Theta Oscillations in Human Cortex During a Working-Memory Task: Evidence for Local Generators

Abstract

Cortical theta appears important in sensory processing and memory. Intracanial electrode recordings provide a high spatial resolution method for studying such oscillations during cognitive tasks. Recent work revealed sites at which oscillations in the theta range (4-12 Hz) could be gated by a working-memory task: theta power was increased at task onset and continued until task offset. Using a large data set that has now been collected (10 participants/619 recording sites), we have sufficient sampling to determine how these gated sites are distributed in the cortex and how they are synchronized. A substantial fraction of sites in occipital/parietal (45/157) and temporal (23/280) cortices were gated by the task. Surprisingly, this aspect of working-memory function was virtually absent in frontal cortex (2/182). Coherence measures were used to analyze the synchronization of oscillations. We suspected that because of their coordinate regulation by the working-memory task, gated sites would have synchronized theta oscillations. We found that, whereas nearby gated sites (<20 mm) were often but not always coherent, distant gated sites were almost never coherent. Our results imply that there are local mechanisms for the generation of cortical theta.

Selective, State-Dependent Activation of Somatostatin-Expressing Inhibitory Interneurons in Mouse Neocortex

“…These values-all larger than those reported by Beierlein et al (2003)-could be due to differences between layers 2/3 and 4. GIN cells share many characteristics with inhibitory interneurons identified in other studies as bitufted cells (Reyes et al 1998), regular-spiking nonpyramidal somatostatin-expressing neurons (Cauli et al 2000), and LTS (low-threshold-spiking) cells (Amitai et al 2002;Beierlein et al 2000Beierlein et al , 2003Gibson et al 1999;Kawaguchi and Kubota 1996).…”

“…In contrast to the IPSPs of GIN 3 RS connections, the EPSPs of RS 3 GIN connections showed substantial frequency-dependent facilitation in the 3-to 40-Hz frequency range (Fig. 3, B and D ;Beierlein et al 2003;Reyes et al 1998). …”

“…In this respect, they act as a sort of filter of incoming excitatory activity, faithfully transmitting abrupt increases in input, but not persistent firing (Abbott and Regehr 2004). This characteristic is typical of synapses that display an initial high probability of neurotransmitter release (Abbott and Regehr 2004;Reyes et al 1998;Watanabe et al 2005).…”

“…Theta-frequency oscillations have been observed in the neocortex both in vitro (Bao and Wu 2003;Flint and Connors 1996;Lukatch and MacIver 1997;Silva et al 1991) andin vivo (Canolty et al 2006;Kahana et al 2001;Raghavachari et al 2006) and have been proposed to play a role in functions such as working memory and synaptic plasticity (Kahana et al 2001;Raghavachari et al 2006;Werk and Chapman 2003). However, the mechanism(s) that generate neocortical as well as hippocampal theta rhythms are not well elucidated (reviewed in Buzsáki 2002) and our results suggest GIN cell activity could be a novel mechanism for inducing or supporting theta oscillations by exerting a networkwide inhibitory thetarange rhythm.…”

Frontal midline theta connectivity is related to efficiency of WM maintenance and is affected by aging

“…One of the putative hypotheses suggests that theta oscillation might coordinate the activation of relevant object information maintained in more posterior brain regions during WM (Sauseng, 2005), whereas the other assumes that theta activity regulates the activation of different items such that each item representation is sequentially activated at different phase of the theta cycle based on the temporal order in which it is perceived (Raghavachari et al, 2006). A possible function of theta oscillation is to hold memory representations in an active state by providing a sustained neural activation that can bridge the temporal gap of the delay period between stimulus presentation and memory test (McClelland et al, 1995).…”