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

Abstract

Episodic memory, which depends critically on the integrity of the medial temporal lobe (MTL), has been described as “mental time travel” in which the rememberer “jumps back in time.” The neural mechanism underlying this ability remains elusive. Mathematical and computational models of performance in episodic memory tasks provide a specific hypothesis regarding the computation that supports such a jump back in time. The models suggest that a representation of temporal context, a representation that changes gradually over macroscopic periods of time, is the cue for episodic recall. According to these models, a jump back in time corresponds to a stimulus recovering a prior state of temporal context. In vivo single-neuron recordings were taken from the human MTL while epilepsy patients distinguished novel from repeated images in a continuous recognition memory task. The firing pattern of the ensemble of MTL neurons showed robust temporal autocorrelation over macroscopic periods of time during performance of the memory task. The gradually-changing part of the ensemble state was causally affected by the visual stimulus being presented. Critically, repetition of a stimulus caused the ensemble to elicit a pattern of activity that resembled the pattern of activity present before the initial presentation of the stimulus. These findings confirm a direct prediction of this class of temporal context models and may be a signature of the mechanism that underlies the experience of episodic memory as mental time travel.

Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval

“…By comparing reinstatement during correct and incorrect retrieval, our findings build upon recent evidence that trial-specific reinstatement of this neural representation of temporal context occurs during successful retrieval (20,21). If successful retrieval is associated with the recovery of a temporal context representation, then we would expect to find a graded decrease in reinstatement as retrieval periods were paired with encoding periods separated by longer time intervals in both the forward and backward direction (6,8,21). Consistent with this prediction, our data demonstrate a contiguity effect for correct trials within lists.…”

“…However, because retrieval in this study was unconstrained, one possibility is that the observed reinstatement was a consequence, rather than a cause, of retrieval contiguity. Spiking activity in the medial temporal lobe has also been shown to reinstate activity present during encoding (21,22). However, it is unknown how the temporal dynamics of neural activity distinguish reinstatement between correct and incorrect memory retrieval across broader cortical regions.…”

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

“…Memory formation is crucial for learning from novel relevant experiences (Rutishauser, Ross, Mamelak, & Schuman, 2010), and iEEG evidence has reliably illustrated the importance of amygdala neuronal activity in encoding, recognition and recall accuracy of objects and events ( c o r t e x 6 0 ( 2 0 1 4 ) 1 0 e3 3 Heit, Smith, & Halgren, 1988;Howard, Viskontas, Shankar, & Fried, 2012;Kreiman, Koch, & Fried, 2000b;Paz et al, 2010;Quian Quiroga, Kraskov, Koch, & Fried, 2009;Quiroga, Mukamel, Isham, Malach, & Fried, 2008, Quiroga, Reddy, Kreiman, Koch, & Fried, 2005Rutishauser et al, 2010). Importantly, this occurs independently of sensory modality (Quian Quiroga et al, 2009).…”

“…For instance, categories (e.g., animals) and specific objects (e.g., individuals) are shown to yield selective amygdala neuronal FR at encoding and recognition irrespective of presentation context and angular configurations (Gelbard-Sagiv et al, 2008;Kreiman, Fried, & Koch, 2002;Mormann et al, 2011;Quian Quiroga et al, 2009;Quiroga et al, 2005). Consequently, the amygdala may be removed from encoding contextual aspects relevant to the experienced stimulus, including temporal relationships of events and objects (Howard et al, 2012;Paz et al, 2010), spatial location of the respective stimulus (Rutishauser, Mamelak, & Schuman, 2006, Rutishauser, Schuman, & Mamelak, 2008, and even affectively neutral associative relationships (Cameron et al, 2001). Single-neuron studies by Howard et al (2012) and Paz et al (2010) both failed to show significant amygdala neural responding that would be indicative of temporal order processing of experienced events.…”

“…Consequently, the amygdala may be removed from encoding contextual aspects relevant to the experienced stimulus, including temporal relationships of events and objects (Howard et al, 2012;Paz et al, 2010), spatial location of the respective stimulus (Rutishauser, Mamelak, & Schuman, 2006, Rutishauser, Schuman, & Mamelak, 2008, and even affectively neutral associative relationships (Cameron et al, 2001). Single-neuron studies by Howard et al (2012) and Paz et al (2010) both failed to show significant amygdala neural responding that would be indicative of temporal order processing of experienced events. Furthermore, Rutishauser, Mamelak, et al (2006) and Rutishauser et al (2008) observed amygdala neurons to discriminate familiar vs. novel stimuli with negligible amygdala neuron spiking activity when recalling the spatial location of the preferred stimulus 24 h post-stimulus presentation.…”