A Specific Role for the Thalamus in Mediating the Interaction of Attention and Arousal in Humans

The physiological basis for the interaction of selective attention and arousal is not clearly understood. Here we present evidence in humans that specifically implicates the thalamus in this interaction. We used functional magnetic resonance imaging to measure brain activity during the performance of an attentional task under different levels of arousal. Activity evoked in the ventrolateral thalamus by the attentional task changed as a function of arousal. The highest level of attention-related thalamic activity is seen under conditions of low arousal (secondary to sleep deprivation) compared with high arousal (secondary to caffeine administration). Other brain regions were also active during the attentional task, but these areas did not change their activity as a function of arousal. Control experiments establish that this pattern of changes in thalamic activity cannot be accounted for by nonspecific effects of arousal on cerebral hemodynamics. We conclude that the thalamus is involved in mediating the interaction of attention and arousal in humans.

[1]  G Mann,et al.  ON THE THALAMUS * , 1905, British medical journal.

[2]  J. Easterbrook.  The effect of emotion on cue utilization and the organization of behavior. , 1959, Psychological review.

[3]  M. Meldman.  Attention, Arousal and the Orientation Reaction , 1967 .

[4]  A. Luria.  The Working Brain , 1973 .

[5]  D. Kahneman,et al.  Attention and Effort , 1973 .

[6]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[7]  Raja Parasuraman,et al.  Varieties of attention , 1984 .

[8]  F. Crick.  Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[9]  R. Heslegrave,et al.  The effects of task duration and work-session location on performance degradation induced by sleep loss and sustained cognitive work , 1985 .

[10]  M. Lader,et al.  The psychopharmacological and electrophysiological effects of single doses of caffeine in healthy human subjects. , 1986, British journal of clinical pharmacology.

[11]  P. Goldman-Rakic.  Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[12]  D. LaBerge,et al.  Theory of attentional operations in shape identification. , 1989 .

[13]  O. Cameron,et al.  Caffeine and human cerebral blood flow: a positron emission tomography study. , 1990, Life sciences.

[14]  D. LaBerge,et al.  Positron emission tomographic measurements of pulvinar activity during an attention task , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  D. McCormick,et al.  Functional implications of burst firing and single spike activity in lateral geniculate relay neurons , 1990, Neuroscience.

[16]  Daniel J Buysse,et al.  Sleep stage physiology, mood, and vigilance responses to total sleep deprivation in healthy 80-year-olds and 20-year-olds. , 1990, Psychophysiology.

[17]  T. Roth,et al.  Alerting effects of caffeine after normal and restricted sleep. , 1991, Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology.

[18]  H. Babkoff,et al.  Subjective sleepiness ratings: the effects of sleep deprivation, circadian rhythmicity and cognitive performance. , 1991, Sleep.

[19]  T. Roth,et al.  Enforced 24-hour recovery following sleep deprivation. , 1991, Sleep.

[20]  M. Buchsbaum,et al.  The effect of sleep deprivation on cerebral glucose metabolic rate in normal humans assessed with positron emission tomography. , 1991, Sleep.

[21]  M. Raichle,et al.  Localization of a human system for sustained attention by positron emission tomography , 1991, Nature.

[22]  R. Turner.  Magnetic resonance imaging of brain function , 1992, American journal of physiologic imaging.

[23]  David LaBerge,et al.  A Network Simulation of Thalamic Circuit Operations in Selective Attention , 1992, Neural Computation.

[24]  D. Perrett,et al.  Brain mechanisms of perception and memory : from neuron to behavior , 1993 .

[25]  D. V. van Essen,et al.  A neurobiological model of visual attention and invariant pattern recognition based on dynamic routing of information , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  A. Muzet,et al.  Interaction of the Alerting Effect of Noise with Partial Sleep Deprivation and Circadian Rhythmicity of Vigilance , 1993, Perceptual and motor skills.

[27]  D. Contreras,et al.  The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  Edward E. Smith,et al.  Spatial working memory in humans as revealed by PET , 1993, Nature.

[29]  Karl J. Friston,et al.  Investigations of the functional anatomy of attention using the stroop test , 1993, Neuropsychologia.

[30]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[31]  J. Naglieri,et al.  Assessment of cognitive processes : the PASS theory of intelligence , 1994 .

[32]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  M. Corbetta,et al.  PET studies of parietal involvement in spatial attention: comparison of different task types. , 1994, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[34]  M. Posner,et al.  Attentional networks , 1994, Trends in Neurosciences.

[35]  M. Posner.  Attention: the mechanisms of consciousness. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Karl J. Friston,et al.  Analysis of functional MRI time‐series , 1994, Human Brain Mapping.

[37]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[38]  The sketchpad model. A theory of consciousness, perception, and imagery. , 1995, Consciousness and cognition.

[39]  R. Passingham,et al.  Functional anatomy of the mental representation of upper extremity movements in healthy subjects. , 1995, Journal of neurophysiology.

[40]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[41]  J. Newman.  Thalmic Contributions to Attention and Consciousness , 1995, Consciousness and Cognition.

[42]  M. Hallett,et al.  Cerebral structures participating in motor preparation in humans: a positron emission tomography study. , 1996, Journal of neurophysiology.

[43]  R. Kronauer,et al.  Simulations of light effects on the human circadian pacemaker: implications for assessment of intrinsic period. , 1996, The American journal of physiology.

[44]  Karl J. Friston,et al.  The Role of the Thalamus in “Top Down” Modulation of Attention to Sound , 1996, NeuroImage.

[45]  E. Courchesne,et al.  Attentional Activation of the Cerebellum Independent of Motor Involvement , 1997, Science.

[46]  Karl J. Friston,et al.  Subtractions, conjunctions, and interactions in experimental design of activation studies , 1997, Human brain mapping.

[47]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[48]  R. Dolan,et al.  The Neural Correlates of the Noradrenergic Modulation of Human Attention, Arousal and Learning , 1997, The European journal of neuroscience.

[49]  R. Guillery,et al.  Paying attention to the thalamic reticular nucleus , 1998, Trends in Neurosciences.