electrical properties of its com-
ponent neurons and their connectivity. In such a view the CNS is a “reality”-
emulating system6 and the parameters of such “reality” are delineated by the
168 ANNALS NEW YORK ACADEMY OF SCIENCES
senses.7 The hypothesis that the brain is a closed system follows from the observa-
tion that the thalamic input from the cortex is larger than that from the peripheral
sensory system,8 suggesting that thalamocortical iterative recurrent activity is the
basis for consciousness.7 In addition, neurons with intrinsic oscillatory capabilities
that reside in this complex synaptic network allow the brain to self-generate dynamic
oscillatory states which shape the functional events elicited by sensory stimuli. In
this context, functional states such as wakefulness or REM sleep and other sleep
stages are prominent examples of the breadth of variation that self-generated brain
activity may yield.
The above hypothesis assumes that, for the most part, the connectivity of the hu-
man brain is present at birth, and is “fine-tuned” later on during normal maturation.
This view of a neurological a priori was suggested in early neurological re-
search,10,11 with the identification by Broca of a cortical speech center and the dis-
covery of point-to-point somatotopic maps in the motor and sensory cortices12 and
in the thalamus.13,14
A second organizing principle may be equally important—one that is based on
the temporal rather then the spatial relationships among neurons. This temporal
mapping may be viewed as a type of functional geometry.15 This mechanism has
been difficult to study until recently, since it requires the simultaneous measurement
of activity from large numbers of neurons and is not an aspect usually considered in
TEMPORAL MAPPING AND COGNITIVE CONJUNCTION
Synchronous neuronal activation during sensory input has recently been studied
in the mammalian visual cortical cells when light bars of optimal orientation and dis-
placement rate are presented.16–18 Furthermore, the components of a visual stimulus
corresponding to a singular cognitive object (e.g., a line in a visual field) yield co-
herent gamma-band oscillations in regions of the cortex that may be as far as 7 mm
apart,17–19 or may even be in the contralateral cortex. In fact, gamma-band oscilla-
tory activity between related cortical columns has a high correlation coefficient un-
der such circumstances. In addition, coherent 40-Hz oscillations throughout the
cortical mantle of awake human subjects have been revealed by magnetoencephalog-
raphy.20 These oscillations may be reset by sensory stimuli; and phase comparison
revealed the presence of a 12- to 13-msec phase shift between the rostral and caudal
poles of the brain.20 These gamma oscillations display a high degree of spatial orga-
nization and thus may be a candidate mechanism for the production of temporal con-
junction of rhythmic activity over a large ensemble of neurons.
From a neuronal point of view the mechanism by which gamma oscillation may
be generated has been studied at the level of single neurons and of neuronal circuits.
For example, it has been shown that the membrane potential of sparsely spiny inhib-
itory neurons in cortical layer IV supports gamma-frequency membrane voltage os-
cillation (FIG. 1), the mechanism for the oscillation being a sequential activation of
a persistent low-threshold sodium current21 followed by a subsequent potassium
conductance.22 The inhibitory input of these sparsely spinous interneurons onto py-
ramidal cells projecting to the thalamus can entrain 40-Hz oscillation in the reticular
nucleus and so entrain, by rebound activation, the specific and nonspecific thalamus.
169 LLINÁS AND RIBARY: CONSCIOUSNESS AND THE BRAIN
Indeed, since the GABAergic reticular thalamic neurons project to most of the relay
nuclei of the thalamus,23 layer-IV cells would indirectly make a contribution to the
40-Hz resonant oscillation in the thalamocortical network. It has recently been dem-
onstrated that under in vivo conditions relay-thalamic and reticular-nucleus neurons
and pyramidal cells themselves are capable of close to 40-Hz oscillation on their
own, laying out in this manner the possibility for network resonance intrinsically at
gamma-band frequency.24 The ionic mechanisms underlying this oscillation are sim-
ilar to those of the spiny layer-IV neurons.25
When the interconnectivity of these nuclei is combined with the intrinsic proper-
ties of the individual neurons, a network for resonant neuronal oscillation emerges
in which specific cortico-thalamo-cortical circuits would tend to resonate at gamma
frequency. According to this hypothesis, neurons at the different levels, and most
particularly those in the reticular nucleus, would be responsible for the synchroniza-
FIGURE 1. 40-Hz oscillation in wakefulness and a lack of 40-Hz reset in delta sleep
and REM sleep. Recording using a 37-channel MEG. In (A–D) spontaneous oscillatory re-
sponses following auditory stimulus. In A, the subject is awake and the stimulus is followed
by a reset of 40-Hz activity. In B and C, the stimulus produced no resetting of the rhythm.
