Limits...
The relation of ongoing brain activity, evoked neural responses, and cognition.

Sadaghiani S, Hesselmann G, Friston KJ, Kleinschmidt A - Front Syst Neurosci (2010)

Bottom Line: Ongoing brain activity has been observed since the earliest neurophysiological recordings and is found over a wide range of temporal and spatial scales.We then highlight the flexibility and context-sensitivity of intrinsic functional connectivity that suggest its involvement in functionally relevant information processing.This role in information processing is pursued by reviewing how ongoing brain activity interacts with afferent and efferent information exchange of the brain with its environment.

View Article: PubMed Central - PubMed

Affiliation: Institut National de la Santé et de la Recherche Médicale Unité 992 Cognitive Neuroimaging Unit Gif-sur-Yvette, France.

ABSTRACT
Ongoing brain activity has been observed since the earliest neurophysiological recordings and is found over a wide range of temporal and spatial scales. It is characterized by remarkably large spontaneous modulations. Here, we review evidence for the functional role of these ongoing activity fluctuations and argue that they constitute an essential property of the neural architecture underlying cognition. The role of spontaneous activity fluctuations is probably best understood when considering both their spatiotemporal structure and their functional impact on cognition. We first briefly argue against a "segregationist" view on ongoing activity, both in time and space, which would selectively associate certain frequency bands or levels of spatial organization with specific functional roles. Instead, we emphasize the functional importance of the full range, from differentiation to integration, of intrinsic activity within a hierarchical spatiotemporal structure. We then highlight the flexibility and context-sensitivity of intrinsic functional connectivity that suggest its involvement in functionally relevant information processing. This role in information processing is pursued by reviewing how ongoing brain activity interacts with afferent and efferent information exchange of the brain with its environment. We focus on the relationship between the variability of ongoing and evoked brain activity, and review recent reports that tie ongoing brain activity fluctuations to variability in human perception and behavior. Finally, these observations are discussed within the framework of the free-energy principle which - applied to human brain function - provides a theoretical account for a non-random, coordinated interaction of ongoing and evoked activity in perception and behavior.

No MeSH data available.


Related in: MedlinePlus

Local spontaneous variations in ongoing activity of specialized sensory regions impact perception. The upper part illustrates the paradigm: (A) auditory detection experiment: in a free-response setting subjects detected an auditory target stimulus presented at perceptual threshold. (B) Perceptual decision on an ambiguous figure: subjects reported either faces or vase perception in response to flashes of the faces-vase ambiguous figure. (C) Motion decision experiment: random dot motion was presented at motion coherence threshold and subjects decided trial by trial whether motion was coherent or random. In all experiments, trials followed at long and unpredictable intervals. In each experiment, the pre-stimulus BOLD signal (dotted vertical line marking stimulus onset) was examined as a function of perceptual outcome and sampled from accordingly specialized sensory areas. The corresponding regions of interest (early auditory cortex, FFA and hMT+, respectively) are presented on a canonical inflated cortical surface of the right hemisphere. In all experiments, higher pre-stimulus time course in the respective sensory region biased towards perceiving stimulus properties for which these regions are particularly sensitive. Error bars represent standard error across subjects. For more details see Hesselmann et al. (2008a,b); Sadaghiani et al. (2009).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2903187&req=5

Figure 3: Local spontaneous variations in ongoing activity of specialized sensory regions impact perception. The upper part illustrates the paradigm: (A) auditory detection experiment: in a free-response setting subjects detected an auditory target stimulus presented at perceptual threshold. (B) Perceptual decision on an ambiguous figure: subjects reported either faces or vase perception in response to flashes of the faces-vase ambiguous figure. (C) Motion decision experiment: random dot motion was presented at motion coherence threshold and subjects decided trial by trial whether motion was coherent or random. In all experiments, trials followed at long and unpredictable intervals. In each experiment, the pre-stimulus BOLD signal (dotted vertical line marking stimulus onset) was examined as a function of perceptual outcome and sampled from accordingly specialized sensory areas. The corresponding regions of interest (early auditory cortex, FFA and hMT+, respectively) are presented on a canonical inflated cortical surface of the right hemisphere. In all experiments, higher pre-stimulus time course in the respective sensory region biased towards perceiving stimulus properties for which these regions are particularly sensitive. Error bars represent standard error across subjects. For more details see Hesselmann et al. (2008a,b); Sadaghiani et al. (2009).

