In normal ageing, structural and functional changes in the brain lead to an altered processing of sensory stimuli and to changes in cognitive functions. The link between changes in sensory processing and cognition is not well understood, but physical fitness is suggested to be beneficial for both. We recorded event-related potentials to somatosensory and auditory stimuli in a passive change detection paradigm from 81 older and 38 young women and investigated their associations with cognitive performance. In older adults also associations to physical fitness were studied. The somatosensory mismatch response was attenuated in older adults and it associated with executive functions. Somatosensory P3a did not show group differences, but in older adults, it associated with physical fitness. Auditory N1 and P2 responses to repetitive stimuli were larger in amplitude in older than in young adults. There were no group differences in the auditory mismatch negativity, but it associated with working memory capacity in young but not in older adults. Our results indicate that in ageing, changes in stimulus encoding and deviance detection are observable in electrophysiological responses to task-irrelevant somatosensory and auditory stimuli, and the higher somatosensory response amplitudes are associated with better executive functions and physical fitness.

Key points Dentate spikes are fast fluctuations of hilar local‐field potentials that take place during rest and are thought to reflect input arriving from the entorhinal cortex to the hippocampus. During dentate spikes, neuronal firing in hippocampal input (dentate gyrus) and output (CA1/CA3) regions is uncoupled. To date, the behavioural significance of dentate spikes is unknown. Here, we provide evidence that disrupting the dentate spike‐related uncoupling of the dentate gyrus and the CA1/CA3 subregions for 1 h after training retards associative learning. We suggest dentate spikes play a significant role in memory consolidation. Abstract Hippocampal electrophysiological oscillations, namely theta and ripples, have been implicated in encoding and consolidation of new memories, respectively. According to existing literature, hippocampal dentate spikes are prominent, short‐duration (<30 ms), large‐amplitude (∼2–4 mV) fluctuations in hilar local‐field potentials that take place during awake immobility and sleep. Interestingly, previous studies indicate that during dentate spikes dentate gyrus granule cells increase their firing while firing of CA1 pyramidal cells are suppressed, thus resulting in momentary uncoupling of the two hippocampal subregions. To date, the behavioural significance of dentate spikes is unknown. Here, to study the possible role of dentate spikes in learning, we trained adult male Sprague–Dawley rats in trace eyeblink classical conditioning. For 1 h immediately following each conditioning session, one group of animals received hippocampal stimulation via the ventral hippocampal commissure (vHC) contingent on dentate spikes to disrupt the uncoupling between the dentate gyrus and the CA1 subregions. A yoked control group was stimulated during immobility, irrespective of brain state, and another control group was not stimulated at all. As a result, learning was impaired only in the group where vHC stimulation was administered contingent on dentate spikes. Our results suggest dentate spikes and/or the associated uncoupling of the dentate gyrus and the CA1 play a significant role in memory consolidation. Dentate spikes could possibly reflect reactivation and refinement of a memory trace within the dentate gyrus triggered by input from the entorhinal cortex.

Cardiac cycle phase is known to modulate processing of simple sensory information. This effect of the heartbeat on brain function is likely exerted via baroreceptors, the neurons sensitive for changes in blood pressure. From baroreceptors, the signal is conveyed all the way to the forebrain and the medial prefrontal cortex. In the two experiments reported, we examined whether learning, as a more complex form of cognition, can be modulated by the cardiac cycle phase. Human participants ( experiment 1) and rabbits ( experiment 2) were trained in trace eyeblink conditioning while neural activity was recorded. The conditioned stimulus was presented contingently with either the systolic or diastolic phase of the cycle. The tone used as the conditioned stimulus evoked amplified responses in both humans (electroencephalogram from "vertex," Cz) and rabbits (hippocampal CA1 local field potential) when its onset was timed at systole. In humans, the cardiac cycle phase did not affect learning, but rabbits trained at diastole learned significantly better than those trained at a random phase of the cardiac cycle. In summary, our results suggest that neural processing of external stimuli and also learning can be affected by targeting stimuli on the basis of cardiac cycle phase. These findings might be useful in applications aimed at maximizing or minimizing the effects of external stimulation. NEW & NOTEWORTHY It has been shown that rapid changes in bodily states modulate neural processing of external stimulus in brain. In this study, we show that modulation of neural processing of external stimulus and learning about it depends on the phase of the cardiac cycle. This is a novel finding that can be applied to optimize associative learning.

Rhythmic variation in heart rate and respiratory pattern are coupled in a way that optimizes the level of oxygen in the blood stream of the lungs and the body as well as saves energy in pulmonary gas exchange. It has been suggested that the cardiac cycle and respiratory pattern are coupled to neural oscillations of the brain. Yet, studies on how this rhythmic coupling is related to behavior are scarce. There is some evidence that, for example, the phase of respiration affects memory retrieval and the electrophysiological oscillatory state of the limbic system. It is also known that the phase of the cardiac cycle and hippocampal electrophysiological oscillations alone affect learning. Here, we studied whether the timing of training trials to different phases of respiration affects learning trace eyeblink conditioning in healthy adult humans. Trials consisting of a neutral conditioned stimulus (200‐ms tone) and a slightly aversive unconditioned stimulus (100‐ms air puff toward the eye), presented with a 600‐ms trace interval, were timed to either inspiration or expiration. A control group was trained regardless of respiratory phase. We found that, at the end of training, the rate of conditioned responses was higher in the group trained at expiration than it was in the other two groups. That is, brain state seems to fluctuate as a function of respiratory rhythm, and this fluctuation is also behaviorally relevant, exerting its effect on, at the least, a simple form of associative learning.

Hippocampal u (3 -12 Hz) oscillations are implicated in learning and memory, but their functional role remains unclear. We studied the effect of the phase of local u oscillation on hippocampal responses to a neutral conditioned stimulus (CS) and subsequent learning of classical trace eyeblink conditioning in adult rabbits. High-amplitude, regular hippocampal u-band responses (that predict good learning) were elicited by the CS when it was timed to commence at the fissure u trough (Trough group). Regardless, learning in this group was not enhanced compared with a yoked control group, possibly due to a ceiling effect. However, when the CS was consistently presented to the peak of u (Peak group), hippocampal u-band responding was less organized and learning was retarded. In well-trained animals, the hippocampal u phase at CS onset no longer affected performance of the learned response, suggesting a time-limited role for hippocampal processing in learning. To our knowledge, this is the first study to demonstrate that timing a peripheral stimulus to a specific phase of the hippocampal u cycle produces robust effects on the synchronization of neural responses and affects learning at the behavioral level. Our results support the notion that the phase of spontaneous hippocampal u oscillation is a means of regulating the processing of information in the brain to a behaviorally relevant degree.