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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

Rest (pre/post) and Delayed Nonmatch-to-Sample (DNMS) task recording paradigm. (A) Prior to each testing session, all rats were recorded in a white, rectangular plastic box for 25–30 min (pre-task recording). Upon completion of pre-task recording phase, the same rats were injected with either vehicle or delta-9-tetrahydrocannabinol (THC) 5–10 min before the start of delayed nonmatch-to-sample (DNMS) task. Immediately after completing the DNMS task, rats were put back into the same plastic chamber for another 25–30 min recording (post-task recording). (B) Progression of the DNMS task is illustrated. A 10 s Intertrial Interval (ITI) precedes the Sample Presentation (SP). Rats must make the Sample Response (SR) and remember the lever position throughout the variable 1–30 s delay that terminates after the Last Nosepoke (LNP). The LNP signals extension of both levers and rats receive a water reward (reinforcement) for appropriately making a Nonmatch Response (NR).
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Figure 1: Rest (pre/post) and Delayed Nonmatch-to-Sample (DNMS) task recording paradigm. (A) Prior to each testing session, all rats were recorded in a white, rectangular plastic box for 25–30 min (pre-task recording). Upon completion of pre-task recording phase, the same rats were injected with either vehicle or delta-9-tetrahydrocannabinol (THC) 5–10 min before the start of delayed nonmatch-to-sample (DNMS) task. Immediately after completing the DNMS task, rats were put back into the same plastic chamber for another 25–30 min recording (post-task recording). (B) Progression of the DNMS task is illustrated. A 10 s Intertrial Interval (ITI) precedes the Sample Presentation (SP). Rats must make the Sample Response (SR) and remember the lever position throughout the variable 1–30 s delay that terminates after the Last Nosepoke (LNP). The LNP signals extension of both levers and rats receive a water reward (reinforcement) for appropriately making a Nonmatch Response (NR).

Mentions: The DNMS task consisted of three main phases: Sample, Delay and Nonmatch (Figure 1B). The Sample phase initiated the trial via presentation of either the left or right lever (50% probability), which required the animal to press and make the Sample Response (SR). The lever was then retracted and the Delay phase of the task initiated, as signaled by the illumination of a cue light over a nosepoke photocell device on the wall opposite to where the lever was presented. At least one nosepoke (NP) was required following the interposed delay interval which varied randomly in duration (1–30 s) on each trial during the session. The Nonmatch phase began when the delay timed out, the photocell cue light turned off, and both the left and right levers on the front panel were extended. Correct responses consisted of pressing the lever in the Nonmatch phase located in the spatial position opposite to the position of the SR; in other words, a Nonmatch response (NR). This produced delivery of a 0.4 ml water reward in a reservoir between the two levers. After the NR the levers were retracted for a 10.0 s intertrial interval (ITI) before the Sample lever for the next trial was presented. A lever press at the same position as the SR (match response) constituted an “error” with no water delivery and turned off chamber house lights for 5.0 s with the next trial presented 5.0 s later. Individual performance was assessed as % NRs (correct responses) with respect to the total number of trials (80–100) per daily (1 h) session.


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)

Rest (pre/post) and Delayed Nonmatch-to-Sample (DNMS) task recording paradigm. (A) Prior to each testing session, all rats were recorded in a white, rectangular plastic box for 25–30 min (pre-task recording). Upon completion of pre-task recording phase, the same rats were injected with either vehicle or delta-9-tetrahydrocannabinol (THC) 5–10 min before the start of delayed nonmatch-to-sample (DNMS) task. Immediately after completing the DNMS task, rats were put back into the same plastic chamber for another 25–30 min recording (post-task recording). (B) Progression of the DNMS task is illustrated. A 10 s Intertrial Interval (ITI) precedes the Sample Presentation (SP). Rats must make the Sample Response (SR) and remember the lever position throughout the variable 1–30 s delay that terminates after the Last Nosepoke (LNP). The LNP signals extension of both levers and rats receive a water reward (reinforcement) for appropriately making a Nonmatch Response (NR).
© Copyright Policy
Related In: Results  -  Collection

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

Figure 1: Rest (pre/post) and Delayed Nonmatch-to-Sample (DNMS) task recording paradigm. (A) Prior to each testing session, all rats were recorded in a white, rectangular plastic box for 25–30 min (pre-task recording). Upon completion of pre-task recording phase, the same rats were injected with either vehicle or delta-9-tetrahydrocannabinol (THC) 5–10 min before the start of delayed nonmatch-to-sample (DNMS) task. Immediately after completing the DNMS task, rats were put back into the same plastic chamber for another 25–30 min recording (post-task recording). (B) Progression of the DNMS task is illustrated. A 10 s Intertrial Interval (ITI) precedes the Sample Presentation (SP). Rats must make the Sample Response (SR) and remember the lever position throughout the variable 1–30 s delay that terminates after the Last Nosepoke (LNP). The LNP signals extension of both levers and rats receive a water reward (reinforcement) for appropriately making a Nonmatch Response (NR).
Mentions: The DNMS task consisted of three main phases: Sample, Delay and Nonmatch (Figure 1B). The Sample phase initiated the trial via presentation of either the left or right lever (50% probability), which required the animal to press and make the Sample Response (SR). The lever was then retracted and the Delay phase of the task initiated, as signaled by the illumination of a cue light over a nosepoke photocell device on the wall opposite to where the lever was presented. At least one nosepoke (NP) was required following the interposed delay interval which varied randomly in duration (1–30 s) on each trial during the session. The Nonmatch phase began when the delay timed out, the photocell cue light turned off, and both the left and right levers on the front panel were extended. Correct responses consisted of pressing the lever in the Nonmatch phase located in the spatial position opposite to the position of the SR; in other words, a Nonmatch response (NR). This produced delivery of a 0.4 ml water reward in a reservoir between the two levers. After the NR the levers were retracted for a 10.0 s intertrial interval (ITI) before the Sample lever for the next trial was presented. A lever press at the same position as the SR (match response) constituted an “error” with no water delivery and turned off chamber house lights for 5.0 s with the next trial presented 5.0 s later. Individual performance was assessed as % NRs (correct responses) with respect to the total number of trials (80–100) per daily (1 h) session.

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