Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Hippocampal Neurons Respond During Free Recall



Science 3 October 2008: Vol. 322. no. 5898, pp. 96 - 101

Internally Generated Reactivation of Single Neurons in Human Hippocampus During Free Recall

Hagar Gelbard-Sagiv,1 Roy Mukamel,2 Michal Harel,1 Rafael Malach,1 Itzhak Fried2,3*

1 Department of Neurobiology, Weizmann Institute of Science, Rehovot, 76100, Israel.
2 Department of Neurosurgery, David Geffen School of Medicine, and Semel Institute for Neuroscience and Human Behavior, University of California Los Angeles, Los Angeles, CA 90095, USA.
3 Functional Neurosurgery Unit, Tel Aviv Medical Center and Sackler School of Medicine, Tel Aviv University, Tel Aviv, 64239, Israel.


The emergence of memory, a trace of things past, into human consciousness is one of the greatest mysteries of the human mind. Whereas the neuronal basis of recognition memory can be probed experimentally in human and nonhuman primates, the study of free recall requires that the mind declare the occurrence of a recalled memory (an event intrinsic to the organism and invisible to an observer). Here, we report the activity of single neurons in the human hippocampus and surrounding areas when subjects first view cinematic episodes consisting of audiovisual sequences and again later when they freely recall these episodes. Subjects were patients with pharmacologically intractable epilepsy implanted with depth electrodes to localize the focus of seizure onset. For each patient, the placement of the depth electrodes was determined exclusively by clinical criteria.

The human hippocampus and its associated structures in the medial temporal lobe (MTL) transform present experience into future conscious recollections. Human MTL neurons respond in a highly specific manner to complex stimulus features, to complex stimulus categories, to individual persons or landmarks, and to previously seen and novel stimuli. These responses have been demonstrated for stationary stimuli and are usually brief, often lasting between 300 and 600 ms following stimulus onset, and rarely persist beyond 1 to 2 s.

Neurons that responded during viewing of a particular clip also responded during recall of that clip. Firing rate was elevated to an average of 15.57 Hz, compared with 2.11 and 2.23 Hz during other clips and blank periods

A neuron in left anterior hippocampus responded with elevated firing rate throughout a single clip from a choice of 48 clips. This cell also exhibited shorter, transient neuronal responses to other clips, i.e., consistent elevation of firing rate above baseline only during particular segments of the clip, possibly reflecting the preference of the cell to a specific feature of the clip or to an episode within the clip

The unit's firing rate rose to more than 3 sigma above baseline about 1500 ms before onset of the verbal report of recall, peaked about 100 ms before verbal report onset, but returned to baseline only after 10 s or more

This recurrence during free recall of the same selective neuronal responses present during viewing was found in the population of hippocampal and entorhinal units but not in medial frontal lobes. The frontal lobes exhibited a significant selective increase in firing rate during viewing, but not during recall.

This episode-specific reactivation phenomenon was weak in amygdala and absent from parahippocampal gyrus, but was particularly striking for hippocampal and entorhinal neurons with sustained responses.

In conclusion, we report here that a subset of neurons in the human hippocampus and entorhinal cortex exhibited highly reliable and specific responses during viewing of video episodes. The same neurons showed an increased firing rate again with free conscious recall. This recurrence during recall of specific past neuronal activity was not observed in medial frontal cortex sites. However, it is possible that top-down early recall signals do originate in other frontal or temporal lobe regions not sampled in this study

The responses to episodes observed here were often remarkably selective and relatively sparse. Whether multiple clips to which a neuron responds may be related by some abstract association rule is not clear at present. It is also important to exercise caution in claims as to what exact aspect of the clips the cell responded to. The critical point, however, is that the same selective responses recur during free recall.

Several neuroimaging studies show that brain activity present during the learning of information, as indirectly measured by the BOLD signal, is reinstated during cued or free recall, although spatiotemporal limits of fMRI restrict the possible conclusions.

The sparse neuronal responses arising from a very low baseline to robust firing during a specific episode are reminiscent of the responses of hippocampal place cells in rodents, in which a cell responds whenever the animal is in a particular place in the environment. The hippocampal and entorhinal machinery used in spatial navigation in rodents may have been preserved in humans but put to a more elaborate and abstract use.

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