Encoding of Predictable and Unpredictable Stimuli by Inferior Temporal Cortical Neurons

Abstract

Animals and humans learn statistical regularities that are embedded in sequences of stimuli. The neural mechanisms of such statistical learning are still poorly understood. Previous work in macaque inferior temporal (IT) cortex demonstrated suppressed spiking activity to visual images of a sequence in which the stimulus order was defined by transitional probabilities (labeled as "standard" sequence), compared with a sequence in which the stimulus order was random ("random" sequence). Here, we asked whether IT neurons encode the images of the standard sequence more accurately compared with images of the random sequence. Previous human fMRI studies in different sensory modalities also found a suppressed response to expected relative to unexpected stimuli but obtained various results regarding the effect of expectation on encoding, with one study reporting an improved classification accuracy of expected stimuli despite the reduced activation level. We employed a linear classifier to decode image identity from the spiking responses of the recorded IT neurons. We found a greater decoding accuracy for images of the standard compared with the random sequence during the early part of the stimulus presentation, but further analyses suggested that this reflected the sustained, stimulus-selective activity from the previous stimulus of the sequence, which is typical for IT neurons. However, the peak decoding accuracy was lower for the standard compared with the random sequence, in line with the reduced response to the former compared with the latter images. These data suggest that macaque IT neurons represent less accurately predictable compared with unpredictable images.

Face Repetition Probability Does Not Affect Repetition Suppression in Macaque Inferotemporal Cortex

“…factors such as attention (Larsson and Smith, 2012) and stimulus category (Kovács et al, 2013;. The present study demonstrates that repetition suppression of spiking activity and LFP power is not modulated by repetition probability in macaque IT even when the subject is attending the stimuli, faces are used, and the repetition probability modulates behavior.…”

“…This task requires the monkey to attend the stimulus content, but is unrelated to face repetitions or alternations. In the initial 58 recording sessions, we used a block length of 40 trials following previous studies (Kaliukhovich and Vogels, 2011; Kovács et al, 2013), which is twice the 20 trials used by Summerfield et al (2008). Later, we increased the number of trials to 120, reasoning that longer blocks provide more information about the repetition probabilities and thus may increase expectation-related effects.…”

“…First, the repetition probability effect is absent when attention is not directed to the stimuli (Larsson and Smith, 2012). Second, repetition probability effects appear to be specific for particular stimulus categories such as faces (Kovács et al, 2013) or letters , not being present in the same subjects for objects but see Mayrhauser et al, 2014) and false fonts . Both constraints could potentially explain the absence of an effect of repetition probability in the single-unit study of Kaliukhovich and Vogels (2011): the monkeys were passively fixating and perhaps paying little to no attention to the stimulus content and unfamiliar fractal patterns or object images were used instead of faces.…”

“…However, it has also been suggested that repetition suppression results from a reduction of responses that encode a prediction error through a mechanism involving top-down influences of perceptual expectation (Friston, 2005;Summerfield et al, 2008). In support of this expectation-based hypothesis, multiple fMRI studies in humans reported stronger repetition suppression in blocks of trials in which a repetition is more frequent compared with those in which a repetition is infrequent and presumably unexpected (Summerfield et al, 2008;Kovács et al, 2012Kovács et al, , 2013Larsson and Smith, 2012;Andics et al, 2013;Mayrhauser et al, 2014;Ewbank et al, 2016). These repetition probability effects were originally reported using faces in the fusiform face area (FFA) (Summerfield et al, 2008) and later in other face selective regions such as the occipital face area (Kovács et al, 2012;Larsson and Smith, 2012;Ewbank et al, 2016) and non face selective regions such as the lateral occipital complex (Kovács et al, 2012;Larsson and Smith, 2012;.…”

Evaluating the neurophysiological evidence for predictive processing as a model of perception

“…4 for a recent review). Although some studies have reported that expected stimulus representations are dampened, 69,79,90,92,105,[109][110][111] others have found that this global suppression is attributable to the suppression of neurons tuned away from the expected stimulus feature, while the representation of the expected stimulus is actually sharpened c . 78,88,112 Interestingly, Marques et al 113 recently found that while backward inputs from rodent lateromedial visual area (LM) to V1 c When interpreting these results, it should be noted that these decoding analyses of global BOLD activity or singleunit responses did not segregate activity from the proposed error unit and expectation unit populations.…”