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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

Average singularity spectra across recording phases and drug conditions. Average spectra were computed by averaging all neurons within the respective recording phase and drug condition. A total of 197 hippocampal neurons were recorded from 10 different rats. Each neuron was recorded from the same electrode over multiple days and multifractal analysis was performed on a total of 5143 individual ISI sequences. 771–1004 individual ISI sequences were averaged for each condition. The legend in the upper right corner of (A) holds true for all figures. (A) Average singularity spectra were obtained from all neurons recorded during their respective recording phase and drug condition. (B) Average singularity spectra from all recording phases during vehicle treatment are plotted for comparison. Neurons exhibit greater multifractal complexity (i.e., wider singularity spectra; wider range of Hölder exponents h) during the task compared to either resting state. Long-range temporal correlations, indicated by the Hurst exponent, which is closely related to the Hölder exponent at the apex of the singularity spectrum [where D(h) = 1], are stronger during the resting states compared to the task. (C) Average singularity spectra from both drug conditions during DNMS task recordings show that THC reduces multifractal complexity, as indicated by decreased singularity spectra width. (D) Average singularity spectra taken from post-task recording phases show that THC reduces LRTCs (i.e., decreased Hurst exponent) compared to vehicle recordings; this effect is seen as the leftward shift in the THC spectrum comapred to the vehicle one. Multifractal complexity was unchanged by THC during post-task recordings.
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Figure 5: Average singularity spectra across recording phases and drug conditions. Average spectra were computed by averaging all neurons within the respective recording phase and drug condition. A total of 197 hippocampal neurons were recorded from 10 different rats. Each neuron was recorded from the same electrode over multiple days and multifractal analysis was performed on a total of 5143 individual ISI sequences. 771–1004 individual ISI sequences were averaged for each condition. The legend in the upper right corner of (A) holds true for all figures. (A) Average singularity spectra were obtained from all neurons recorded during their respective recording phase and drug condition. (B) Average singularity spectra from all recording phases during vehicle treatment are plotted for comparison. Neurons exhibit greater multifractal complexity (i.e., wider singularity spectra; wider range of Hölder exponents h) during the task compared to either resting state. Long-range temporal correlations, indicated by the Hurst exponent, which is closely related to the Hölder exponent at the apex of the singularity spectrum [where D(h) = 1], are stronger during the resting states compared to the task. (C) Average singularity spectra from both drug conditions during DNMS task recordings show that THC reduces multifractal complexity, as indicated by decreased singularity spectra width. (D) Average singularity spectra taken from post-task recording phases show that THC reduces LRTCs (i.e., decreased Hurst exponent) compared to vehicle recordings; this effect is seen as the leftward shift in the THC spectrum comapred to the vehicle one. Multifractal complexity was unchanged by THC during post-task recordings.

Mentions: The singularity and frequency spectra for two different example neurons are shown in Figure 4 while the population singularity spectra are shown in Figure 5. Repeated measures ANOVA results from population analyses are briefly mentioned here and presented fully in the subsequent sections. The first example permits comparision of all three recording phases taken from vehicle treatment conditions (Figures 4A,B, 5B). One example neuron exhibits increased multifractal complexity during the DNMS compared to either resting state recordings (Figure 4A). The frequency spectra for this same neuron exhibits both delta and theta power in all recording phases (Figure 4B). This neuron illustrates the same effect found in the population (Figure 5B): multifractal complexity (width) increases from post-task to pre-task to task (Figure 7F) and LRTCs (Hurst exponent) are larger during the resting states (pre- and post-task) compared to the task (Figure 6F). Although the singularity spectra are discernable across task phases for this neuron, the frequency spectra were not (Figure 4B). However, the population analyses revealed increased theta power during vehicle resting state recordings (pre- and post-task) compared to vehicle task recordings (Figure 8E).


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)

Average singularity spectra across recording phases and drug conditions. Average spectra were computed by averaging all neurons within the respective recording phase and drug condition. A total of 197 hippocampal neurons were recorded from 10 different rats. Each neuron was recorded from the same electrode over multiple days and multifractal analysis was performed on a total of 5143 individual ISI sequences. 771–1004 individual ISI sequences were averaged for each condition. The legend in the upper right corner of (A) holds true for all figures. (A) Average singularity spectra were obtained from all neurons recorded during their respective recording phase and drug condition. (B) Average singularity spectra from all recording phases during vehicle treatment are plotted for comparison. Neurons exhibit greater multifractal complexity (i.e., wider singularity spectra; wider range of Hölder exponents h) during the task compared to either resting state. Long-range temporal correlations, indicated by the Hurst exponent, which is closely related to the Hölder exponent at the apex of the singularity spectrum [where D(h) = 1], are stronger during the resting states compared to the task. (C) Average singularity spectra from both drug conditions during DNMS task recordings show that THC reduces multifractal complexity, as indicated by decreased singularity spectra width. (D) Average singularity spectra taken from post-task recording phases show that THC reduces LRTCs (i.e., decreased Hurst exponent) compared to vehicle recordings; this effect is seen as the leftward shift in the THC spectrum comapred to the vehicle one. Multifractal complexity was unchanged by THC during post-task recordings.
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Related In: Results  -  Collection

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Figure 5: Average singularity spectra across recording phases and drug conditions. Average spectra were computed by averaging all neurons within the respective recording phase and drug condition. A total of 197 hippocampal neurons were recorded from 10 different rats. Each neuron was recorded from the same electrode over multiple days and multifractal analysis was performed on a total of 5143 individual ISI sequences. 771–1004 individual ISI sequences were averaged for each condition. The legend in the upper right corner of (A) holds true for all figures. (A) Average singularity spectra were obtained from all neurons recorded during their respective recording phase and drug condition. (B) Average singularity spectra from all recording phases during vehicle treatment are plotted for comparison. Neurons exhibit greater multifractal complexity (i.e., wider singularity spectra; wider range of Hölder exponents h) during the task compared to either resting state. Long-range temporal correlations, indicated by the Hurst exponent, which is closely related to the Hölder exponent at the apex of the singularity spectrum [where D(h) = 1], are stronger during the resting states compared to the task. (C) Average singularity spectra from both drug conditions during DNMS task recordings show that THC reduces multifractal complexity, as indicated by decreased singularity spectra width. (D) Average singularity spectra taken from post-task recording phases show that THC reduces LRTCs (i.e., decreased Hurst exponent) compared to vehicle recordings; this effect is seen as the leftward shift in the THC spectrum comapred to the vehicle one. Multifractal complexity was unchanged by THC during post-task recordings.
Mentions: The singularity and frequency spectra for two different example neurons are shown in Figure 4 while the population singularity spectra are shown in Figure 5. Repeated measures ANOVA results from population analyses are briefly mentioned here and presented fully in the subsequent sections. The first example permits comparision of all three recording phases taken from vehicle treatment conditions (Figures 4A,B, 5B). One example neuron exhibits increased multifractal complexity during the DNMS compared to either resting state recordings (Figure 4A). The frequency spectra for this same neuron exhibits both delta and theta power in all recording phases (Figure 4B). This neuron illustrates the same effect found in the population (Figure 5B): multifractal complexity (width) increases from post-task to pre-task to task (Figure 7F) and LRTCs (Hurst exponent) are larger during the resting states (pre- and post-task) compared to the task (Figure 6F). Although the singularity spectra are discernable across task phases for this neuron, the frequency spectra were not (Figure 4B). However, the population analyses revealed increased theta power during vehicle resting state recordings (pre- and post-task) compared to vehicle task recordings (Figure 8E).

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