Mentions: Taken together, these observations could further support a simple dichotomy in which higher ongoing activity in “task-positive” brain networks would facilitate perceptual performance whereas higher activity levels in the default-mode network would degrade performance. A recent study speaks against the generality of this scenario by showing that functional context determines in which brain regions ongoing activity will affect perceptual performance and whether this will be a facilitating or detrimental effect (Sadaghiani et al., 2009). In a free-response, auditory detection task, we presented broad-band noise stimuli in unpredictable intervals of 20–40 s and at individual detection threshold. Subjects pressed a button whenever they perceived the target sound. Successful detection as compared to misses was preceded by significantly higher pre-stimulus activity in early auditory cortex (Figure 3A) as well as in two ICNs. Perceptual performance was better with higher pre-stimulus activity in a network comprising thalamus, anterior insula and dACC, which suggests a role for this ICN in maintaining alertness and task-set (Figure 2A). Conversely, and counter to common intuition, higher baseline activity in the dorsal attention system of parietal and frontal areas biased towards misses (Figure 2B) presumably expressing the lack of spatial connotation in our stimulus and task. The observation of opposite effects in these two task-positive ICNs shows that in spite of shared variance, the networks are sufficiently segregated to exert independent influences on perceptual outcome. And finally, higher baseline activity in the precuneus/PCC region of the default-mode network preceded hits, which in turn yielded a biphasic response with a “task-positive” activation component preceding the typical but delayed deactivation (Figure 2C). At first glance, this finding might appear at odds with the existing literature but it probably reflects the importance of retrieving a memory template of the target for successful performance on the continuous sensory input (Shannon and Buckner, 2004; Daselaar et al., 2009).


The relation of ongoing brain activity, evoked neural responses, and cognition.

Sadaghiani S, Hesselmann G, Friston KJ, Kleinschmidt A - Front Syst Neurosci (2010)

Local spontaneous variations in ongoing activity of specialized sensory regions impact perception. The upper part illustrates the paradigm: (A) auditory detection experiment: in a free-response setting subjects detected an auditory target stimulus presented at perceptual threshold. (B) Perceptual decision on an ambiguous figure: subjects reported either faces or vase perception in response to flashes of the faces-vase ambiguous figure. (C) Motion decision experiment: random dot motion was presented at motion coherence threshold and subjects decided trial by trial whether motion was coherent or random. In all experiments, trials followed at long and unpredictable intervals. In each experiment, the pre-stimulus BOLD signal (dotted vertical line marking stimulus onset) was examined as a function of perceptual outcome and sampled from accordingly specialized sensory areas. The corresponding regions of interest (early auditory cortex, FFA and hMT+, respectively) are presented on a canonical inflated cortical surface of the right hemisphere. In all experiments, higher pre-stimulus time course in the respective sensory region biased towards perceiving stimulus properties for which these regions are particularly sensitive. Error bars represent standard error across subjects. For more details see Hesselmann et al. (2008a,b); Sadaghiani et al. (2009).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2903187&req=5

