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Scientific Understanding of Consciousness |
Consciousness and the Thalamocortical Loop
International Congress Series, Volume 1250, October 2003, Pages 409-416 Consciousness and the thalamocortical loop Rodolfo Llinás Department of Physiology and Neuroscience, New York University Medical School, 550 First Avenue, New York, NY 10016, USA (Paraphrase) One aspect of the brain’s neuronal organization that seems particularly central to global function is the rich thalamocortical interconnectivity and most particularly the reciprocal nature of the thalamocortical neuronal loop function. Moreover, the interaction between the specific and nonspecific thalamic loops suggests that rather than a gate into the brain, the thalamus represents a hub from which any site in the cortex can communicate with any other such site or sites. The goal of this paper is to explore the basic assumption that large-scale, temporal coincidence of specific and nonspecific thalamic activity generates the functional states that characterize human cognition. Prior research suggests that the brain is a closed system generating intrinsic electrical activity via its component neurons and their connectivity. The CNS is a "reality"-emulating system, with the parameters of the "reality" delineated by the senses.The thalamic input from the cortex is larger than that from the peripheral sensory system, suggesting that thalamocortical iterative recurrent activity is the basis for consciousness. 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 will yield. A second organizing principle may be equally important—one that is based on the temporal rather than on the spatial relationships among neurons. This temporal mapping may be viewed as a type of functional geometry. 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 a parameter usually considered in neuroscience. Temporal mapping and cognitive conjunction Synchronous neuronal activation during sensory input has recently been studied in the mammalian visual cortical cells. Coherent 40-Hz oscillations throughout the cortical mantle of awake human subjects has been revealed by magnetoencephalagraphy. These oscillations may he reset by sensory stimuli, and phase comparison revealed the presence of a 12- to 13-ms phase shift between the rostral and caudal poles of the brain. These gamma oscillations display a high degree of spatial organization and thus may be a candidate mechanism for the production of temporal conjunction of rhythmic activity over a large ensemble of neurons. Thalamocortical resonance and consciousness Based on research on the minimal temporal interval to sensory discrimination, we may conclude that consciousness is a noncontinuous event determined by synchronous activity in the thalamocortical system. Since this activity is present during REM sleep 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 sensory input in the awake state and by intrinsic activity during dreaming. These findings indicate that while the awake state and the REM sleep state are electrically similar with respect to the presence of 40-Hz oscillations, a central difference is the inability of sensory input to reset the 40-Hz activity during REM sleep. By contrast, during delta sleep, the amplitude of these oscillators differs from that of wakefulness and REM sleep but as in REM sleep, there is no 40-Hz sensory 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. We consider this to be the central difference between dreaming and wakefulness. These data suggest that we do not perceive the external world during REM sleep because the intrinsic activity of the nervous system does not place sensory input in the context of the functional state being generated by the brain. 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, neurons in 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 appealing since single neurons burst at 30-40 Hz, especially during REM sleep, which is also consistent with the macroscopic magnetic recordings observed in this study, and is given additional support by the fact that the damage of the intralaminar system results in lethargy or coma. Binding of specific and nonspecific gamma band activity Gamma oscillations in neurons in specific thalamic nuclei establish cortical resonance through direct activation of pyramidal cells and feed forward inhibition through activation of 40-Hz inhibitory interneurons in layer IV. These oscillations re-enter the thalamus via layer-VI pyramidal-cell axon collaterals, producing thalamic feedback inhibition via the reticular nucleus. In a second system, the intralaminar nonspecific thalamic nuclei project to cortical layers I and V and to the reticular nucleus. Layer-V pyramidal cells return oscillations to the reticular nucleus and intralaminar nuclei. The cells in this complex have been shown to oscillate at gamma band frequency and to be capable of recursive activation. These findings suggests a hypothesis regarding the overall organization of brain function. First, the "specific" thalamocortical system is viewed as encoding specific sensory and motor activity by the resonant 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. Second, following optimal activation, any such thalamocortical 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 description into a single cognitive event. We propose that this could come about by the concurrent summation of specific and nonspecific 40-Hz activity along the radial dendritic axis of given cortical elements, that is, by coincidence detection.
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