Theta and High-Frequency Activity Mark Spontaneous Recall of Episodic Memories

Abstract

Humans possess the remarkable ability to search their memory, allowing specific past episodes to be re-experienced spontaneously. Here, we administered a free recall test to 114 neurosurgical patients and used intracranial theta and high-frequency activity (HFA) to identify the spatiotemporal pattern of neural activity underlying spontaneous episodic retrieval. We found that retrieval evolved in three electrophysiological stages composed of: (1) early theta oscillations in the right temporal cortex, (2) increased HFA in the left hemisphere including the medial temporal lobe (MTL), left inferior frontal gyrus, as well as the ventrolateral temporal cortex, and (3) motor/language activation during vocalization of the retrieved item. Of these responses, increased HFA in the left MTL predicted recall performance. These results suggest that spontaneous recall of verbal episodic memories involves a spatiotemporal pattern of spectral changes across the brain; however, high-frequency activity in the left MTL represents a final common pathway of episodic retrieval.

Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility?

“…This approach was recently used to map the brain regions responsible for episodic memory encoding [27] and retrieval [4] during verbal free recall (modified in Figure 2A). During successful memory encoding, HFA could be separated into two spatiotemporal distinct stages: an early stage consisting of HFA increases along the ventral visual pathway culminating in hippocampal activation ( Early Encoding ; Figure 2A), and a late stage consisting of HFA increases in discrete areas of the left neocortex ( Late Encoding ; Figure 2A) [27].…”

“…During successful memory encoding, HFA could be separated into two spatiotemporal distinct stages: an early stage consisting of HFA increases along the ventral visual pathway culminating in hippocampal activation ( Early Encoding ; Figure 2A), and a late stage consisting of HFA increases in discrete areas of the left neocortex ( Late Encoding ; Figure 2A) [27]. Episodic retrieval could be similarly staged into (1) early retrieval, consisting of a decrease in HFA in the right temporal cortex ( Early Retrieval ; Figure 2A), (2) late retrieval, consisting of an increase in HFA in the left neocortex and medial temporal lobe immediately before spontaneous recall ( Late Retrieval ; Figure 2A) and finally (3) motor/language activation during vocalization of the recalled item ( Response Production ; Figure 2A) [4]. Of note, theta oscillations (not shown) occurred simultaneously with decreases in HFA during early retrieval.…”

“…Radiological slice view is shown with right (R) and left (L) hemispheres labeled. Data modified from [4] and [27]. B: In the left medial temporal lobe (MTL), HFA correlated with overall memory performance across patients (r=0.3911, p=0.0015).…”

“…For example, HFA in the medial temporal lobe (MTL) increases during both episodic memory retrieval [4] and working memory load [5]. In the posteromedial cortex, HFA increases during the retrieval of autobiographical memories [6].…”

Is it time to replace epileptic spikes with fast ripples?

“…4 It is of importance to distinguish HFOs as distinct burstlike events in contrast to continuous HFO activity during cognitive processing that is locked to stimulus events. 4,13 The value of recording interictal spikes with electrocorticography as a biomarker to tailor resections has been disputed. 2 van 't Klooster et al confirmed that spikes are not a good biomarker for the epileptogenic zone, and their removal is not correlated with a good seizure outcome.…”