Attentional Filtering of Visual Information by Neuronal Ensembles in the Primate Lateral Prefrontal Cortex

Abstract

The activity of neurons in the primate lateral prefrontal cortex (LPFC) is strongly modulated by visual attention. Such a modulation has mostly been documented by averaging the activity of independently recorded neurons over repeated experimental trials. However, in realistic settings, ensembles of simultaneously active LPFC neurons must generate attentional signals on a single-trial basis, despite the individual and correlated variability of neuronal responses. Whether, under these circumstances, the LPFC can reliably generate attentional signals is unclear. Here, we show that the simultaneous activity of neuronal ensembles in the primate LPFC can be reliably decoded to predict the allocation of attention on a single-trial basis. Decoding was sensitive to the noise correlation structure of the ensembles. Additionally, it was resilient to distractors, predictive of behavior, and stable over weeks. Thus, LPFC neuronal ensemble activity can reliably encode attention within behavioral time frames, despite the noisy and correlated nature of neuronal activity.

Correlated variability modifies working memory fidelity in primate prefrontal neuronal ensembles

“…Reports of the effects of ensemble r sc structure on information content vary significantly in sign and magnitude (19,22,24,27,42,48,49); our results can help reconcile these disparate accounts. For example, previous studies that applied decoding techniques to simultaneously recorded ensembles found that removing the r sc structure decreased decoding accuracy for grating orientation (48) and remembered location (49) whereas another study reported a positive effect of pairwise r sc on information coding (32).…”

“…We collected spike data from a total of 545 single units and multiunits across 12 recording sessions, out of which 417 (76%) exhibited sustained activity and selectivity during the delay epoch (P < 0.05, Kruskal-Wallis; firing rate × location) (Materials and Methods). We included both multiunits and single units in our analyses, as in similar previous studies (21,25,27,34). A unit's preferred location during a given epoch was defined as the location that elicited the largest response averaged over that epoch ( Fig.…”

“…For example, previous studies that applied decoding techniques to simultaneously recorded ensembles found that removing the r sc structure decreased decoding accuracy for grating orientation (48) and remembered location (49) whereas another study reported a positive effect of pairwise r sc on information coding (32). Moreover, spatial attention increases signal-to-noise primarily by reducing r sc (25)(26)(27). We found that the effect of r sc structure on ensemble information varied dramatically depending on an ensemble's size and composition; removing the r sc structure from the full recorded ensembles increased decoding accuracy, but removing the r sc structure from the most informative subensembles decreased decoding accuracy.…”

“…These results are difficult to extend to WM coding in the LPFC. Furthermore, there are relatively few studies investigating r sc in the LPFC (21,27,(29)(30)(31)(32)(33); and only one of these studies directly examined the effects of r sc on information coding (27). Prior results examining pairwise correlations are also difficult to extrapolate to larger neuronal ensembles, which have a complex, multidimensional r sc structure that cannot be characterized by pairwise measurements alone (20).…”

“…For example, spatial attention improves neural coding in the visual cortex primarily by reducing r sc (25)(26)(27)). Another study reported that increased r sc improved perceptual discrimination in macaque area S2 (28).…”