A temporal record of the past with a spectrum of time constants in the monkey entorhinal cortex

Abstract

Episodic memory is believed to be intimately related to our experience of the passage of time. Indeed, neurons in the hippocampus and other brain regions critical to episodic memory code for the passage of time at a range of time scales. The origin of this temporal signal, however, remains unclear. Here, we examined temporal responses in the entorhinal cortex of macaque monkeys as they viewed complex images. Many neurons in the entorhinal cortex were responsive to image onset, showing large deviations from baseline firing shortly after image onset but relaxing back to baseline at different rates. This range of relaxation rates allowed for the time since image onset to be decoded on the scale of seconds. Further, the ensemble carried information about image content suggesting that neurons in the entorhinal cortex carry information not only about when an event took place but also the identity of that event. Taken together, these findings suggest that the primate entorhinal cortex uses a spectrum of time constants to construct a temporal record of the past in support of episodic memory.Episodic memory, the vivid recollection of an event situated in a specific time and place 1 , depends critically on medial temporal lobe (MTL) structures, including the hippocampus and entorhinal cortex (EC) 2-5 . Building on pioneering work demonstrating a spatial code in the hippocampus and entorhinal cortex 6,7 , recent research has shown that hippocampal representations also carry information about the time at which past events took place, suggesting that the MTL maintains a representation of spatiotemporal context in support of episodic memory [8][9][10] . Although a great deal is known about the temporal coding properties of neurons in the hippocampus, the temporal code in the entorhinal cortex, which provides the majority of the cortical input to the hippocampus is less understood, but see [11][12][13][14] .Hippocampal time cells provide a record of recent events including explicit information about when an event occurred. Analogous to hippocampal place cells that fire when an animal is in a circumscribed region of physical space 6, 15 , hippocampal time cells fire during a circumscribed period of time within unfilled delays 8,9,16 . Across studies, there is a remarkable consistency in the properties of hippocampal time cells. Hippocampal time cells peak at a range of times during the delay interval and typically code time with decreasing accuracy as the delay unfolds, as manifest 1 by fewer neurons with peak firing late in the delay and wider time fields later in the delay 12,17,18 . Hippocampal time cells have been observed in a wide range of behavioral paradigms, including tasks with and without explicit memory demands during the delay 17 and experiments in which the animal is fixed in space 19,20 . In addition, it has been shown that different stimuli trigger different time cell sequences 19,20 . Taken together, time cells provide an explicit record of how far in the past an event took place, i.e., the amount of time that h...

Conjunctive representation of what and when in monkey hippocampus and lateral prefrontal cortex during an associative memory task

“…Similarly, there have been reports of firing rates that decay as a duration elapses (Blanchard, Strait, & Hayden, 2015; Kim et al, 2013; Sakon et al, 2014). In particular, decaying and ramping of an exponential form is described in Monkey EC in Bright et al (2020). Notably, a Gaussian receptive field is nested with the statistical model used by Bright et al (2020) and yet they did not identify any cells best described by a Gaussian receptive field, that is, they did not identify any time cells.…”

“…In particular, decaying and ramping of an exponential form is described in Monkey EC in Bright et al (2020). Notably, a Gaussian receptive field is nested with the statistical model used by Bright et al (2020) and yet they did not identify any cells best described by a Gaussian receptive field, that is, they did not identify any time cells. It is possible that differences in experimental paradigms can result in different temporal coding schemes taking precedent.…”

The Tolman-Eichenbaum Machine: Unifying Space and Relational Memory through Generalization in the Hippocampal Formation

“…Each stream can therefore learn a different smoothing kernel (leading to different temporal scales). (Note that a population of exponential kernels forms a Laplace Transform with real coefficients, as observed in LEC in rodents [Tahvildari et al, 2007;Tsao et al, 2018] and monkeys [Bright et al, 2020]). 2.…”

The genie in the bottle-magnified calcium signaling in dorsolateral prefrontal cortex

“…The analyses of rhesus monkey data revealed still longer timescales from neurons in the anterior cingulate cortex (ACC), which integrate affective and cognitive information [8], and in humans, can contribute to sustained mood states [9,10]. Finally, a recent analysis of monkey entorhinal cortex (ERC) revealed a range of timescales, including very long scales consistent with the ERC-hippocampal role in longer term memory consolidation [11].…”