Persistently active neurons in human medial frontal and medial temporal lobe support working memory

Kamiński J, Sullivan S, Chung JM, Ross IB, Mamelak AN, Rutishauser U                              Publication      Press release

 

Nature Neuroscience (2017)

 

Persistent neural activity is a putative mechanism for the maintenance of working memories. Persistent activity relies on the activity of a distributed network of areas, but the differential contribution of each area remains unclear. We recorded single neurons in the human medial frontal cortex and medial temporal lobe while subjects held up to three items in memory. We found persistently active neurons in both areas. Persistent activity of hippocampal and amygdala neurons was stimulus-specific, formed stable attractors and was predictive of memory content. Medial frontal cortex persistent activity, on the other hand, was modulated by memory load and task set but was not stimulus-specific. Trial-by-trial variability in persistent activity in both areas was related to memory strength, because it predicted the speed and accuracy by which stimuli were remembered. This work reveals, in humans, direct evidence for a distributed network of persistently active neurons supporting working memory maintenance.

Concept cells are persistently active during WM maintenance.  Example concept cell recorded from amygdala. Top: PSTH (bin size, 200 ms; step size, 2 ms). Shaded areas represent ± s.e.m. across trials. Insets: mean extracellular waveform ± s.e.m. of all spikes associated with that cell. Middle: periods of significance (black) between preferred vs. nonpreferred stimuli (corrected for multiple comparisons using a cluster-size correction; Online Methods). Bottom: raster plot of trials reordered according to condition for plotting purposes only. Both neurons show both visually evoked selective activity (red) and sustained activity (blue) during maintenance. Note that during maintenance, concept cells have elevated activity only when their preferred stimulus was held in memory (blue vs. gray), and that the sustained activity (blue) was suppressed during encoding of the nonpreferred image (i.e., encoding 3) when the preferred stimulus was already held in memory.
Persistent activity during maintenance forms attractors.​​
Illustration of the mean trajectories in neuronal state space formed by the three demixed principal components (dPCs) associated with picture identity during encoding (thin line) and maintenance (thick line). The transition from thin to thick lines indicates the onset of the maintenance period. Points of time are indicated in the upper left corner. Colors mark different images

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