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Distinguishing cognitive state with multifractal complexity of hippocampal interspike interval sequences.

Fetterhoff D, Kraft RA, Sandler RA, Opris I, Sexton CA, Marmarelis VZ, Hampson RE, Deadwyler SA - Front Syst Neurosci (2015)

Bottom Line: Our results demonstrate that multifractal firing patterns of hippocampal spike trains are a marker of functional memory processing, as they are more complex during the working memory task and significantly reduced following administration of memory impairing THC doses.These results showed that LRTCs, multifractality, and theta rhythm represent independent processes, while delta rhythm correlated with multifractality.Taken together, these results provide a novel perspective on memory function by demonstrating that the multifractal nature of spike trains reflects hippocampal microcircuit activity that can be used to detect and quantify cognitive, physiological, and pathological states.

View Article: PubMed Central - PubMed

Affiliation: Neuroscience Program, Wake Forest School of Medicine Winston-Salem, NC, USA ; Department of Physiology and Pharmacology, Wake Forest School of Medicine Winston-Salem, NC, USA.

ABSTRACT
Fractality, represented as self-similar repeating patterns, is ubiquitous in nature and the brain. Dynamic patterns of hippocampal spike trains are known to exhibit multifractal properties during working memory processing; however, it is unclear whether the multifractal properties inherent to hippocampal spike trains reflect active cognitive processing. To examine this possibility, hippocampal neuronal ensembles were recorded from rats before, during and after a spatial working memory task following administration of tetrahydrocannabinol (THC), a memory-impairing component of cannabis. Multifractal detrended fluctuation analysis was performed on hippocampal interspike interval sequences to determine characteristics of monofractal long-range temporal correlations (LRTCs), quantified by the Hurst exponent, and the degree/magnitude of multifractal complexity, quantified by the width of the singularity spectrum. Our results demonstrate that multifractal firing patterns of hippocampal spike trains are a marker of functional memory processing, as they are more complex during the working memory task and significantly reduced following administration of memory impairing THC doses. Conversely, LRTCs are largest during resting state recordings, therefore reflecting different information compared to multifractality. In order to deepen conceptual understanding of multifractal complexity and LRTCs, these measures were compared to classical methods using hippocampal frequency content and firing variability measures. These results showed that LRTCs, multifractality, and theta rhythm represent independent processes, while delta rhythm correlated with multifractality. Taken together, these results provide a novel perspective on memory function by demonstrating that the multifractal nature of spike trains reflects hippocampal microcircuit activity that can be used to detect and quantify cognitive, physiological, and pathological states.

No MeSH data available.


Related in: MedlinePlus

Summary of how multifractal complexity relates to memory processing. Hypothetical singularity spectra were constructed based on the qualitative results of the study. The gray spectrum represents the maximal amount of multifractal complexity possible in a system (i.e., hippocampal spike trains in this example). Active memory processing recruits a large portion of this potential, but additional resources are still available to support more cognitively demanding instances. THC impaired working memory and reduced multifractal complexity. During resting conditions, the singularity spectrum shrinks compared to the task (blue) condition. Multifractality may be highest when embedded information relevant for working memory is being processed. Consequently, resting and pharmacological impairment could reduce multifractal complexity by decreasing the fraction of utilized resources.
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Figure 10: Summary of how multifractal complexity relates to memory processing. Hypothetical singularity spectra were constructed based on the qualitative results of the study. The gray spectrum represents the maximal amount of multifractal complexity possible in a system (i.e., hippocampal spike trains in this example). Active memory processing recruits a large portion of this potential, but additional resources are still available to support more cognitively demanding instances. THC impaired working memory and reduced multifractal complexity. During resting conditions, the singularity spectrum shrinks compared to the task (blue) condition. Multifractality may be highest when embedded information relevant for working memory is being processed. Consequently, resting and pharmacological impairment could reduce multifractal complexity by decreasing the fraction of utilized resources.

Mentions: Learning and memory require information to be carried from the past into the future, and multifractal complexity of hippocampal neurons may fluctuate depending on how strongly information is received, processed and sent by these neurons. To put our results into a more general perspective, hypothetical singularity spectra were constructed to match our qualitative findings with respect to memory processing (Figure 10). We hypothesize that physiological states are characterized by specific monofractal and multifractal features. All different states must fall within a range of possible dynamics (Figure 10, gray spectrum) and thus a range of possible multifractality. Active memory processing (Figure 10, blue) recruits this system to a stronger degree than resting (Figure 10, orange) and therefore neurons recorded during the task exhibit stronger multifractality. This multifractality may facilitate memory processing by offering a larger range of spike train variability and greater processing capacity. When THC or other memory impairing agents are administered during the task (Figure 10, green), the normal level of multifractal complexity exhibited is reduced and memory performance suffers. Alterations in multifractal complexity may reflect the degree of presently embedded information and therefore would provide information relevant for detection of physiological state.


