Interactions between thalamic and cortical rhythms during semantic memory recall in human

Abstract

Human scalp electroencephalographic rhythms, indicative of cortical population synchrony, have long been posited to reflect cognitive processing. Although numerous studies employing simultaneous thalamic and cortical electrode recording in nonhuman animals have explored the role of the thalamus in the modulation of cortical rhythms, direct evidence for thalamocortical modulation in human has not, to our knowledge, been obtained. We simultaneously recorded from thalamic and scalp electrodes in one human during performance of a cognitive task and found a spatially widespread, phase-locked, low-frequency rhythm (7-8 Hz) power decrease at thalamus and scalp during semantic memory recall. This low-frequency rhythm power decrease was followed by a spatially specific, phase-locked, fast-rhythm (21-34 Hz) power increase at thalamus and occipital scalp. Such a pattern of thalamocortical activity reflects a plausible neural mechanism underlying semantic memory recall that may underlie other cognitive processes as well.E lectroencephalographic (EEG) fast rhythm power increases have been shown to occur during numerous cognitive tasks, including learning, reading, face perception, posture recognition, and chess playing (1-5). Cortical electrode recording in cat (6-9) and nonhuman primate (10) during visual perception indicates that phase-locked, fast rhythm power can reflect synchronous activity between distinct neuronal populations that may ''bind'' features into unitary objects. Simultaneous thalamic and cortical electrode recording in cat and thalamic computational modeling indicate that low-frequency (7-14 Hz) and fast cortical rhythms (11) are influenced by spatially widespread (12, 13) and spatially specific (14-16) thalamocortical connections, respectively. Similar to findings in cat, there is convincing evidence that human thalamus interacts with fast cortical rhythms (17,18).Although fast rhythms have been postulated to reflect other cognitive functions, the role of such rhythms in semantic recall has not been explored. Recent functional MRI (fMRI) results (19,20) suggest that the human thalamus is involved during semantic memory recall. We hypothesized that fMRI thalamic activation during semantic recall could reflect a thalamocortical interaction associated with this memory component. To investigate this possibility, we simultaneously recorded from thalamic and scalp electrodes and conducted epoch-based frequency analysis. To our knowledge, this is the first time in human when such a procedure has been conducted during a cognitive process, revealing a phase-locked, thalamocortical fast rhythm during semantic memory recall.

Transient relay function of midline thalamic nuclei during long-term memory consolidation in humans

“…Moreover, PPI parameters do not provide information about the underlying neuronal mechanisms and cannot reveal whether different brain regions share the computation of information or if one brain region provides information for another. Nonetheless, our findings are consistent with models that are based on neurophysiological data describing functionally specific thalamo-cortical interactions (Slotnick et al 2002) that enable feature binding (Engel et al 1997). In this framework, the retrieval of "partly" consolidated memories may require increased midline thalamic support in binding or integrating cortically distributed information.…”

The increase in medial prefrontal glutamate/glutamine concentration during memory encoding is associated with better memory performance and stronger functional connectivity in the human medial prefrontal–thalamus–hippocampus network

“…With respect to the functional connectivity to the dorsal margin of the thalamus, albeit speculative, one may assume that this thalamic region represents the thalamic reticular nucleus (Viviano and Schneider, 2015; Zikopoulos and Barbas, 2006; Jones, 1985), a layer of GABAergic cells wrapping the dorsolateral segments of the thalamus (Jones, 1985; Zikopoulos and Barbas, 2006). GABAergic neurons in the thalamic reticular nucleus modulate both corticothalamic and thalamocortical communications (Slotnick, Moo, Kraut, Lesser, & Hart, 2002; Lozsádi, 1995; Steriade, Contreras, Curró Dossi, & Nuñez, 1993; Jones, 1985). For instance, the thalamic reticular nucleus receives excitatory inputs from cortex and other thalamic nuclei and sends inhibitory projections (GABAergic) back to thalamic nuclei thereby controlling the activity/oscillations in thalamocortical loops (Slotnick et al, 2002; Lozsádi, 1995; Steriade et al,1993).…”

“…GABAergic neurons in the thalamic reticular nucleus modulate both corticothalamic and thalamocortical communications (Slotnick, Moo, Kraut, Lesser, & Hart, 2002; Lozsádi, 1995; Steriade, Contreras, Curró Dossi, & Nuñez, 1993; Jones, 1985). For instance, the thalamic reticular nucleus receives excitatory inputs from cortex and other thalamic nuclei and sends inhibitory projections (GABAergic) back to thalamic nuclei thereby controlling the activity/oscillations in thalamocortical loops (Slotnick et al, 2002; Lozsádi, 1995; Steriade et al,1993). Brain oscillations result in synaptic plasticity via synchronizing and desynchronizing neural assemblies and are therefore one of the core mechanisms underlying episodic memory (Hanslmayr, Staresina, & Bowman, 2016).…”

Subcortical functions in cognition: Toward a consensus

“…Results suggest the dorsomedial nucleus has a role in early search processes, but the pulvinar participates in binding features into object representations. In addition to these data, the authors cite electrophysiological evidence from their lab in support of the feature binding hypothesis (Slotnick et al, 2002).…”