S4 – Ongoing fluctuation of neural activity and its relationship to visual perception

Friday, May 6, 2:30 – 4:30 pm, Royal Ballroom 1-3

Organizer: Hakwan Lau, Columbia University, Donders Institute, Netherlands

Presenters: Biyu Jade He, National Institute of Health; Charles Schroeder, Nathan S. Kline Institute for Psychiatric Research, Columbia University; Andreas Kleinschmidt, INSERM-CEA, NeuroSpin, Gif/Yvette, France; Hakwan Lau, Columbia University, Donders Institute, Netherlands; Tony Ro, City University of New York

Symposium Description

Even in the absence of external stimulation, the visual system shows ongoing fluctuations of neural activity. While some early theoretical analyses suggest that the impact of such fluctuations in activity on visual perception may be minimal, recent empirical results have given new insights on this issue. We will review this evidence and the new theoretical perspectives in this symposium. Below are a few key themes:

– Coverage of multiple experimental methods and fluctuations in activity at different time scales:

The 5 speakers will discuss experiments that employ different methods to measure ongoing fluctuations in neural activity, such as human fMRI (functional magnetic resonance imaging) in patients and healthy subjects, intracranial cortical EEG (electroencephalography) in presurgical epileptics, combined use of TMS (transcranial magnetic stimulation) and optical imaging, and electrophysiological studies in non-human primates. These methods investigate fluctuations in neural activity at different time scales, from 10-20 seconds per cycle to the sub-second oscillatory range. The relationship between these different activities will be discussed.

– What ongoing activities tell us about the mechanisms of attention?

In addition to discussing the nature of ongoing activity and its impact on perception, several speakers will also use ongoing activity as a tool to understand the basic mechanisms of attention and awareness.

– Implication for clinical studies of perception:

Several speakers will discuss data collected from presurgical epileptics, where intracranial cortical EEG data were recorded. The nature of ongoing fMRI activity in patients suffering from strokes will also be discussed.

– Debate of theoretical perspectives and interpretations of data:

The different speakers will present competing theoretical perspectives on the nature of ongoing activity, as well as alternative interpretations of the same results. This will promote an exchange of ideas and hopefully lead to consensus on and illumination of the issues.

The nature of ongoing neural activity and its relationship to perception should be relevant to all attendants of VSS. We aim to have a broad audience, as we will be covering different experimental paradigms with different empirical methods. We expect the symposium to be especially interesting for researchers specializing in attention and awareness. Also, although the topic is primarily on neural activity, one focus of the symposium is its relationship to behavior. Hence some speakers will also present behavioral studies inspired by the investigation of ongoing neural activity, which will be of interests to many. Specifically, in some talks the implications of our understanding of ongoing neural activity and issues of experimental design will be discussed.

Presentations

Spontaneous fMRI signals and slow cortical potentials in perception

Biyu Jade He, National Institute of Health

The brain is not a silent, complex input/output system waiting to be driven by external stimuli; instead, it is a closed, self-referential system operating on its own with sensory information modulating rather than determining its activity. Ongoing spontaneous brain activity costs the majority of the brain’s energy budget, maintains the brain’s functional architecture, and makes predictions about the environment and the future. I will discuss some recent research on the functional significance and the organization of spontaneous brain activity, with implications for perception research. The past decade has seen rapid development in the field of resting-state fMRI networks. In one of the first studies that established the functional significance of these networks, we showed that strokes disrupted large-scale networks in the spontaneous fMRI signals, and that the degree of such disruption predicted the patients’ behavioral impairment (spatial neglect). Next, we identified the neurophysiological signal underlying the coherent patterns in the spontaneous fMRI signal, the slow cortical potential (SCP). The SCP is a novel neural correlate of the fMRI signal; existing evidence suggests that it most likely underlies both spontaneous fMRI signals and task-evoked fMRI responses. I further discuss some existing data suggesting a potential involvement of the SCP in conscious awareness, including the influence of spontaneous SCP fluctuations on visual perception. Lastly, given that both the SCP and the fMRI signal display a power-law distribution in their temporal power spectra, I argue that the role of scale-free brain activity in perception and consciousness warrants future investigation.