However, spontaneous 40-Hz oscillations occur in REM sleep independent of the stimulus.
(D) The noise of the system in femtotesla (fT). (Modified from Llinás and Ribary28).
170 ANNALS NEW YORK ACADEMY OF SCIENCES
tion of gamma oscillation in distant thalamic and cortical sites. We will see later that
these oscillations may be organized globally over the CNS, especially as it has been
shown that neighboring reticular-nucleus cells may be linked by dendro-dendritic
and intranuclear axon collaterals.26
THALAMOCORTICAL RESONANCE AND CONSCIOUSNESS
On the basis of research about the minimal temporal interval in sensory discrim-
ination we may establish that consciousness is a noncontinuous event determined by
synchronous activity in the thalamocortical system.27 Since this activity is present
during REM sleep28 but is not seen during non-REM sleep, we may postulate further
that the resonance is modulated by the brainstem and would be given content by sen-
sory input in the awake state and by intrinsic activity during dreaming. These studies
have addressed issues concerning: (a) the presence of gamma-band activity during
sleep and (b) the possible differences between gamma resetting in different sleep/
Spontaneous magnetic activity was recorded continuously during wakefulness,
delta sleep, and REM sleep using a 37-channel sensor array (FIG. 1). Since Fourier
analysis of the spontaneous, broadly filtered rhythmicity (1–200 Hz) demonstrated
a large peak of activity at 40 Hz over much of the cortex, we decided that it was per-
missible to filter the data at gamma-band frequency (30–50 Hz). Large coherent sig-
nals with a very high signal-to-noise ratio were typically recorded from all 37
sensors, as shown in FIG. 1A for a single 0.6-sec epoch of global spontaneous oscil-
lations in an awake individual.
The second set of experiments examined the responsiveness of the oscillation to
an auditory stimulus during wakefulness, delta sleep, and REM sleep. The stimulus
comprised frequency-modulated 500-msec tone bins, triggered 100 msec after the
onset of the 600-msec recording epoch; recordings were made at random intervals
over about 10 minutes. In agreement with previous findings,28,30,31 auditory stimuli
produced well-defined 40-Hz oscillation during wakefulness (FIG. 1A), but no reset-
ting was observed during delta (FIG. 1B) or REM sleep (FIG. 1C) in this or the six
other subjects we examined.
The traces in FIGURE 1 are a superposition of the 37 traces recorded during a sin-
gle 600-msec epoch. Their alignment indicates the high level of coherence of the 40-
Hz activity at all the recording points following the auditory stimulus. A high level
of coherence is also typical of spontaneous 40-Hz bursts.
These findings indicated that while the awake state and the REM sleep state are
electrically similar with respect to the presence of 40-Hz oscillations, a central dif-
ference remains in the inability of sensory input to reset the 40-Hz activity during
REM sleep. By contrast, during delta sleep the amplitude of these oscillations differs
from that of wakefulness and REM sleep, but as in REM sleep there is no 40-Hz sen-
sory response. Another significant finding is that gamma oscillations are not reset by
sensory input during REM sleep, although clear evoked-potential responses indicate
that the thalamo-neocortical system is accessible to sensory input.7,33 We consider
this to be the central difference between dreaming and wakefulness. These data sug-
gest that we do not perceive the external world during REM sleep because the intrin-
sic activity of the nervous system does not place sensory input in the context of the
171 LLINÁS AND RIBARY: CONSCIOUSNESS AND THE BRAIN
functional state being generated by the brain.7 That is, the dreaming condition is a
state of hyperattentiveness to intrinsic activity in which sensory input cannot access
the machinery that generates conscious experience.