Distinguishing cognitive state with multifractal complexity of hippocampal interspike interval sequences.

Fetterhoff D, Kraft RA, Sandler RA, Opris I, Sexton CA, Marmarelis VZ, Hampson RE, Deadwyler SA - Front Syst Neurosci (2015)

Summary of how multifractal complexity relates to memory processing. Hypothetical singularity spectra were constructed based on the qualitative results of the study. The gray spectrum represents the maximal amount of multifractal complexity possible in a system (i.e., hippocampal spike trains in this example). Active memory processing recruits a large portion of this potential, but additional resources are still available to support more cognitively demanding instances. THC impaired working memory and reduced multifractal complexity. During resting conditions, the singularity spectrum shrinks compared to the task (blue) condition. Multifractality may be highest when embedded information relevant for working memory is being processed. Consequently, resting and pharmacological impairment could reduce multifractal complexity by decreasing the fraction of utilized resources.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4585000&req=5

Figure 10: Summary of how multifractal complexity relates to memory processing. Hypothetical singularity spectra were constructed based on the qualitative results of the study. The gray spectrum represents the maximal amount of multifractal complexity possible in a system (i.e., hippocampal spike trains in this example). Active memory processing recruits a large portion of this potential, but additional resources are still available to support more cognitively demanding instances. THC impaired working memory and reduced multifractal complexity. During resting conditions, the singularity spectrum shrinks compared to the task (blue) condition. Multifractality may be highest when embedded information relevant for working memory is being processed. Consequently, resting and pharmacological impairment could reduce multifractal complexity by decreasing the fraction of utilized resources.
Mentions: Learning and memory require information to be carried from the past into the future, and multifractal complexity of hippocampal neurons may fluctuate depending on how strongly information is received, processed and sent by these neurons. To put our results into a more general perspective, hypothetical singularity spectra were constructed to match our qualitative findings with respect to memory processing (Figure 10). We hypothesize that physiological states are characterized by specific monofractal and multifractal features. All different states must fall within a range of possible dynamics (Figure 10, gray spectrum) and thus a range of possible multifractality. Active memory processing (Figure 10, blue) recruits this system to a stronger degree than resting (Figure 10, orange) and therefore neurons recorded during the task exhibit stronger multifractality. This multifractality may facilitate memory processing by offering a larger range of spike train variability and greater processing capacity. When THC or other memory impairing agents are administered during the task (Figure 10, green), the normal level of multifractal complexity exhibited is reduced and memory performance suffers. Alterations in multifractal complexity may reflect the degree of presently embedded information and therefore would provide information relevant for detection of physiological state.

Bottom Line: Our results demonstrate that multifractal firing patterns of hippocampal spike trains are a marker of functional memory processing, as they are more complex during the working memory task and significantly reduced following administration of memory impairing THC doses.These results showed that LRTCs, multifractality, and theta rhythm represent independent processes, while delta rhythm correlated with multifractality.Taken together, these results provide a novel perspective on memory function by demonstrating that the multifractal nature of spike trains reflects hippocampal microcircuit activity that can be used to detect and quantify cognitive, physiological, and pathological states.

View Article: PubMed Central - PubMed

Affiliation: Neuroscience Program, Wake Forest School of Medicine Winston-Salem, NC, USA ; Department of Physiology and Pharmacology, Wake Forest School of Medicine Winston-Salem, NC, USA.

ABSTRACT
Fractality, represented as self-similar repeating patterns, is ubiquitous in nature and the brain. Dynamic patterns of hippocampal spike trains are known to exhibit multifractal properties during working memory processing; however, it is unclear whether the multifractal properties inherent to hippocampal spike trains reflect active cognitive processing. To examine this possibility, hippocampal neuronal ensembles were recorded from rats before, during and after a spatial working memory task following administration of tetrahydrocannabinol (THC), a memory-impairing component of cannabis. Multifractal detrended fluctuation analysis was performed on hippocampal interspike interval sequences to determine characteristics of monofractal long-range temporal correlations (LRTCs), quantified by the Hurst exponent, and the degree/magnitude of multifractal complexity, quantified by the width of the singularity spectrum. Our results demonstrate that multifractal firing patterns of hippocampal spike trains are a marker of functional memory processing, as they are more complex during the working memory task and significantly reduced following administration of memory impairing THC doses. Conversely, LRTCs are largest during resting state recordings, therefore reflecting different information compared to multifractality. In order to deepen conceptual understanding of multifractal complexity and LRTCs, these measures were compared to classical methods using hippocampal frequency content and firing variability measures. These results showed that LRTCs, multifractality, and theta rhythm represent independent processes, while delta rhythm correlated with multifractality. Taken together, these results provide a novel perspective on memory function by demonstrating that the multifractal nature of spike trains reflects hippocampal microcircuit activity that can be used to detect and quantify cognitive, physiological, and pathological states.

No MeSH data available.


Related in: MedlinePlus