Tuning of the neocortex to the temporal dynamics of attended event streams

Charles Schroeder, Nathan S. Kline Institute for Psychiatric Research, Columbia University

When events occur in rhythmic streams, attention may use the entrainment of neocortical excitability fluctuations (oscillations) to the tempo of a task-relevant stream, to promote its perceptual selection, and its representation in working memory. To test this idea, we studied humans and monkeys using an auditory-visual stream selection paradigm. Electrocortical (ECoG) activity sampled from subdural electrodes in epilepsy patients showed that: 1) attentional modulation of oscillatory entrainment operates in a network of areas including auditory, visual, posterior parietal, inferior motor, inferior frontal, cingulate and superior midline frontal cortex, 2) strength of oscillatory entrainment depends on the predictability of the stimulus stream, and 3) these effects are dissociable from attentional enhancement of evoked activity. Fine-grained intracortical analysis of laminar current source density profiles and concomitant neuronal firing patterns in monkeys showed that: 1) along with responses “driven” by preferred modality stimuli (e.g., visual stimuli in V1), attended non-preferred modality stimuli (e.g., auditory stimuli in V1) could “modulate” local cortical excitability by entraining ongoing oscillatory activity, 2) while this “heteromodal” entrainment occurred in the extragranular layers, the granular layers remain phase-locked to the stimulus stream in the preferred modality. Thus, attention may use phase modulation (coherence vs opposition) to control the projection of information from input to output layers of cortex. On a regional scale, oscillatory entrainment across a network of brain regions to may provide a mechanism for a sustained and distributed neural representation of attended event patterns, and for their availability to working memory.

Probing Perceptual Consequences of Ongoing Activity Variations

Andreas Kleinschmidt, INSERM-CEA, NeuroSpin, Gif/Yvette, France

Recordings of ongoing brain activity show remarkable spontaneous fluctuations such that detecting stimulus-driven responses usually requires multiple repetitions and averaging. We have assessed the functional impact of such fluctuations on evoked neural responses and human perceptual performance. We studied human participants using functional neuroimaging and sparse event-related paradigms with sensory probes that could be either ambiguous with respect to perceptual categories (faces) or peri-liminal for a given feature (visual motion coherence). In both instances, fluctuations in ongoing signal of accordingly specialized brain regions (FFA, hMT+) biased how upcoming stimuli were perceived. Moreover, the relation between evoked and ongoing activity was not simply additive, as previously described in other settings, but showed an interaction with perceptual outcome. This latter observation questions the logic of event-related averaging where responses are thought to be unrelated from the level of pre-stimulus activity. We have further analyzed the functional connotation of the imaging signal by analyzing false alarm trials. Counter the notion of this signal being a proxy of sensory evidence, false alarms were preceded by especially low signal. A theoretical framework that is compatible with our observations comes from the family of predictive coding models, the ‘free energy’ principle proposed by Karl Friston. Together, our findings illustrate the functional consequences of ongoing activity fluctuations and underline that they should not be left unaccounted for as in the traditional mainstream of data analysis.

The paradoxical negative relationship between attention-related spontaneous neural activity and perceptual decisions

Hakwan Lau, Columbia University, Donders Institute, Netherlands; Dobromir Rahnev, Columbia University

One recent study reported that when ongoing pre-stimulus fMRI activity in the dorsal attention network was high, the hit rate in an auditory detection task was surprisingly low. This result is puzzling because pre-stimulus activity in the dorsal attention network presumably reflects the subjects’ attentional state, and high attention is supposed to improve perception, not impair it. However, it is important to distinguish between the capacity and decision/criterion aspects of perception. Using signal detection theoretic analysis, we provide empirical evidence to show that spatial attention can lead to conservation bias in detection, although it boosts detection capacity. In behavioral experiments we confirmed the prediction, derived from signal detection theory, that this conservative bias in detection is coupled with lowered confidence ratings in a discrimination task. Based on these results, we then used fMRI to test the hypothesis that low pre-stimulus ongoing activity in the dorsal attention network predicts high confidence rating in a visual motion discrimination task. We confirmed this counter-intuitive hypothesis, and also found that functional connectivity (i.e. correlation) between areas within the dorsal attention network negatively predicts confidence rating.

Taken together, these results support the notion that attention may have a negative impact on the decision/criterion aspects of perception. This negative relationship may explain why under the lack of attention, we may have an inflated sense of subjective experience: e.g. the vividness of peripheral vision; and the overconfidence in naïve subjects in inattentional blindness and change blindness experiments despite their poor performance capacity.

Oscillatory and Feedback Activity Mediate Conscious Visual Perception

Tony Ro, City University of New York

Under identical physical stimulus conditions, sometimes visual events are detected whereas at other times these same visual events can go unnoticed. Using both metacontrast masking and transcranial magnetic stimulation (TMS) of the primary visual cortex to induce visual suppression, we have been examining the neural mechanisms underlying this variability in perception. Our results indicate that the timing of arrival of visual events in primary visual cortex with respect to ongoing oscillatory activity and feedback signals play an important role in dictating whether a visual event is detected or not. Furthermore, experiments manipulating visual stimulus salience suggest that the strength of only feedforward signals, but not feedback signals in primary visual cortex is affected by manipulations of saliency. Taken together, our studies shed some insight into the nature and variability of the neural signals that support conscious visual perception.