Conscious Report Threshold for Visual Signals

 

Science  04 May 2018: Vol. 360, Issue 6388, pp. 537-542

The threshold for conscious report: Signal loss and response bias in visual and frontal cortex

Bram van Vugt, et.al.

Department of Vision and Cognition, Netherlands Institute for Neuroscience, Meibergdreef 47, 1105 BA Amsterdam, Netherlands.

Department of Neurobiology, Harvard Medical School, Boston, MA 02115, USA.

Neural Computation Laboratory, Istituto Italiano di Tecnologia, 38068 Rovereto, Italy.

Cognitive Neuroimaging Unit, Commissariat à l’Énergie Atomique et aux Énergies Alternatives, Direction des Sciences du Vivant/Institut d’Imagerie Biomédicale, INSERM, NeuroSpin Center, Université Paris-Sud and Université Paris-Saclay, 91191 Gif-sur-Yvette, France.

Collège de France, 75005 Paris, France.

Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Vrije Universiteit, Amsterdam, Netherlands.

Department of Psychiatry, Academic Medical Center, Amsterdam, Netherlands.

[paraphrase]

Why are some visual stimuli consciously detected, whereas others remain subliminal? We investigated the fate of weak visual stimuli in the visual and frontal cortex of awake monkeys trained to report stimulus presence. Reported stimuli were associated with strong sustained activity in the frontal cortex,    and frontal activity was weaker and quickly decayed for unreported stimuli. Information about weak stimuli could be lost at successive stages    en route from the visual to the frontal cortex, and these propagation failures were confirmed through microstimulation of area V1. Fluctuations in response bias and sensitivity during perception of identical stimuli were traced back to prestimulus brain-state markers. A model in which stimuli become consciously reportable when they elicit a nonlinear ignition process in higher cortical areas explained our results.

Understanding how conscious perception arises in the brain is a major challenge for neuroscience. Experimentally, one approach consists of comparing the neuronal activity evoked by identical weak stimuli, which are sometimes perceived and sometimes remain subliminal. Previous experiments have shown that subliminal stimuli    elicit considerable activity in many brain areas, including the prefrontal cortex, raising the question of why this activity is insufficient for conscious report.

The classical model that describes how weak stimuli are perceived or missed is signal detection theory (SDT). It posits that stimuli elicit a stochastic signal, which has to reach a threshold for perception. Stimuli that fail to reach the threshold are missed. In the absence of a stimulus, the signal usually stays below the threshold (correct rejection) but may cross the threshold on occasion, giving rise to a false alarm. According to SDT, a higher threshold decreases the number of false alarms but also increases the number of misses.

SDT does not specify the brain processes that determine the variability of the stimulus-induced signal nor the mechanism that determines the threshold. By contrast, global neuronal workspace theory (GNWT) proposes that stimuli reach awareness by propagating to the higher levels of the cerebral cortex, where they can lead to “ignition,” a nonlinear event that causes information about a brief stimulus to become sustained and broadcasted back through recurrent interactions between many brain areas. According to GNWT, there are two reasons why a stimulus may fail to become consciously accessible. First, the propagation of activity to higher levels may be too weak. Second, global ignition may fail—for example, if the system is refractory because another stimulus caused ignition or if attention is diverted. Combining insights from SDT and GNWT, we hypothesized that the SDT threshold might equal the amount of neural activity required for ignition. Furthermore, the stochasticity in signal strength might relate to variations in the propagation of activity from lower to higher cortical levels, possibly caused by fluctuations in prestimulus brain state.

We trained monkeys to detect low-contrast stimuli and recorded multiunit activity (MUA) in areas V1 and V4 of the visual cortex and in the dorsolateral prefrontal cortex (dlPFC) in order to examine the fate of identical subliminal and supraliminal stimuli. We asked the following questions: (i) Where in the visual hierarchy do subliminal signals get lost? (ii) Which neuronal mechanisms underlie the threshold for reporting a stimulus? (iii) What are the internal sources of fluctuations that allow a fixed stimulus to either cross or fail to cross the threshold?

The monkeys directed their gaze to a fixation point, and on half of the trials, we presented a 2° low-contrast circle as stimulus in the neurons’ receptive field (RF) for 50 ms. After a delay of 450 ms, introduced to prevent reflexive eye movements, the monkey reported the stimulus by making a saccade to its previous location. In the absence of a stimulus, the monkey made a saccade to another, smaller gray circle (the reject dot). Accuracy on such stimulus-absent trials was high (~5 to 10% of false alarms). We adjusted the contrast on stimulus-present trials close to the threshold of perception, at an accuracy of ~80%. The contrast threshold (θ_High; accuracy of 80%) varied with stimulus eccentricity between 2.5 and 7%. To examine perception of very weak stimuli, we also defined a second threshold, θ_Low, associated with an accuracy of 40% and categorized stimulus strength into three categories: easy (contrast > θ_High), intermediate (θ_Low < contrast < θ_High), and difficult (contrast < θ_Low). We normalized the neuronal responses to the activity elicited by a high-contrast stimulus.

Stimuli with higher contrasts elicited more activity than did stimuli with lower contrasts (time window 0 to 300 ms after stimulus onset, t tests, all P < 10⁻³). During misses information is lost during the propagation of visual information to higher cortical areas. In the dlPFC and, to a lesser extent, areas V4 and V1, the extra neuronal activity for hits was maintained until the saccade (time window 300 to 500 ms, all areas and categories P < 0.05). We interpreted our results in terms of variation in signal propagation from area V1 to V4 and then onward to the PFC, but visual information can reach higher areas through multiple routes, some of which bypass area V1.

We created a model architecture based on previous modeling studies, which contained the lateral geniculate nucleus and four hierarchically arranged cortical areas. We represented the population of neurons in each area with a single, stochastic process so that only five variables described the evolution of the network state during simulated trials, one for each brain region. The model contained feedforward connections,    self-connections within the areas,    and feedback connections. The reciprocal connections between the parietal and frontal cortex were relatively strong so that activity exceeding a threshold in these areas became self-sustained. The model produced a realistic psychometric function, with increased accuracy for higher contrasts.

Overall, our results provide new insights into why a fixed stimulus sometimes leads to a conscious report and sometimes remains subliminal and inspire unification of SDT and GNWT. Both data and model support the concept of multiple bottlenecks for conscious access: Weak stimuli tend to get lost at early processing levels, whereas stronger stimuli may transiently activate frontal cortex but still fail to reach the threshold for reportability. For conscious detection to occur in the model, stimuli must elicit a threshold level of prefrontal activity that is sufficient for ignition; stimuli that fail to reach this level are missed.    Ignition corresponds to a self-sustained pattern of neuronal activity at the higher processing levels.    Because of the variability of neuronal activity, the ignition threshold is occasionally reached on stimulus-absent trials, so that a false alarm occurs. The model proposes that ignition is caused by strong reciprocal interactions between the parietal and frontal cortex, in accordance with studies demonstrating that anesthesia weakens these interactions.

[end of paraphrase]

 

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