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...

The functional profile of the human amygdala in affective processing: Insights from intracranial recordings

“…While complementary functions such as novelty/familiarity detection, arousal processing and memory should not be discounted, this study suggests that specific amygdala neurons may scan the environment for relevance amongst novel stimuli (Pedreira et al, 2010). While contemporary neuroscience literature supports amygdala relevance processing (Pessoa & Adolphs, 2010;Sander et al, 2003), intracranial data evidence a direct relation between amygdala neuronal activity and relevance processing, both implicitly (Br azdil et al, 2002;Viskontas, Quiroga, & Fried, 2009) and explicitly (Jenison, Rangel, Oya, Kawasaki, & Howard, 2011). Concretely, these iEEG data have delineated two broad types of amygdala relevance processing: (i) behavioral and (ii) motivational.…”

“…Interestingly, family and self were statistically equal to faces of celebrities and strangers. Authors concluded that the amygdala may be involved in processes related to salience/novelty and emotional significance (Viskontas et al, 2009). Together, these single-neuron studies implicate amygdala neurons in relevance processing in both valuation of preferred objects and in viewing faces of potentially self-relevant others (cf.…”

“…Unlike behavioral relevance, this may relate to stimuli/events affecting selfpromoting pursuits like goal-acquisition, self-affirmation, basic needs satisfaction, and overall survival. Two singleneuron studies have demonstrated amygdala involvement in processing motivational relevance (Jenison et al, 2011;Viskontas et al, 2009). Using a judgment preference task, Jenison et al (2011) illustrated the amygdala to be involved in either encoding or computing of the value of the respective stimulus during the time of choice (Jenison et al, 2011).…”

“…Motivational relevance processing was equally implied when identifying the faces of proxy caregivers. In a singleneuron study, patients identified individual faces differing in levels of familiarity and relevance (Viskontas et al, 2009). Stimuli included faces of self, family members, the experimenters, famous politicians and celebrities, and complete strangers as well as non-face control images such as landmarks.…”

“…More research replicating and elaborating upon the present study would be warranted in order to develop reliable conclusions on the amygdala's direct involvement in valuing of external stimuli. Next, Viskontas et al (2009) illustrated differential amygdala FR to faces of people differing in degrees of personal relevance. In their single-neuron study, the authors demonstrated that images of experimenters elicited greater amygdala FR than family and self.…”