Differences in Coupling Between Cortical Networks Related to Arousal in Neural Activity and Hemodynamics

Academic Background

In the absence of specific sensory inputs or behavioral tasks, the brain generates structured activity patterns. This organized activity is modulated by the state of arousal. The relationship between arousal and cortical activity is significant for understanding the function of neural networks. Previous studies have shown that arousal levels affect neural activity and hemodynamic changes, but it is still unclear whether these effects are consistent across different cortical areas and behavioral states.

Source of the Paper

This paper was authored by Lisa Meyer-Baese and colleagues from the Departments of Biomedical Engineering and Biology at Emory University and Georgia Tech. It was published in May 2024 in the Journal of Neuroscience.

Research Process

This study used wide-field voltage imaging technology to investigate how arousal states are related to spontaneous behavioral corticometric voltage and hemodynamic activities in head-fixed mice. The study included the following key steps:

Preparation of Animal Models and Imaging Techniques

Transgenic mice expressing voltage-sensitive fluorescent proteins (VSFP) were used, and the voltage and hemodynamic activities of head-fixed mice in the awake state were recorded using wide-field voltage imaging technology. The mice were placed in a restrained state, and fluorescence imaging was conducted using the VSFP-Butterfly sensor.

Data Collection and Processing

During the imaging experiments, facial video recordings were taken to track facial movements and pupil diameter changes. The analysis process distinguished between voltage signals and hemodynamic signals by performing gain correction on the fluorescence signals. The time series signals of each imaging experiment were filtered and decoupled to eliminate noise and non-physiological signals.

Validation of Voltage Imaging and Hemodynamic Signals

To validate the voltage and hemodynamic signals, air-puff stimuli were applied to the mice, and responses in the right barrel cortex were recorded. The signals associated with the air-puff stimuli showed expected characteristics: the voltage signals displayed a rapid biphasic response, while the hemodynamic signals showed a slower response. These results indicate that VSFP imaging technology can reliably capture neural activity and hemodynamic changes.

Main Findings of the Study

Arousal State and Global Cortical Signals

The study found that global voltage signals were significantly correlated with pupil diameter changes, with a peak correlation coefficient of approximately 0.5, while the correlation coefficient of global hemodynamic signals with pupil diameter changes was about 0.25. This suggests a closer coupling between cortical arousal and overall neural activity.

Regional Cortical Activity and Pupil Diameter Relationship

The correlations between voltage and hemodynamic signals and pupil diameter varied across different cortical regions. Voltage signals exhibited positive correlations with pupil diameter changes in most sensory-motor cortical areas, while negative correlations were observed in the prefrontal cortex. Similarly, hemodynamic signals showed positive correlations in sensory-motor cortical areas but weaker correlations in the prefrontal cortex.

Conclusions

This study demonstrates that the regulation of cortical networks by arousal state is dynamically variable, and that the functional networks of voltage and hemodynamic signals only partially overlap. The research reveals the differential impacts of arousal states on neural activity and hemodynamics at different frequencies, highlighting the need to consider behavioral state influences when interpreting hemodynamic signals.

Research Highlights

1. Technical Innovation: The use of wide-field voltage imaging technology in combination with the VSFP-Butterfly sensor enabled simultaneous recording of voltage activity and hemodynamic signals for the first time.

2. Complex Effects of Arousal: The study revealed the spatiotemporal dynamic regulation of cortical network voltage and hemodynamic activities by arousal, indicating differential coupling at different frequencies and behavioral states.

3. Regional Analysis: Specific analysis of the correlations between voltage and hemodynamic signals with states of arousal across different cortical regions provided deeper insights into functional networks.

Future Directions

Future research should further explore the effects of deconvolution methods on cerebral hemodynamics signals. Combining higher-frame-rate behavior tracking technology would enable capturing finer behavioral variations’ impact on cortical activity. Additionally, data processing strategies after removing global signals should be considered to better understand the intrinsic relationships between neural activity and hemodynamic signals. This study offers a new perspective on the dynamic regulation of brain functional networks by arousal states, emphasizing the necessity to consider behavioral states and frequency dependence in neuroimaging research.