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Neuropsychologia. 2015 Sep;76:108-24. doi: 10.1016/j.neuropsychologia.2015.03.021. Epub 2015 Mar 20.

Laminar profile of spontaneous and evoked theta: Rhythmic modulation of cortical processing during word integration.

Author information

1
Departments of Radiology and Neurosciences, University of California at San Diego, La Jolla, CA 92069, USA. Electronic address: ehalgren@ucsd.edu.
2
Interdepartmental Neurosciences Program, University of California at San Diego, La Jolla, CA 92069, USA.
3
Department of Psychology, San Diego State University, San Diego, CA, USA.
4
Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02129, USA.
5
Departments of Radiology and Neurosciences, University of California at San Diego, La Jolla, CA 92069, USA; Interdepartmental Neurosciences Program, University of California at San Diego, La Jolla, CA 92069, USA; Department of Psychology, San Diego State University, San Diego, CA, USA; Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02129, USA; Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA; Department of Neurosurgery, Children's Hospital, Harvard Medical School, Boston, MA, USA; Institute of Cognitive Neuroscience and Psychology, Research Center for Natural Sciences, Hungarian Academy of Sciences, Budapest-1117, Hungary.
6
Department of Neurology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA.
7
Department of Neurosurgery, Children's Hospital, Harvard Medical School, Boston, MA, USA.
8
Institute of Cognitive Neuroscience and Psychology, Research Center for Natural Sciences, Hungarian Academy of Sciences, Budapest-1117, Hungary.

Abstract

Theta may play a central role during language understanding and other extended cognitive processing, providing an envelope for widespread integration of participating cortical areas. We used linear microelectrode arrays in epileptics to define the circuits generating theta in inferotemporal, perirhinal, entorhinal, prefrontal and anterior cingulate cortices. In all locations, theta was generated by excitatory current sinks in middle layers which receive predominantly feedforward inputs, alternating with sinks in superficial layers which receive mainly feedback/associative inputs. Baseline and event-related theta were generated by indistinguishable laminar profiles of transmembrane currents and unit-firing. Word presentation could reset theta phase, permitting theta to contribute to late event-related potentials, even when theta power decreases relative to baseline. Limited recordings during sentence reading are consistent with rhythmic theta activity entrained by a given word modulating the neural background for the following word. These findings show that theta occurs spontaneously, and can be momentarily suppressed, reset and synchronized by words. Theta represents an alternation between feedforward/divergent and associative/convergent processing modes that may temporally organize sustained processing and optimize the timing of memory formation. We suggest that words are initially encoded via a ventral feedforward stream which is lexicosemantic in the anteroventral temporal lobe; its arrival may trigger a widespread theta rhythm which integrates the word within a larger context.

KEYWORDS:

Cingulate; Current-source density; Delta; Entorhinal; Feedback; Feedforward; Gamma; Inferotemporal; Perirhinal; Prefrontal

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