Abstract
The hippocampus and cerebellum are critically involved in trace eyeblink classical conditioning (EBCC). The mechanisms underlying the hippocampal-cerebellar interaction during this task are not well-understood, although hippocampal theta (3-7 Hz) oscillations are known to reflect a favorable state for EBCC. Two groups of rabbits received trace EBCC in which a brain-computer interface administered trials in either the explicit presence or absence of naturally occurring hippocampal theta. A high percentage of robust theta led to a striking enhancement of learning accompanied by rhythmic theta-band (6-7 Hz) oscillations in the interpositus nucleus (IPN) and cerebellar cortex that were time-locked both to hippocampal rhythms and sensory stimuli during training. Rhythmic oscillations were absent in the cerebellum of the non-theta group. These data strongly suggest a beneficial impact of theta-based coordination of hippocampus and cerebellum and, importantly, demonstrate that hippocampal theta oscillations can be used to index, and perhaps modulate, the functional properties of the cerebellum.
Highlights
N eurobiological oscillations act as timing signals in the brain, organizing and coordinating activity within and across different regions [1,2,3,4,5]
Trial 41 occurred on the first day of acquisition for Tϩ animals, while trial 174 typically occurred on day 4 for TϪ animals
The major findings of the current study are that the presence of pretrial hippocampal theta occurs in conjunction with a substantial increase in acquisition rate, accompanied by (i) amplitude modulation of cerebellar evoked responses to conditioning stimuli, (ii) cerebellar theta oscillations that are time-locked to the sensory stimuli in awake, behaving animals, and (iii) synchronization of hippocampal and cerebellar interpositus nucleus (IPN) and hemispheric lobule VI (HVI) local field potentials (LFPs) at 6–7 Hz theta frequency
Summary
N eurobiological oscillations act as timing signals in the brain, organizing and coordinating activity within and across different regions [1,2,3,4,5]. We report that pretrial hippocampal theta state predicts the synchronization of hippocampal (CA1) and cerebellar local field potentials (LFPs) into a rhythmic theta oscillation that accompanies a striking cognitive/behavioral benefit over non-theta conditioning. This finding supports a hypothesized role for theta in coordinating a widely distributed memory system for trace EBCC and demonstrates the effective use of a hippocampal BCI to modulate cerebellar responses to conditioning stimuli
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