Inferior temporal cortex leads prefrontal cortex in response to a violation of a learned sequence

Abstract

Primates learn statistical regularities that are embedded in visual sequences, a form of statistical learning. Single-unit recordings in macaques showed that inferior temporal (IT) neurons are sensitive to statistical regularities in visual sequences. Here, we asked whether ventrolateral prefrontal cortex (VLPFC), which is connected to IT, is also sensitive to the transition probabilities in visual sequences and whether the statistical learning signal in IT originates in VLPFC. We recorded simultaneously multiunit activity (MUA) and local field potentials (LFPs) in IT and VLPFC after monkeys were exposed to triplets of images with a fixed presentation order. In both areas, the MUA was stronger to images that violated the learned sequence (deviants) compared to the same images presented in the learned triplets. The high-gamma and beta LFP power showed an enhanced and suppressed response, respectively, to the deviants in both areas. The enhanced response was present also for the image following the deviant, suggesting a sensitivity for temporal adjacent dependencies in IT and VLPFC. The increased response to the deviant occurred later in VLPFC than in IT, suggesting that the deviant response in IT was not inherited from VLPFC. These data support predictive coding theories that propose a feedforward flow of prediction errors.

Location-specific deviant responses to object sequences in macaque inferior temporal cortex

“…After this exposure phase, lasting several weeks, we recorded in IT, assessing whether the response to S2 differed between the exposed (Fixed) and new, Deviant sequences in which the image identity of S1 of a pair differed from the one during the exposure. In agreement with previous studies from different groups 5 – 7 , 11 , 12 , we observed an enhanced response to Deviant compared to Fixed sequences in which both S1 and S2 were presented foveally during the exposure phase. However, no such across-monkey consistent deviant responses were observed for sequences in which S1 was presented peripherally during the exposure phase.…”

“…Recently, we showed that the deviant response occurs later in the frontal cortex than in IT 12 , which is in line with a feedforward flow of prediction errors resulting from the mismatch between the predicted and presented stimulus in the deviant sequences. The present data show no evidence for a later onset of the deviant response in AIT compared to PIT, although the onset latencies for the S1 stimuli were shorter in PIT than in AIT.…”

“…Since statistical learning can be reflected in the pupil response of monkeys 12 , 32 , we examined whether the mean pupil size differed between the Fixed and Deviant sequences for each of the 3 location conditions (Figure S3). In M1, mean pupil size was smaller for the Deviant S2 than for the Fixed S2 stimuli for the foveal S1 conditions (Wilcoxon signed-rank test; p = 0.039; uncorrected for multiple comparisons), which is in line with the pupil constriction observed before for Deviant stimuli of other learned sequences in this monkey 12 . However, this pupil size difference was no longer significant ( p = 0.116) when correcting for multiple comparisons (three locations; FDR correction).…”

“…Typically, exposure to a set of fixed sequences of visual images produces a smaller neural response to an image in its learned sequence compared to the response to that image when positioned in another sequence. This has been observed in the macaque inferior temporal (IT) cortex 5 – 12 , and frontal cortex 12 . A higher fMRI activation to stimuli that violated learned sequences, “deviants”, is also seen in various human brain regions, ranging from the early visual cortex 13 – 15 , over occipito-temporal cortex 14 , 16 to regions outside the visual cortex such as the frontal cortex 14 , 15 , 17 , 18 .…”

“…The origin of the deviant response in IT is still unclear. One possibility we recently tested is whether it reflects feedback from the prefrontal cortex that detects the violation of the learned sequence 12 . However, the deviant response onset was not earlier in the frontal cortex compared to IT, refuting this possibility.…”