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

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.

Oscillatory dynamics of perceptual to conceptual transformations in the ventral visual pathway

“…Together, this suggests a functional dissociation between theta and alpha in cortex. Theta activity in the hippocampus and medial temporal lobes is tightly linked to long term memory (Fell and Axmacher, 2011;Fell et al, 2001;Halgren et al, 2015;Sederberg et al, 2003;Staresina et al, 2012). Our theta effects for semantic object properties in the pVTC and ATL are consistent with intracranial recordings in humans from anterior IT and the PRC which show a modulation of theta activity according to the semantic category of words (Halgren et al, 2015), where it is further hypothesised that ATL structures aid the encoding of attributes in coordination with theta in the hippocampus (Fell et al, 2001;Halgren et al, 2015;Staresina et al, 2012).…”

“…Crucially, recurrent activity will be associated with the activation of semantic object information that will also depend on the coordinated activity within the VVP. Whilst visual object properties are predicted in alpha (VanRullen et al, 2014), semantic information may be more associated with theta activity (Halgren et al, 2015) and gamma activity (Mollo et al, 2017;Supp et al, 2007).…”

Intracranial neuronal ensemble recordings and analysis in epilepsy

“…In contrast, the disadvantage of microarrays placed within macroarrays lies in the difficulty to control the implantation depth and therefore the cortical (or subcortical) layer it probes. This type of paired micro/macroelectrode is typically to study activity from deep structures such as the mesial temporal lobe (Jacobs et al, 2007;Kreiman et al, 2002;Ogren et al, 2009;Quiroga et al, 2005) or frontoparieto-medial surfaces (Halgren et al, 2015). Due to the nature of its design, neocortical sites cannot be approached by this technique.…”

“…This probe consists of a long shaft of the thumbtack without the flat head, designed to insert into the lumen of the depth macro-electrode, allowing the laminar probe to reach hippocampal, parahippocampal, frontobasal, and cingular surfaces (Halgren et al, 2015).…”

“…Unit recordings in epileptic patients will be important to develop a deeper understanding of different kinds of multisensory integration processes such as visual, both in motion detection or emotional reactions (Kawasaki et al, 2001), and auditory and speech functions (Halgren et al, 2015).…”