Rapid changes in bodily and neural states affect learning

Abstract

Declarative memories consist of the past events and factual information that can be recalled. One of the most popular experimental paradigms used in studying long-term memory formation is classical conditioning. Trace conditioning is a hippocampus-dependent task where two separate sensory stimuli are presented in contingency but with a temporal gap between. In trace eyeblink conditioning a conditioned stimulus, usually a tone, is presented with a short silent period followed by an airpuff to the eye. In the beginning of the learning process the behavioral response to the airpuff is naturally a blink of an eye. After repeated trials the subject learns to shut the eyelid after perceiving the tone but timing it before the noxious airpuff. These are called the conditioned responses. Neural oscillations occurring in the hippocampus are connected to learning. In addition, hippocampal oscillations and some rapidly changing bodily states, such as the cardiac cycle and respiration pattern, have rhythmical coupling. In the studies reported here, rabbits and humans were trained in trace eyeblink conditioning in contingency with specific states of hippocampal theta oscillation, cardiac cycle and respiration. The neural processing of the external stimuli and behavioral learning was affected when the conditioned stimulus was presented during different phases of hippocampal theta oscillation. Next, we showed that processing of responses evoked by an external stimulus was modulated differently in the cortex and in the hippocampus when the conditioned stimulus was presented either at the diastolic or systolic phase of the cardiac cycle. Learning was enhanced if the conditioned stimulus was presented during the diastolic phase. Finally, we showed that timing the whole conditioning trial to the expiration phase was optimal for learning. The findings of these studies are novel and suggest that not only the rapid changes in neural states but also bodily states are connected and have an impact on learning and the neural processing of the perceived external world. The aforementioned effects of bidirectional coupling of bodily states and the limbic system and, thus, the modulation of stimulus processing should be considered in electrophysiological measurements and experimental psychology. Furthermore, timing the presentation of significant stimulus to noninvasively monitored specific bodily states could be used to facilitate learning in cognitively demanding tasks.