Firework Memories: Neural Mechanism Central to Human Free Recall Identified

Summary: Hippocampal short-wave ripples trigger spontaneous recollections and reinstate cortical representation during free recall of episodic memories.

Source: Weizmann Institute of Science

Extraterrestrial scientists landing in a football stadium would be struck by the sight of the crowd suddenly standing up and shouting in unison. In a similar manner, since the nineties, researchers have observed a special pattern of neuronal activity in rodents: tens of thousands of nerve cells firing in unison in a part of the brain called the hippocampus. But, like an alien scientist, the researchers have not been able to understand the “language” of the rodents’ minds when these mysterious synchronous bursts occurred. Recently Weizmann Institute scientists succeeded in recording these rapid bursts of activity – called “hippocampal ripples” – in the human brain, and they were able to demonstrate their importance as a neuronal mechanism underlying the engraving of new memories and their subsequent recall. These findings appear today in Science.

“The ripple is an amazing event in its intensity and timing. It is an orchestrated burst of synchronous activation by about 15% of hippocampal neurons – all firing together within about a tenth of a second. It’s a nerve-cell fireworks display,” explains Prof. Rafi Malach of the Institute’s Neurobiology Department. It was first revealed that they emerge during mental states of sleep and rest, and that they play an important role in rodents’ spatial navigational memory. Only recently it was found that such synchronous electrical activity in large groups of neurons also occurs in the primate hippocampus during the awake state. However, until now, scientists have been kept in the dark as to the roles the ripples play in human cognition and mental activity.

Humans can, of course, communicate their thoughts, but most research methods do not give scientists a detailed view of what happens at the same time within the brain. Yitzhak Norman, a PhD student in Malach’s lab, who led the current research in collaboration with the group of Prof. Ashesh Mehta from the Feinstein Institute for Medical Research in the US, recruiting patients who undergo invasive recordings in the course of their medical diagnosis. In this clinical procedure, patients suffering from intractable epilepsy get electrodes implanted in multiple brain regions to locate the epileptic focus and surgically remove it. These patients freely volunteered to participate in the memory experiments while they waited in the hospital between seizures.

During the experiment, the patients were presented with pictures, rich in color and visual detail, of either faces of famous people (e.g., Barack Obama, Uma Thurman) or famous monuments (e.g., the Statue of Liberty, the Leaning Tower of Pisa). The patients were asked to try to remember these pictures in as much detail as possible. After this picture-viewing stage, and following a short distraction task, they were asked, with their eyes covered, to freely recall the pictures and describe them in detail. Throughout the experiment, the talking of the patients was recorded simultaneously with their corresponding brain activity, which was revealed through the electrodes implanted both in the hippocampus, as well as other regions in the cerebral cortex.

Correlating the brain’s activity and the patient’s verbal reports revealed a number of striking observations. First, it was found that ripple-bursts had a critical role in the free recall process: about a second or two before the patients recalled and began describing a new picture, there was a significant increase in the ripple rate anticipating their recall. Importantly, the hippocampal ripples re-expressed the content of the pictures: pictures that elicited a higher number of ripples during the viewing stage also elicited a higher number of ripples during the subsequent recall.

this shows a brain scan with the hippocampus highlighted

Electrode (yellow dots) implanted in the hippocampus of a patient undergoing epilepsy monitoring, viewed with MRI. Colors indicate sub regions of the hippocampus. Sharp wave ripples appear most prominently in the CA1 region, shown in red. The image is credited to Weizmann Institute of Science.

Since brain activity was recorded simultaneously in the hippocampus and the cerebral cortex, the researchers were able to demonstrate that the ripples were synchronized with cortical activation, specifically in the visual centers of the brain where the detailed visual information is likely to be stored. Furthermore, high-level visual centers are known to be specialized in representing specific visual categories – for example, faces are represented in one cortical region and monuments in another region. Accordingly, when patients recalled a face, for example, Barack Obama, or alternatively, a monument, such as the Eiffel Tower, cortical activity was selectively enhanced in the corresponding visual centers. Norman explains: “An orchestrated action across a number of centers is revealed during free recall, with the hippocampus playing the role of the conductor.”

The findings substantially expand our understanding of the function of the hippocampus. They emphasize the importance of synchronized neuronal group activity. The hippocampal burst, it should be remembered, involves the synchronous activation of hundreds of thousands of nerve cells. “This constitutes a major advance in our understanding of neuronal mechanisms underlying human memory,” summarizes Malach. “Engraving memories, their storage and their recall are naturally dependent on a complex set of processes. However, the ‘neuronal drama’ of such synchronized hippocampal bursts clearly points to their central role in memory formation and recall.”

Funding: Prof. Rafael Malach’s research is supported by the Dr. Lou Siminovitch Laboratory for Research in Neurobiology; and the estate of Florence and Charles Cuevas. Prof. Malach is the incumbent of the Barbara and Morris L. Levinson Professorial Chair in Brain Research.

About this neuroscience research article

Source:
Weizmann Institute of Science
Media Contacts:
Gizel Maimon – Weizmann Institute of Science
Image Source:
The image is credited to Weizmann Institute of Science.

Original Research: Closed access
“Hippocampal sharp-wave ripples linked to visual episodic recollection in humans”. Rafi Malach et al.
Science. doi:10.1126/science.aax1030

Abstract

Hippocampal sharp-wave ripples linked to visual episodic recollection in humans

INTRODUCTION
Sharp-wave ripples (SWRs) are rapid bursts of synchronized neuronal activity elicited by the hippocampus. Extensive study of SWRs, mainly in the rodent brain, has linked these bursts to navigation, memory formation, and offline memory consolidation. However, fundamental questions remain regarding the functional meaning of this striking example of network synchrony. Perhaps the most glaring unknown is the relationship between SWRs and conscious cognition. We still do not know what cognitive process, if any, is linked to the emergence of SWRs; to put it simply, we still do not know what an animal thinks about (if anything) when the hippocampus elicits a ripple. Furthermore, the potential role of SWRs in human episodic memory is still largely unknown. Thus, studying this phenomenon in conscious, awake human patients opens a unique window, as it allows direct examination of detailed verbal reports with respect to SWR occurrences.

RATIONALE
We took advantage of the unique ability of humans to communicate verbally about their inner cognitive state to examine the role of SWRs in memory formation and retrieval, using intracranial electrophysiological recordings in patients. This approach allowed us to study free recall, the process of self-initiated, internal generation of memories. It is a uniquely powerful approach because it isolates the process of recall from external stimulation.

RESULTS
Our study revealed three major aspects linking SWRs to human declarative memory. First, the SWR rate during picture viewing (i.e., memory encoding) predicted subjects’ subsequent free-recall performance. Second, a transient increase in SWR rate preceded the verbal report of recall by 1 to 2 s. This increase was content-selective, recapitulating the same picture preferences observed during viewing. Finally, during recollection, high-order visual areas showed content-selective reactivation coupled to SWR emission.

CONCLUSION
By direct recordings of electrophysiological events in the brains of individuals who could inform, in real time, on their cognitive state, we were able to demonstrate and characterize an important role of SWRs in human episodic memory. Our findings point to the involvement of hippocampal SWRs in establishing and triggering spontaneous recollections in the human brain. They implicate SWRs in the process of engraving new memories, and reveal their fundamental contribution in orchestrating the dialogue between memory centers (hippocampus) and high-level representations (cerebral cortex), which underlies the retrieval of these memories. Our study thus highlights the function of SWRs as powerful multitasking signals that contribute both to the encoding and to the spontaneous access and reinstatement of human memories.

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