An attractive possibility in considering the morphophysiological substrate is that
the “nonspecific” thalamic system, particularly the intralaminar complex, plays an
important part in such coincidence generation. Indeed the neurons of this complex
project in a spatially continuous manner to the most superficial layers of all cortical
areas, including the primary sensory cortices. This possibility is particularly attrac-
tive, given that single neurons burst at 30–40 Hz especially during REM sleep,24
which is a finding consistent with the macroscopic magnetic recordings observed in
this study, and with the fact that damage to the intralaminar system results in lethargy
BINDING OF SPECIFIC AND NONSPECIFIC GAMMA BAND ACTIVITY
A schematic of a neuronal circuit that may subserve temporal binding is present-
ed in the left side of FIGURE 2. Gamma oscillations in neurons in specific thalamic
nuclei19 establish cortical resonance through direct activation of pyramidal cells and
feed-forward inhibition through activation of 40-Hz inhibitory interneurons in layer
IV.22 These oscillations re-enter the thalamus via layer-VI pyramidal–cell axon col-
laterals,36 producing thalamic feedback inhibition via the reticular nucleus.23 A sec-
ond system is illustrated on the right side of FIGURE 2. Here the intralaminar
nonspecific thalamic nuclei projection to cortical layers I and V and to the reticular
nucleus is illustrated.28 Layer-V pyramidal cells return oscillations to the reticular
nucleus and intralaminar nuclei. The cells in this complex have been shown to oscil-
late at gamma-band frequency and to be capable of recursive activation.24
It is also apparent from the literature that neither of these two circuits alone can
generate cognition. Indeed, as stated above, damage of the nonspecific thalamus pro-
duces deep disturbances of consciousness, while damage of specific systems produc-
es loss of the particular modality. Although at this early stage it must be quite simple
in its formulation, the above suggests a hypothesis regarding the overall organization
of brain function. The hypothesis rests on two tenets: First, the “specific” thalamo-
cortical system is viewed as encoding specific sensory and motor activity by the res-
onant thalamocortical system specialized to receive such inputs (e.g., the LGN and
visual cortex); the specific system is understood to comprise those nuclei, whether
sensorimotor or associative, that project mainly, if not exclusively, to layer IV in the
cortex. And the second tenet is that, following optimal activation, any such thalamo-
cortical loop would tend to oscillate at gamma-band frequency, and activity in the
“specific” thalamocortical system could be easily “recognized” over the cortex by
this oscillatory characteristic.
In this scheme, areas of cortical sites “peaking” at gamma-band frequency would
represent the different components of the cognitive world that have reached optimal
activity at that time. The problem now is the conjunction of such a fractured descrip-
tion into a single cognitive event. We propose that this could come about by the con-
current summation of specific and nonspecific 40-Hz activity along the radial
dendritic axis of given cortical elements, that is, by coincidence detection. This view
172 ANNALS NEW YORK ACADEMY OF SCIENCES
differs from the binding hypothesis proposed by Crick and Koch in which cortical
binding is attributed to the activation of cortical V4, pulvinar or claustrum.3
THE THALAMOCORTICAL DYSRHYTHMIC SYNDROME
Very recently, a significant corollary to the thalamocortical dialogue hypothesis for
consciousness has been encountered concerning several neurological and psychiatric
FIGURE 2. Thalamocortical circuits proposed to subserve temporal binding. Diagram
of two thalamocortical systems. Left: Specific sensory or motor nuclei project to layer IV of
the cortex, producing cortical oscillation by direct activation and feed-forward inhibition via
40-Hz inhibitory interneurons. Collaterals of these projections produce thalamic feedback
inhibition via the reticular nucleus. The return pathway (circular arrow on the right) re-en-
ters this oscillation to specific- and reticularis-thalamic nuclei via layer-VI pyramidal cells.