Figure 3: Local spontaneous variations in ongoing activity of specialized sensory regions impact perception. The upper part illustrates the paradigm: (A) auditory detection experiment: in a free-response setting subjects detected an auditory target stimulus presented at perceptual threshold. (B) Perceptual decision on an ambiguous figure: subjects reported either faces or vase perception in response to flashes of the faces-vase ambiguous figure. (C) Motion decision experiment: random dot motion was presented at motion coherence threshold and subjects decided trial by trial whether motion was coherent or random. In all experiments, trials followed at long and unpredictable intervals. In each experiment, the pre-stimulus BOLD signal (dotted vertical line marking stimulus onset) was examined as a function of perceptual outcome and sampled from accordingly specialized sensory areas. The corresponding regions of interest (early auditory cortex, FFA and hMT+, respectively) are presented on a canonical inflated cortical surface of the right hemisphere. In all experiments, higher pre-stimulus time course in the respective sensory region biased towards perceiving stimulus properties for which these regions are particularly sensitive. Error bars represent standard error across subjects. For more details see Hesselmann et al. (2008a,b); Sadaghiani et al. (2009).
Mentions: Taken together, these observations could further support a simple dichotomy in which higher ongoing activity in “task-positive” brain networks would facilitate perceptual performance whereas higher activity levels in the default-mode network would degrade performance. A recent study speaks against the generality of this scenario by showing that functional context determines in which brain regions ongoing activity will affect perceptual performance and whether this will be a facilitating or detrimental effect (Sadaghiani et al., 2009). In a free-response, auditory detection task, we presented broad-band noise stimuli in unpredictable intervals of 20–40 s and at individual detection threshold. Subjects pressed a button whenever they perceived the target sound. Successful detection as compared to misses was preceded by significantly higher pre-stimulus activity in early auditory cortex (Figure 3A) as well as in two ICNs. Perceptual performance was better with higher pre-stimulus activity in a network comprising thalamus, anterior insula and dACC, which suggests a role for this ICN in maintaining alertness and task-set (Figure 2A). Conversely, and counter to common intuition, higher baseline activity in the dorsal attention system of parietal and frontal areas biased towards misses (Figure 2B) presumably expressing the lack of spatial connotation in our stimulus and task. The observation of opposite effects in these two task-positive ICNs shows that in spite of shared variance, the networks are sufficiently segregated to exert independent influences on perceptual outcome. And finally, higher baseline activity in the precuneus/PCC region of the default-mode network preceded hits, which in turn yielded a biphasic response with a “task-positive” activation component preceding the typical but delayed deactivation (Figure 2C). At first glance, this finding might appear at odds with the existing literature but it probably reflects the importance of retrieving a memory template of the target for successful performance on the continuous sensory input (Shannon and Buckner, 2004; Daselaar et al., 2009).

Bottom Line: Ongoing brain activity has been observed since the earliest neurophysiological recordings and is found over a wide range of temporal and spatial scales.We then highlight the flexibility and context-sensitivity of intrinsic functional connectivity that suggest its involvement in functionally relevant information processing.This role in information processing is pursued by reviewing how ongoing brain activity interacts with afferent and efferent information exchange of the brain with its environment.

View Article: PubMed Central - PubMed

Affiliation: Institut National de la Santé et de la Recherche Médicale Unité 992 Cognitive Neuroimaging Unit Gif-sur-Yvette, France.

ABSTRACT
Ongoing brain activity has been observed since the earliest neurophysiological recordings and is found over a wide range of temporal and spatial scales. It is characterized by remarkably large spontaneous modulations. Here, we review evidence for the functional role of these ongoing activity fluctuations and argue that they constitute an essential property of the neural architecture underlying cognition. The role of spontaneous activity fluctuations is probably best understood when considering both their spatiotemporal structure and their functional impact on cognition. We first briefly argue against a "segregationist" view on ongoing activity, both in time and space, which would selectively associate certain frequency bands or levels of spatial organization with specific functional roles. Instead, we emphasize the functional importance of the full range, from differentiation to integration, of intrinsic activity within a hierarchical spatiotemporal structure. We then highlight the flexibility and context-sensitivity of intrinsic functional connectivity that suggest its involvement in functionally relevant information processing. This role in information processing is pursued by reviewing how ongoing brain activity interacts with afferent and efferent information exchange of the brain with its environment. We focus on the relationship between the variability of ongoing and evoked brain activity, and review recent reports that tie ongoing brain activity fluctuations to variability in human perception and behavior. Finally, these observations are discussed within the framework of the free-energy principle which - applied to human brain function - provides a theoretical account for a non-random, coordinated interaction of ongoing and evoked activity in perception and behavior.

No MeSH data available.


Related in: MedlinePlus