Prior expectations evoke stimulus-specific activity in the deep layers of the primary visual cortex

Abstract

The way we perceive the world is strongly influenced by our expectations. In line with this, much recent research has revealed that prior expectations strongly modulate sensory processing. However, the neural circuitry through which the brain integrates external sensory inputs with internal expectation signals remains unknown. In order to understand the computational architecture of the cortex, we need to investigate the way these signals flow through the cortical layers. This is crucial because the different cortical layers have distinct intra- and interregional connectivity patterns, and therefore determining which layers are involved in a cortical computation can inform us on the sources and targets of these signals. Here, we used ultra-high field (7T) functional magnetic resonance imaging (fMRI) to reveal that prior expectations evoke stimulus-specific activity selectively in the deep layers of the primary visual cortex (V1). These findings are in line with predictive processing theories proposing that neurons in the deep cortical layers represent perceptual hypotheses and thereby shed light on the computational architecture of cortex.

Predictive coding during action observation - a depth-resolved intersubject functional correlation study at 7T

“…Importantly, for the first time we resolved the depth-profile of such sequence-level information. In accordance with predictive coding and the notion that predictive top-down information should be strongest in deeper layers (Kok et al 2016; de Lange et al 2018; Aitken et al 2020), we found the significant difference with ISC intact > ISC scrambled to be observed in the deeper half of PFt, peaking at a depth that aligns with layer V in postmortem histological examinations of the brains of other individual(Caspers et al 2006). In line with anatomical tracing studies in monkeys, suggesting that feedback connections from BA44 to PFt should terminate in layer III in addition to layers V/VI, this increased ISC was significant also at depth compatible with the location of layer III.…”

“…Because this increased ISFC is calculated across different subjects, it indicates that it is signal relating to the intactness of the sequence in the stimuli that synchronizes across BA44 and PFt (Simony et al 2016; Nastase et al 2019). The depth of this channel of increased ISFC dovetails remarkably well with recent observations that predictive processes in other domains of visual processing are accompanied by an increased recruitment of the deeper layers of the cortical visual system (Kok et al 2016; de Lange et al 2018; Aitken et al 2020), and with anatomical consideration that the dominant origin of feedback originates from deep layers in higher cortical region(Shipp 2007).…”

“…After we found evidence for differential ISC values for Intact and Scrambled movies at different cortical depth within PFt, we probed the interaction between PFt and either BA44 or latOCC in the two conditions. We hypothesized that during the observation of Intact movies, brain activity would be more enhanced in the feed-back stream from BA44 to PFt, terminating at depth aligning with layers V/VI and III (Gerbella et al 2011), with the deep-layers particularly associated with predictive brain activity (Shipp 2007; Kok et al 2016; de Lange et al 2018; Aitken et al 2020). In contrast, for the information transfer across latOCC and PFt, because the latOCC appears to represent information at the short temporal scale of acts, too fast for the the Nyquist limit of our acquisition, we do not expect measurable changes in ISFC.…”

“…Pioneering studies in the early visual cortex have shown that acquiring fMRI at submillimeter resolution at high-field strength (≥7T) can indeed test predictive coding hypotheses (Kok et al 2016; Lawrence et al 2018, 2019a, b; Finn et al 2020; Aitken et al 2020). Recent work in particular confirms that activations in deep layers is indeed measurable when feedback predictions about upcoming sensory events are likely to occur in the visual system (Kok et al 2016; de Lange et al 2018; Aitken et al 2020), while activation in superficial layers seem to be measured when there is a mismatch between predicted and observed input and attentional signals (de Lange et al 2018). Unfortunately, experiments testing whether deep layers carry signals that could be related to predictions have so far been restricted to early visual cortices and we do not know whether the same might be observed in parietal and premotor regions (Finn et al 2020).…”

Statistical learning of frequent distractor locations in visual search involves regional signal suppression in early visual cortex

“…The behavioural signature of statistical distractor-location learning has been well documented recently: RT interference is reduced for distractors occurring at frequent versus rare locations, and this is associated with reduced capture of the first saccade by distractors at frequent locations (Di Caro et al 2019;Wang et al 2019a;Sauter et al 2020). Together with an ERP component interpreted in terms of distractor suppression (Wang et al 2019b), this has been taken as evidence that observers learn to down-modulate the attentional priority signals (Itti and Koch 2001;Fecteau and Munoz 2006;Wolfe and Gray 2007;Kok et al 2012;Aitken et al 2020) generated by distractors at frequent locations, thus reducing their potential to capture attention and cause interference. In line with this, we found that early visual-cortex signalling was reduced for distractors occurring in the frequent versus rare region.…”