Right: Second loop shows nonspecific intralaminary nuclei projecting to the most superfi-
cial layer of the cortex and giving collaterals to the reticular nucleus. Layer-V pyramidal
cells return oscillation to the reticular- and the nonspecific-thalamic nuclei, establishing a
second resonant loop. The conjunction of the specific and nonspecific loops is proposed to
generate temporal binding. (Modified from Llinás and Ribary.28)
173 LLINÁS AND RIBARY: CONSCIOUSNESS AND THE BRAIN
conditions.37 Indeed spontaneous magnetoencephalography (MEG) activity from pa-
tients suffering from neurogenic pain, tinnitus, Parkinson’s disease or depression
showed increased low-frequency theta rhythmicity, in conjunction with a widespread
and marked increase of coherence among high- and low-frequency oscillations.
These data indicate the presence of a thalamocortical dysrhythmia which we pro-
pose is responsible for all the above-mentioned conditions. The coherent theta activ-
ity, which results from a resonant interaction between thalamus and cortex, is due to
the generation of low-threshold calcium spike bursts by thalamic cells. The presence
of these bursts is directly related to thalamic cell hyperpolarization brought about by
either excess inhibition or disfacilitation.37 The emergence of positive clinical symp-
toms is viewed as resulting from ectopic gamma-band activation, which we refer to
as the “edge effect.” This effect is observable as increased coherence between low-
and high-frequency oscillations, probably resulting from inhibitory asymmetry be-
tween high- and low-frequency thalamocortical modules at the cortical level.
The basic assumption concerning the genesis of this syndrome is that thalamo-
cortical dysrhythmia is a CNS intrinsic property brought about by changes in intrin-
sic voltage-gated ionic conductances at the level of thalamic relay cells, namely the
deinactivation of T channels by cell membrane hyperpolarization.4 Low-threshold
spike bursts are thus produced and lock the related thalamocortical circuits in low-
frequency resonance. Low-frequency loops interact at the cortical level with high-
frequency ones, giving rise to the edge effect and the generation of a positive symp-
tom. In tinnitus, peripheral neurogenic pain, Parkinson’s disease, and some neuro-
psychiatric disorders with striatal origin, the dysrhythmic mechanism is triggered
“bottom up,” which means from the thalamus toward the cortex. In other situations
like epilepsy, neuropsychiatric conditions of cortical origin, and central cortical neu-
rogenic pain, we may have a “top down” mechanism, triggered by a reduction of the
cortico-thalamic input. Both “bottom up” and “top down” situations result in excess
inhibition or disfacilitation, generating thalamic cell membrane hyperpolarization
and low-frequency oscillation. And so, the same mechanism responsible for the or-
ganization of consciousness, when altered in its organization and timing, can be the
genesis of neuropsychiatric conditions.
Cognition, a property of thalamocortical cycling, appears to function on the basis
of temporal coherence. Such coherence would be embodied by the simultaneity of
neuronal firing based on passive and active dendritic conduction along the apical den-
dritic core conductors. In this fashion, the time-coherent activity of the specific and
nonspecific oscillatory inputs, obtained by summing distal and proximal activity in
given dendritic elements, would enhance de facto 40-Hz cortical coherence by their
multimodal character. And in this way it provides one mechanism for global binding.
The “specific” system would supply the content that relates to the external world, and
the nonspecific system would give rise to the temporal conjunction, or the context (on
the basis of a more interoceptive context concerned with alertness). Together they
would generate a single cognitive experience. Furthermore, when this rhythmicity is
altered in particular fashions, neurological and psychiatric conditions ensue.
174 ANNALS NEW YORK ACADEMY OF SCIENCES
This work was supported by Grant NS13742 (to R.L.) from the National Insti-
tutes of Health (NINCDS) and by the Charles A. Dana Foundation.
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