Pupil fluctuations track fast switching of cortical states during quiet wakefulness.
Neural responses are modulated by brain state, which varies with arousal, attention, and behavior. In mice, running and whisking desynchronize the cortex and enhance sensory responses, but the quiescent periods between bouts of exploratory behaviors have not been well studied. We found that these periods of "quiet wakefulness" were characterized by state fluctuations on a timescale of 1-2 s. Small fluctuations in pupil diameter tracked these state transitions in multiple cortical areas. During dilation, the intracellular membrane potential was desynchronized, sensory responses were enhanced, and population activity was less correlated. In contrast, constriction was characterized by increased low-frequency oscillations and higher ensemble correlations. Specific subtypes of cortical interneurons were differentially activated during dilation and constriction, consistent with their participation in the observed state changes. Pupillometry has been used to index attention and mental effort in humans, but the intracellular dynamics and differences in population activity underlying this phenomenon were previously unknown.
Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA. Electronic address: jreimer@cns.bcm.edu.
Jacob
J
Reimer
Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA.
Emmanouil
E
Froudarakis
Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA.
Cathryn R
CR
Cadwell
Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA.
Dimitri
D
Yatsenko
Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA.
George H
GH
Denfield
Department of Neuroscience, Baylor College of Medicine, Houston, TX 77030, USA; Department of Computational and Applied Mathematics, Rice University, Houston, TX 77005, USA. Electronic address: atolias@cns.bcm.edu.
Andreas S
AS
Tolias
D000818:Animals; D001288:Attention / Q000502:physiology; D001921:Brain / Q000502:physiology*; D004569:Electroencephalography / Q000379:methods; D005106:Exploratory Behavior / Q000502:physiology*; D008564:Membrane Potentials / Q000502:physiology; D051379:Mice; D009474:Neurons / Q000502:physiology; D011680:Pupil / Q000502:physiology*; D013997:Time Factors; D014738:Vibrissae / Q000502:physiology; D014851:Wakefulness / Q000502:physiology*