Behaviourally modulated hippocampal theta oscillations in the ferret persist during both locomotion and immobility

Abstract

Theta oscillations are a hallmark of hippocampal activity across mammals and play a critical role in many hippocampal models of memory and spatial navigation. To reconcile the cross-species differences observed in the presence and properties of theta, we recorded hippocampal local field potentials in rats and ferrets during auditory and visual localisation tasks designed to vary locomotion and sensory attention. Here, we show that theta oscillations occur during locomotion in both ferrets and rats, however during periods of immobility, theta oscillations persist in the ferret, contrasting starkly with the switch to large irregular activity (LIA) in the rat. Theta during immobility in the ferret is identified as analogous to Type 2 theta that has been observed in rodents due to its sensitivity to atropine, and is modulated by behavioural state with the strongest theta observed during reward epochs. These results demonstrate that even under similar behavioural conditions, differences exist between species in the relationship between theta and behavioural state.

Frequency matters: how changes in hippocampal theta frequency can influence temporal coding, anxiety-reduction, and memory

“…Species differences in hippocampal theta do occur across different mammalian species. For instance, compared to rodents, theta is more prevalent in the ferret (Dunn et al, 2022), and less so in humans; however more insight is emerging into human theta via intracranial recordings and MEG. We anticipate such studies will likely reveal broadly similar theta-slope "stimulus rate" frequency correlates (Santos-Pata et al, 2022), and theta-intercept "baseline" frequency correlates, as obtained in locomoting rodents.…”

Learning to predict future locations with internally generated theta sequences

“…Theta frequency has also been shown to increase modestly with speed (by about 1 or 2 Hz within the range of speeds assessed in experiments; [ 76 – 78 ]), or perhaps with acceleration [ 79 ], but see [ 80 ]. However, there appear to be compensatory mechanisms in place such that changes in theta frequency do not affect the theta phase code [ 15 , 70 – 72 , 81 , 82 ].…”

Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movement

“…a rat having visual contact with the movement of a cat 17,18 . Since such alert immobility is not obviously different from the movement arrest induced by optogenetic stimulation in the PPN, it is not unlikely that theta rhythm could remain during PPN stimulation, especially the type-2 theta rhythm 13,53 .…”

“…A part of the brain, which is known to have a central role in both memories of events and spatial navigation is the hippocampus 7,8 . A prominent feature of the hippocampus is the strong concerted rhythmic activity, known as the theta rhythm (6-9 Hz in rats), which is prominent, especially during movement, locomotion [11][12][13] as well as the acceleration of the body 51 . It often appears together with a widespread desynchronization of cortical electroencephalography (EEG) and was therefore suggested early on to be involved in arousal 14 .…”