Neural Correlates of human cognitive abilities during sleep

Inter-individual differences in sleep spindles are highly correlated with “Reasoning” abilities (problem solving skills; i.e., the ability to employ logic, identify complex patterns), but not Short Term Memory or Verbal abilities. Simultaneous electroencephalography and functional magnetic resonance imaging (EEG-fMRI) have revealed brain activations time-locked to spindles (e.g., thalamic, paralimbic, and motor cortical areas)–yet the functional significance of inter-individual differences in spindle-related brain activation remains to be investigated. Using EEG-fMRI during sleep, we identified, for the first time, the neural activation patterns time-locked to spindles that are correlated with cognitive abilities. Similar to previous studies, activations time-locked to spindles were observed in thalamocortical circuitry and basal ganglia regions. Importantly, spindle-related activation in a subset of these regions were specifically related to inter-individual differences in Reasoning, but not STM or Verbal abilities. These results may help elucidate the physiological mechanisms which support the function of sleep for the capacity for reasoning.


INTRODUCTION
The sleep spindle is the only known spontaneous neural oscillation that has been identified 16 as an electrophysiological marker of cognitive abilities and aptitudes, that are typically assessed substrates that support spindle generation (e.g., thalamocortical circuitry) may be related to the 32 capacity for these cognitive skills. Interestingly, spindle production is reduced with age (Carrier  Relationship between sleep spindles and cognitive abilities 145 Standard multiple linear regression revealed that, taken together, Reasoning, Short Term were conducted for slow spindles at Fz and fast spindles at Pz, however, we did not observe 154 any significant relationship between spindles and cognitive abilities. 155 Reasoning ability, over-and-above STM and Verbal abilities with spindle amplitude during NREM2. 161 162 Activation of brain regions time-locked to spindles during NREM sleep 163 As shown in Figure 2A, activations time-locked to all spindles (11-16 Hz) at Cz during 164 NREM sleep, were observed in the thalamus/midbrain, the bilateral striatum (putamen/globus 165 pallidum and caudate), the medial frontal cortex, cerebellum, and the brain stem (cluster-level 166 FWE corrected p < 0.05, Table 4). These results were statistically robust, as it is worth noting 167 that even when a conservative whole-brain voxel-wise FWE statistical threshold correction (p 168 < 0.05) was used, activations remained statistically significant in the thalamus/midbrain, the 169 brainstem, the cerebellum, and the right putamen.  Given the two physiologically distinct spindles types (fast and slow), we also explored 177 the brain activations time-locked to fast (13.5-16 Hz) spindles and slow (11-13.5 Hz) spindles 178 during NREM sleep. As shown in Figure S1, activations time-locked to fast spindles at Pz 179 ( Figure S1A) and slow spindles at Fz ( Figure S1B) were very similar in most brain regions, 180 including the thalamus, the precuneus, and the cerebellum. There were no significant 181 differences between fast spindle and slow spindle-related activations.

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To examine the neural correlates of the relationship between sleep spindles and cognitive 185 abilities, we conducted whole-brain spatial correlation analyses between brain activation maps 186 time-locked to all spindles at Cz and the scores on the three cognitive factors (Reasoning, STM, 187 and Verbal abilities) assessed by the Cambridge Brain Sciences tests. As shown in Figure 2B, 188 Reasoning ability was significantly correlated with spindle-related activation maps in the 189 thalamus, bilateral putamen, brainstem/pons anterior cingulate cortex, the middle cingulate 190 cortex, the paracentral lobe, the posterior cingulate cortex, the precuneus, and bilateral 191 temporal lobe (see Table 5).   spindles. The same whole-brain spatial correlation analyses were conducted for fast spindle 207 and slow spindle activation maps, however, we did not observe significant correlations between 208 any cognitive ability and the activation maps for each individual spindle type.

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From Figure 2, we can see that there were several overlapping regions between the 210 spindle activation maps (Figure 2A) and the maps that show activations time-locked to spindles 211 that were correlated with Reasoning abilities (Figure 2B). The conjunction (at p < 0.001 using  Table 6).
216 Table 6. Conjunction between the spindle-related activation maps and the spindle-related activations correlated with reasoning abilities maps. (see Figure 2C)

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Finally, to ensure that activations time-locked to spindles were specific to spindles per se,  The results of the current study identified a correlation between Reasoning, but not Short  Intelligence Test, and also the WAIS-R (Gong et al., 2005). Taken together, these findings 308 suggest that the thalamus and prefrontal cortex region supports Reasoning abilities. The current study suggests that interindividual differences in spindle-related activation of these 328 regions are related to Reasoning ability. at Cz, and fast spindles (13.5-16 Hz) at Pz ( Table 2). Despite having no minimum detection criteria, the detection method employed here did not detect spindles lower than 0.2 sec, as 481 found in a previous validation study (Ray et al., 2015).

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Recording Parameters. Brain images were acquired using a 3.0T TIM TRIO magnetic