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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

Delayed nonmatch-to-sample behavioral performance during vehicle and tetrahydrocannabinol (THC) sessions. Mean correct nonmatch responses summed across all rats (n = 10) shows the delay-dependent decline in performance under both conditions. A within subjects design with at least one non-drug day between THC administration was used. All animals were given THC (1.0–3.0 mg/kg) for at least five sessions spaced over consecutive weeks. Error bars indicate S.E.M.
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Figure 3: Delayed nonmatch-to-sample behavioral performance during vehicle and tetrahydrocannabinol (THC) sessions. Mean correct nonmatch responses summed across all rats (n = 10) shows the delay-dependent decline in performance under both conditions. A within subjects design with at least one non-drug day between THC administration was used. All animals were given THC (1.0–3.0 mg/kg) for at least five sessions spaced over consecutive weeks. Error bars indicate S.E.M.

Mentions: Hippocampal spike trains were recorded during a resting state condition in a neutral (i.e., task-independent) environment both before (pre) and after (post) the DNMS task (Figure 1A) to assess the influence that active memory processing (during the task) exerts on the structure of spike train variability, as indicated by multifractal analysis. This approach was designed to assess electrophysiologcal distinctions between three different recording phases (pre-task, task, post-task) and in two drug conditions. Since drug injections (pluronic vehicle or THC) were given immediately after the pre-task/pre-drug resting state recording phase, all computed measures for the pre-task phase are equal across the two drug conditions. THC, the main active ingredient in cannabis (Gaoni and Mechoulam, 1964), was chosen because it impairs memory encoding during the DNMS task (Hampson and Deadwyler, 1999, 2000), reduces LRTCs and multifractal complexity of task-related neuronal spike trains (Fetterhoff et al., 2015) and impairs theta frequency-related working memory performance in both rats (Robbe et al., 2006) and humans (Ilan et al., 2004; Böcker et al., 2010). THC doses were chosen to maximally impair DNMS performance in order to examine effects on associated multifractal spike train characteristics using previously established dose-response relationships (Hampson and Deadwyler, 2000). Working memory was assessed in 10 rats after vehicle or THC administration using the DNMS task (Figure 1B). A within subjects design was used to assess behavioral performance and hippocampal electrophysiology for 5–8 days per drug condition (vehicle or THC) per rat. The DNMS performance was inversely correlated with delay length, as all animals performed worse at longer delays (Figure 3). THC (green line) impaired performance compared to vehicle (Figure 3, blue line).


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)

Delayed nonmatch-to-sample behavioral performance during vehicle and tetrahydrocannabinol (THC) sessions. Mean correct nonmatch responses summed across all rats (n = 10) shows the delay-dependent decline in performance under both conditions. A within subjects design with at least one non-drug day between THC administration was used. All animals were given THC (1.0–3.0 mg/kg) for at least five sessions spaced over consecutive weeks. Error bars indicate S.E.M.
© Copyright Policy
Related In: Results  -  Collection

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

Figure 3: Delayed nonmatch-to-sample behavioral performance during vehicle and tetrahydrocannabinol (THC) sessions. Mean correct nonmatch responses summed across all rats (n = 10) shows the delay-dependent decline in performance under both conditions. A within subjects design with at least one non-drug day between THC administration was used. All animals were given THC (1.0–3.0 mg/kg) for at least five sessions spaced over consecutive weeks. Error bars indicate S.E.M.
Mentions: Hippocampal spike trains were recorded during a resting state condition in a neutral (i.e., task-independent) environment both before (pre) and after (post) the DNMS task (Figure 1A) to assess the influence that active memory processing (during the task) exerts on the structure of spike train variability, as indicated by multifractal analysis. This approach was designed to assess electrophysiologcal distinctions between three different recording phases (pre-task, task, post-task) and in two drug conditions. Since drug injections (pluronic vehicle or THC) were given immediately after the pre-task/pre-drug resting state recording phase, all computed measures for the pre-task phase are equal across the two drug conditions. THC, the main active ingredient in cannabis (Gaoni and Mechoulam, 1964), was chosen because it impairs memory encoding during the DNMS task (Hampson and Deadwyler, 1999, 2000), reduces LRTCs and multifractal complexity of task-related neuronal spike trains (Fetterhoff et al., 2015) and impairs theta frequency-related working memory performance in both rats (Robbe et al., 2006) and humans (Ilan et al., 2004; Böcker et al., 2010). THC doses were chosen to maximally impair DNMS performance in order to examine effects on associated multifractal spike train characteristics using previously established dose-response relationships (Hampson and Deadwyler, 2000). Working memory was assessed in 10 rats after vehicle or THC administration using the DNMS task (Figure 1B). A within subjects design was used to assess behavioral performance and hippocampal electrophysiology for 5–8 days per drug condition (vehicle or THC) per rat. The DNMS performance was inversely correlated with delay length, as all animals performed worse at longer delays (Figure 3). THC (green line) impaired performance compared to vehicle (Figure 3, blue line).

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