Human medial temporal lobe neurons respond preferentially to personally relevant images

Abstract

People with whom one is personally acquainted tend to elicit richer and more vivid memories than people with whom one does not have a personal connection. Recent findings from neurons in the human medial temporal lobe ( epilepsy ͉ hippocampus ͉ memory ͉ familiarity ͉ single-unit recordings H umans are self-absorbed by nature. One virtually infallible method of enhancing memory is simply to relate the to-be-remembered information to one's self. The self-reference effect (1) is a well-documented encoding enhancement: people are more likely to remember items that are personally relevant, than items that have undergone some other deep or semantically elaborative encoding processes (2). One mechanism by which the self-referent effect might operate is via the incidental recollection of a rich network of information related to past experiences with that particular item. In addition, incidental recollection of related autobiographical associations can lead to performance advantages such as enhanced memory and speeded responding (3). This incidental recollection has been shown to occur in the context of identifying famous people (3), and has also been shown to involve the hippocampus (4, 5). Furthermore, famous faces and names have long been used to query the integrity of recent and remote semantic memory in patients with temporal lobe epilepsy (TLE) (3, 6-11). Finally, autobiographical memory retrieval consistently engages the medial temporal lobe (12), suggesting that cells in this region may respond differentially to faces that elicit autobiographical memory retrieval.Recently, recordings from the human medial temporal lobe (MTL) have shown that individual neurons can be highly selective in terms of the stimuli to which they respond (13). Out of a set of about 100 visual images across several categories, such as faces, animals, and landmarks, some cells showed robust responses to only a handful of pictures pertaining to a single conceptual category, such a particular famous person. This selectivity provides an important clue as to the mechanism by which the brain represents information currently in awareness (14). In animals, selective sparse coding has also been observed in recordings from the MTL (15, 16). In fact, the idea that the MTL represents information using a sparse code is one of the basic tenets of most contemporary memory models (17)(18)(19). Given that the MTL assigns a relatively small number of neurons to a specific stimulus (20), and that the number of stimuli in the environment is very large, does a feature such as personal relevance, which may be related to the incidental recollection of autobiographically significant information (3), make a stimulus more likely to elicit a selective excitatory response from a cell? Here, we address the question of whether individual neurons in the MTL show a preference for personally relevant pictures.In this study, patients with intracranial electrodes implanted for clinical reasons were shown photographs of varying personal relevance: previously unknown faces and...

Decoding movie content from neuronal population activity in the human medial temporal lobe

“…Most participants had neither seen the movie before nor encountered the actors in other media prior to its presentation as part of this study. This interpretation aligns with previous research showing that neuronal selectivity to individuals varies with familiarity and personal relevance, as photos depicting personally known individuals are more likely to elicit selective responses in MTL neurons 37 .…”

Decoding movie content from neuronal population activity in the human medial temporal lobe

“…Most participants had neither seen the movie before nor encountered the actors in other media prior to its presentation as part of this study. This interpretation aligns with previous research showing that neuronal selectivity to individuals varies with familiarity and personal relevance, as photos depicting personally known individuals are more likely to elicit selective responses in MTL neurons 37 .…”

Long-term coding of personal and universal associations underlying the memory web in the human brain

“…This is in agreement with the fact that MTL neurons do not represent visual features, as they show visual invariance (that is, they respond to completely different pictures of the same person)16 and their firing can be triggered by different sensory modalities (responding to the person's written and spoken name)17. Another potential confound is given by the familiarity of the images: since familiar pictures are represented by more neurons18, there is in principle a higher chance of finding neurons firing to pairs of familiar pictures compared with non-familiar ones. To rule out this possibility, we performed two control analyses (see Methods: ‘Effect of the relative number of hits').…”

Ensembles of human MTL neurons “jump back in time” in response to a repeated stimulus

“…The unit isolation algorithms used here are consistent with many prior studies (Viskontas et al, 2009; Gelbard-Sagiv et al, 2008; Ekstrom et al, 2003; Viskontas et al, 2006). Nonetheless, the problem of sorting spikes from many individual neurons recorded on a single recording wire is a difficult one.…”

Decoding movie content from neuronal population activity in the human medial temporal lobe

“…Most participants had neither seen the movie before nor encountered the actors in other media prior to its presentation as part of this study. This interpretation aligns with previous research showing that neuronal selectivity to individuals varies with familiarity and personal relevance, as photos depicting personally known individuals are more likely to elicit selective responses in MTL neurons 37 .…”

Long-term coding of personal and universal associations underlying the memory web in the human brain

“…This is in agreement with the fact that MTL neurons do not represent visual features, as they show visual invariance (that is, they respond to completely different pictures of the same person)16 and their firing can be triggered by different sensory modalities (responding to the person's written and spoken name)17. Another potential confound is given by the familiarity of the images: since familiar pictures are represented by more neurons18, there is in principle a higher chance of finding neurons firing to pairs of familiar pictures compared with non-familiar ones. To rule out this possibility, we performed two control analyses (see Methods: ‘Effect of the relative number of hits').…”

Ensembles of human MTL neurons “jump back in time” in response to a repeated stimulus

“…The unit isolation algorithms used here are consistent with many prior studies (Viskontas et al, 2009; Gelbard-Sagiv et al, 2008; Ekstrom et al, 2003; Viskontas et al, 2006). Nonetheless, the problem of sorting spikes from many individual neurons recorded on a single recording wire is a difficult one.…”

Decoding movie content from neuronal population activity in the human medial temporal lobe

“…Most participants had neither seen the movie before nor encountered the actors in other media prior to its presentation as part of this study. This interpretation aligns with previous research showing that neuronal selectivity to individuals varies with familiarity and personal relevance, as photos depicting personally known individuals are more likely to elicit selective responses in MTL neurons 37 .…”

Long-term coding of personal and universal associations underlying the memory web in the human brain

“…This is in agreement with the fact that MTL neurons do not represent visual features, as they show visual invariance (that is, they respond to completely different pictures of the same person)16 and their firing can be triggered by different sensory modalities (responding to the person's written and spoken name)17. Another potential confound is given by the familiarity of the images: since familiar pictures are represented by more neurons18, there is in principle a higher chance of finding neurons firing to pairs of familiar pictures compared with non-familiar ones. To rule out this possibility, we performed two control analyses (see Methods: ‘Effect of the relative number of hits').…”

Ensembles of human MTL neurons “jump back in time” in response to a repeated stimulus

“…The unit isolation algorithms used here are consistent with many prior studies (Viskontas et al, 2009; Gelbard-Sagiv et al, 2008; Ekstrom et al, 2003; Viskontas et al, 2006). Nonetheless, the problem of sorting spikes from many individual neurons recorded on a single recording wire is a difficult one.…”